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Vol. 58, No. 4
MICROBIOLOGICAL REVIEWS, Dec. 1994, p. 700-754
0146-0749/94/$04.00+0
Copyright © 1994, American Society for Microbiology
Chloroplast Ribosomes and Protein Synthesis
ELIZABETH H. HARRIS,`* JOHN E. BOYNTON,' AND NICHOLAS W. GILLHAM2
DCMB Group, Departments of Botany' and Zoology,2 Duke University, Durham, North Carolina 27708-1000
.700
ORIGIN OF CHLOROPLASTS................................................................
CHLOROPLAST GENOME STRUCTURE AND GENE CONTENT..
THE PROCESS OF CHLOROPLAST PROTEIN SYNTHESIS...........
-s
F'
-
..................
704
Phylogenetic Conservation ........................
General Characteristics of Chloroplast rRNA Gene Organization .........................................*707
...........................
..................
707
16S rRNA .....................................................................
23S rRNA ..................................................................... 709
5S rRNA ..................................................................o.. 709
709
Introns in rRNA Genes .....................................................................
712
The 16S-23SSpacer ....................................................................
712
tRNAs Flanking the rRNA Operons.....................................................................
...2.0..................712
Antibiotic Resistance Mutations in the Chloroplast rRNA Genes ......................1..
714
RIBOSOMAL PROTEINS .....................................
714
Number and Nomenclature .....................................................................
715
Organization of Chloroplast Ribosomal Protein Genes ....................................... ............*.................
716
Correspondence of Chloroplast Ribosomal Proteins to Bacterial Ribosomal Proteins ................ ...............
716
Proteins of the Small Subunit................................
726
Proteins of the Large Subunit.
Chloroplast Ribosomal Proteins with No Obvious Homology to Those of E. coli
. 729
........................30
Comparative Analysis of Ribosomal Proteins ...............................
ASSEMBLY OF CHLOROPLAST RIBOSOMES ..................................................................... 730
SYNTHESIS OF THE COMPONENTS OF CHLOROPLAST RIBOSOMES .............................................., 731
731
Transcription of rRNA
Transcription of Chloroplast Genes Encoding Ribosomal Proteins ..................................................................... 732
..........733
Posttranscriptional Regulatory Mechanisms Affecting Chloroplast mRNAs ..........................
Membrane Binding of Chloroplast Ribosomes ..................................................................... 733
734
HOW ESSENTIAL IS CHLOROPLAST PROTEIN SYNTHESIS?...........-..................'...............
735
CONCLUSIONS .....................................................................
735
.......................
ACKNOWLEDGMENTS.
73
REFERENCES ....................
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Genes..................................................................
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among these various taxa have produced intriguing directions
for future evolutionary studies, while analysis of ribosomal
protein sequences, particularly among the diverse algal groups,
promises. to be a valuable tool for determining conserved
regions likely to have essential functions in ribosome assembly
or protein synthesis.
ORIGIN OF CHLOROPLASTS
Chloroplasts and mitochondria contain protein synthesizingsystems more similar to those of bacteria than to those of the
eukaryotic cytoplasm, consistent with the hypothesis that these
organelles had xenogenous (endosymbiotic) rather than autogenous (intracellular differentiation) origins (see. references 5,
205, 220-223, 274, 633, and 694 for discussions). Phylogenies
based mostly on rRNA sequences indicate that the cyanobacteria are ancestral to chloroplasts while the members of the
alpha subdivision of the purple sulfur bacteria are the likely
progenitors of mitochondria (221, 222). Whether the, chlorophyte algae and land plants on the one hand, and the rhodophyte, chromophyte, and euglenoid algae on the other represent more than one endosymbiotic event remains unresolved
(130, 403, 434). Comparisons of gene order and arrangement
CHLOROPLAST GENOME STRUCTURE AND
GENE CONTENT
Unlike their prokaryotic ancestors, neither chloroplasts nor
mitochondria are genetically autonomous, and information
specifying components of the organelle protein synthesizing
systems is divided between organelle and nucleus. Separation
of the genes encoding these RNAs and proteins between two
discrete cellular compartments suggests that mechanisms must
have evolved to coordinate expression of these genes so that
protein synthesis in the organelle can proceed efficiently.
Whereas chloroplast genomes of land plants usually have a
common organization and gene content, a great deal more
variability is encountered among the algae, particularly with
*
Corresponding author. Mailing address: DCMB, Duke University
Box 91000, Durham, NC 27708-1000. Phone: (919) 613-8164. Fax:
(919) 613-8177. Electronic mail address: [email protected].
700
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..700
..702
.....................................................................................................................................t.a..i.....n.... ... .....1....'rnl
Initiation
kElongation.........417d 0304
A
704
Chloroplast tRNAs and Aminoacyl-tRNA Synthetases .....................................................................
704
PLASTID GENES FOR rRNAs ...................................................
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
VOL. 58, 1994
encoding ribosomal proteins. Gene locations
are
from reference 560.
regard to the ribosomal protein genes that have been retained
in the organelle. In this section we review the chloroplast
genome structure
of land plants and the algal genera that have
been investigated to date with respect to composition and
organization of genes encoding rRNAs and ribosomal proteins.
Chloroplasts are highly polyploid organelles containing circular DNA molecules of 85 to 200 kb organized into discrete
membrane-associated nucleoids (see references 50, 206, 260,
337, 482, 483, 558, 613, and 614 for reviews). Three land plant
chloroplast genomes have been completely sequenced: the
dicotyledon tobacco (Nicotiana tabacum, 156 kb [560, 561]),
the monocotyledon rice (Oryza sativa, 135 kb [265]); and a
liverwort (Marchantia polymorpha, 121 kb [471-473]). Each
contains 110 to 120 genes (482, 614). These sequences, as well
as restriction maps and partial sequences from many other
species, indicate that the basic chloroplast genome structure
and overall gene order in land plants are highly conserved.
Although green algae (Chlorophyta) are regarded as ancestral
to land plants, modern green algae often show substantial
rearrangements in chloroplast gene order (see below). Other
of algae (Rhodophyta, Euglenophyta, Chromophyta)
show even more diversity in gene content and organization.
In the typical land plant chloroplast genome, unique sequence regions of 15 to 25 kb and 80 to 100 kb are separated
groups
by the two copies of an inverted repeat, which is usually 20 to
30 kb in size and contains genes encoding the chloroplast
rRNAs, certain tRNAs, and often one or more genes specifying proteins (Fig. 1) (see references 482 and 614 for reviews).
Within the inverted repeat, the rRNA operon is usually
oriented with the 23S rRNA gene closer to the small singlecopy region and the 16S rRNA gene closer to the large
single-copy region. The two repeats are identical in sequence
as a consequence of an active copy correction system (50).
Nearly two-thirds of the variation in size among land plant
chloroplast genomes (120 to 216 kb) is accounted for by
expansion or contraction of the inverted repeat (482). The
smallest chloroplast genomes among land plants are seen in
conifers (355, 600, 695) and in six tribes of the legume family
Fabaceae (314, 482, 487), which have lost the inverted repeat
and thus contain only a single copy of each of the rRNA genes.
Black pine (Pinus thunbergii) chloroplast DNA does possess a
short inverted repeat sequence, which contains a tRNA gene
and part of the 3' portion of the psbA gene, but not the rRNA
genes (654). In contrast, species with the largest chloroplast
genomes often have expanded inverted repeats (e.g., Pelargonium hortorum has a 76-kb inverted repeat encompassing
nearly half of the 216-kb chloroplast genome, in which many
genes normally in the single-copy region have been duplicated
[482]).
Chloroplast genomes from land plants specify a relatively
constant set of components for the protein-synthesizing machinery of the organelle (4 rRNAs, 30 to 31 tRNAs, 21
ribosomal proteins, and 4 RNA polymerase subunits) and for
photosynthesis (28 thylakoid proteins plus 1 soluble protein,
the ribulose-1,5-bisphosphate carboxylase/oxygenase [Rubisco]
large subunit). In addition, homologs of 11 subunits of mammalian mitochondrial complex I (the ndh genes) have now
been found to be encoded by chloroplast DNA in flowering
plants and Marchantia species (9,713). Chloroplast genomes of
gymnosperms, liverworts, and algae (e.g., Chlamydomonas
reinhardtii) which synthesize chlorophyll in darkness possess
genes encoding three subunits of a light-independent protochlorophyllide reductase that is also found in photosynthetic
prokaryotes (see reference 367 for a summary). These genes
are absent from the tobacco and rice chloroplast genomes.
Mapping and sequencing studies of chloroplast genomes
from widely different algal taxa reveal that these are much
more variable in organization and gene content than those of
land plants. The well-characterized chloroplast genomes of
three species of unicellular green algae in the genus Chlamydomonas are substantially larger (C. reinhardtii, 196 kb; C.
eugametos, 243 kb; C. moewusii, 292 kb) than the chloroplast
genomes of land plants (42, 43, 50, 247). In these species the
two copies of the large inverted repeat encoding the rRNAs
are separated by unique sequence regions of roughly equal
size. Chloroplast genes in Chlamydomonas species are also
extensively rearranged between distantly related species and
with respect to land plants (43). The green alga Spirogyra
maxima, in the charophyte lineage presumed to be ancestral to
land plants, lacks an inverted repeat and shows altered gene
order relative to land plants (352, 393).
The organization, structure, and gene content of the completely sequenced 145-kb chloroplast genome of Euglena gracilis Z (243) depart markedly from the chloroplast genomes of
chlorophyte algae or land plants. In this Euglena strain and in
its colorless relative Astasia longa, the plastid genome contains
three tandemly repeated rRNA operons plus an additional 16S
gene or fragment thereof (288, 289, 315-317, 478, 569).
Euglena gracilis var. bacillaris has only a single complete rRNA
operon (720). Most of the Euglena chloroplast tRNA genes are
grouped in tight clusters of two to five genes, whereas they tend
to be scattered in plastid genomes of land plants. While most
protein-coding chloroplast genes in land plants or Chlamydomonas species are uninterrupted or contain at most one or two
introns, comparable genes in Euglena gracilis each contain
multiple introns (243, 482). However, several chloroplast
tRNA genes that have introns in land plants lack introns in
Euglena or Chlamydomonas species (331). A number of other
genes found in land plant chloroplast genomes, including three
genes encoding ribosomal proteins, are missing from the
Euglena chloroplast genome (see below), but this algal genome
also contains some genes not found in plastid genomes of land
plants.
The plastid of Cyanophora paradoxa is often referred to as
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FIG. 1. Schematic diagram of a typical land plant chloroplast
showing the positions of the inverted repeat, rRNA
genome (tobacco),
genes, and genes
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HARRIS ET AL.
MICROBIOL. REV.
chloroplast protein synthesis has been presented by Steinmetz
and Weil (593).
has now been sequenced (32, 598). This genome contains an
inverted repeat which encodes the cyanelle rRNAs and several
other genes. Although the gene content of the cyanelle generally resembles that of land plant chloroplasts, there are about
30% more genes, including 11 additional genes encoding
components of the translational apparatus. So far, only a single
type I intron has been found in Cyanophora paradoxa, in a
tRNAIeU gene (162). The same intron is found in cyanobacteria.
Cryptomonad algae contain a plastid and residual nucleus or
nucleomorph enclosed within the endoplasmic reticulum of the
cytoplasm and thus effectively separated from the normal cell
nucleus (see 123, 386). Distinctly different 18S rRNAs are
encoded by the nucleus and nucleomorph of Cryptomonas (D
and are spatially separated within the cell (129, 414). The
nucleomorph rRNA genes are related to those of red algae,
while the nuclear rRNA genes are clustered separately in the
phylogenetic branch containing land plants and green algae.
This suggests that cryptomonad algae may have arisen through
a second endosymbiotic event in which a eukaryotic symbiont
from the red algal lineage was taken up by a unicellular host
more closely related to the green algae (129, 130, 386). Partial
sequencing of the plastid genome of Cryptomonas (D has
revealed the presence of several novel genes, including four
genes for ribosomal proteins not found in chloroplast genomes
of land plants (122, 124, 680; also see below).
In the red alga Porphyra purpurea, over 125 genes have been
identified in the ca. 60% sequenced chloroplast genome (514,
515), suggesting that the entire genome may contain as many
as 200 to 220 genes, about twice as many as found in the
completely sequenced genomes of land plant chloroplasts.
These include at least seven photosynthesis and nine ribosomal
protein genes not present in land plants. Introns have not been
found in any of the 80 genes sequenced to date. The chloroplast genome of P. yezoensis possesses an inverted repeat
containing the rRNA genes (353, 562, 563), but the related red
algae P. purpurea and Grijflthsia pacifica lack this invertedrepeat structure. In P. purpurea the rRNA genes are encoded
in direct repeats which are not identical in sequence (514, 516,
563). The unicellular red alga Cyanidium caldarium possesses
an inverted repeat containing only the rRNA genes, but gene
order appears to be more similar overall to that of Cryptomonas (D than to that of P. yezoensis or Griffithsia pacifica (385).
Inverted repeats containing rRNA genes are also found in
the plastid genomes of the brown alga Dictyota dichotoma
(330) and the golden-brown algae Olisthodiscus luteus and
Ochromonas danica (108, 563). The plastid genome of the
brown alga Pylaiella littoralis contains two different circular
DNA molecules (369, 370, 404, 405). The larger (133 kb)
molecule resembles a typical land plant chloroplast genome,
with two rRNA operons in an inverted repeat. The smaller (58
kb) molecule contains a 16S pseudogene sequence, which is
65% homologous to the functional 16S genes of the large
molecule, and a complex region that hybridizes with a 23S
rRNA probe (369, 370).
Initiation
THE PROCESS OF CHLOROPLAST
PROTEIN SYNTHESIS
We begin this brief review of chloroplast protein synthesis
with a comparison with the process as it occurs in bacteria. This
section will be followed by discussion of the tRNAs and
aminoacyl-tRNA synthetases. A more detailed discussion of
In prokaryotes, protein synthesis begins with formation of a
preinitiation complex from the 30S ribosomal subunit and
tRNAIMetUAC, with the 30S subunit binding to the purine-rich
Shine-Dalgarno sequence 7 ± 2 nucleotides (nt) upstream of
the initiator AUG (230, 261, 323). The canonical ShineDalgarno sequence, GGAGG, or a variant, pairs with a
pyrimidine-rich complementary sequence, the anti-Shine-Dalgarno sequence, near the 3' end of the 16S rRNA molecule.
Addition of a 50S ribosomal subunit converts the preinitiation
complex to an initiation complex that can enter the elongation
phase of protein synthesis. These reactions are promoted by
the three initiation factors, IF-1, IF-2, and IF-3. IF-1 enhances
the rates of ribosome dissociation and association and the
activities of the other initiation factors (261). IF-2 is involved in
initiator tRNA binding and GTP hydrolysis, while IF-3 prevents ribosomal subunit association in the absence of mRNA
and appears to stabilize mRNA binding by promoting the
conversion of a preternary ribosome-mRNA-fMet tRNA complex into a ternary complex in which codon-anticodon interaction has occurred. IF-3 also is thought to proofread the
AUG-anticodon interaction. Chloroplast equivalents of IF-2
and IF-3Chl, have been characterand IF-3, designated
ized from Euglena gracilis (212, 324, 325, 375,527, 678). Roney
et al. 527) confirmed that IF-2Chl is required for binding of
tRNA et to chloroplast 30S subunits, as is prokaryotic IF-2.
IF-2,hl occurs in several complex forms, varying in molecular
mass from 200 to 800 kDa (375). Subunits of 97 to >200 kDa
have been observed in these preparations. IF-3,hl promotes
Alinitiation complex formation in the presence of
though IF-3Chl will replace Escherichia coli IF-3 in initiation
complex formation, there is some evidence that its function
may be modified (527).
A DNA sequence with homology to the E. coli infA gene
encoding initiation factor IF-1 has been identified in the
chloroplast genomes of land plants, including the colorless
parasite Epifagus virginiana (558, 714), but is apparently absent
from the completely sequenced chloroplast genome of Euglena
gracilis (243). The tobacco infA gene, in contrast to the spinach
gene (571), lacks the ATG translation initiation codon and
thus may be a pseudogene. Reading frames with homology to
the genes encoding IF-2 and IF-3 have not been detected in the
sequenced plastid genomes of green plants, Epifagus virginiana,
or Euglena gracilis, and inhibitor experiments suggest that the
Euglena genes specifying these factors are nuclear in location.
However, homologs of the infB gene encoding IF-2 have been
found in the chloroplast genomes of the red algae P. purpurea
(514) and Galdieria sulphuraria (322). Lin et al. (359) have
recently reported characterization of a cDNA clone encoding
IF-3Chl in Euglena gracilis. This nuclear gene appears to be
present in about four copies, one of which is probably a
pseudogene. The putative protein contains two acidic regions
with no homology to other known sequences, in addition to a
175-amino-acid region with 31 to 37% homology to other IF-3
proteins.
Shine-Dalgarno-like sequences are present in the untranslated leader regions of many but not all chloroplast mRNAs
(35, 44, 318, 532, 593, 746). Ruf and Kossel (532) reported that
37 of 41 chloroplast genes examined in tobacco have such
sequences if one extends the anti-Shine-Dalgarno sequence in
the 16S rRNA beyond the canonical CCUCC to include the
adjacent unpaired ACUAG sequence. Bonham-Smith and
IF-2Ch,
IF-2Chi.
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the cyanelle because of its secondary peptidoglycan wall and
photosynthetic apparatus with phycobiliproteins typical of cyanobacteria and red algae. Most of the 133-kb cyanelle genome
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
VOL. 58, 1994
Elongation
Elongation of the peptide chain requires three steps, i.e.,
aminoacyl-tRNA binding, peptide bond formation, and translocation, and involves three binding sites for tRNA (261, 460,
518, 690). The aminoacylated tRNA combines with elongation
factor EF-Tu and GTP to form a ternary complex, which then
associates with a ribosome complexed to mRNA and peptidyl-
tRNA. The specific ternary complex is selected on the basis of
codon-anticodon recognition at the A site and is followed by
GTP hydrolysis and the release of an EF-Tu-GDP complex.
Peptide bond formation takes place with transfer of the
growing peptide chain to the aminoacyl-tRNA in the A site.
Translocation is promoted by EF-G and GTP hydrolysis, and
involves movement of the peptidyl-tRNA-mRNA complex
from the A to the P site. The process is then repeated, and the
deacylated tRNA moves from the P to the E site. The A and E
sites themselves are allosterically linked in a negative sense so
that occupation of the A site by aminoacylated tRNA reduces
the affinity of the E site for deacylated tRNA and vice versa.
Regeneration of the active EF-Tu-GTP complex from EF-TuGDP is mediated by elongation factor EF-Ts. All three elongation factors have been characterized from Euglena chloroplasts by Spremulli and colleagues (53, 145, 173, 341, 585), and
the structure of the guanine nucleotide-binding domain of
EF-Tu has been modeled by Lapadat et al. (341). EF-Tu has
also been purified from pea and tobacco chloroplasts (445,
589).
Reading frames with homology to the bacterial genes encoding the three elongation factors EF-Tu, EF-G, and EF-Ts
are absent from the three completely sequenced land plant
chloroplast genomes (482, 558), but some of these genes have
been retained in the plastid genomes of certain algae (see
below). Two distinct nuclear genes encoding chloroplast
EF-Tu have been identified in tobacco (445, 611, 661). A
nuclear EF-G gene has been cloned and sequenced from
soybean (650), and a partial clone obtained from pea (2).
Early inhibitor experiments with Euglena gracilis indicated
that EF-Ts and EF-G were nuclear gene products but that
EF-Tu might be encoded in the chloroplast (52, 173). These
predictions were confirmed by identification of a chloroplast
tufA gene encoding EF-Tu (429) and by failure to find genes
encoding EF-Ts or EF-G in the recently completed Euglena
chloroplast genome sequence (243). The Euglena tufA gene is
split into three exons separated by two introns (429). An
uninterrupted sequence with homology to the E. coli tufA gene
has been reported from the chloroplast genome of C. reinhardtii (15, 684). The tufA gene sequence is also found in the
Cyanophora cyanelle genome (32, 598) and in the chloroplast
genomes of representative green algae in the families Ulvophyceae, Chlorophyceae, and Charophyceae, the latter group
being the presumed ancestors of land plants (14, 15). However,
tufA is absent from the chloroplast genome of the liverwort
Marchantia polymorpha, representative of the earlier land plant
lineages (472, 473). Baldauf and Palmer (15) concluded that
transfer of this gene to the nucleus probably occurred in the
charophycean lineage prior to the emergence of land plants.
Reith and Munholland (514) have reported that the chloroplast genome of the red alga P. purpurea not only possesses a
reading frame corresponding to tufA but also possesses one
corresponding to tsf which encodes EF-Ts in prokaryotes. This
gene has also been found in the chloroplast genome of the
thermophilic red alga Galdieria sulphuraria (322). In prokaryotes, mutations to fusidic acid resistance can occur in the
structural gene for EF-G (fus) (357). A nuclear mutation in C.
reinhardtii has been reported to confer fusidic acid resistance
on chloroplast EF-G, but the gene encoding this factor has not
yet been identified (74; also see 247).
Production of chloroplast protein synthesis factors appears
to be light regulated. Spremulli and coworkers have shown that
activities of Euglena IF-2, IF-3, EF-Tu, EF-G, and EF-Ts all
increase on transfer of cells from dark growth to light (52, 173,
324, 585). In Chlamydomonas synchronous cultures, transcription rates for four chloroplast-encoded photosynthetic genes
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Bourque (35) observed that 181 of 196 chloroplast-encoded
transcripts examined possessed a Shine-Dalgarno sequence
within 100 bp 5' to the initiation codon. However, spacing of
Shine-Dalgarno sequences in chloroplast mRNAs is less uniform than in bacteria. Frequency distributions of the most
common individual positions potentially involved in base pairing with 16S rRNA ranged from -2 to -29, with a major peak
(ca. 40%) at -7 to -8, a smaller peak at -15 to -16, and a
third small peak at -21 to -23 (35, 532). Thus, chloroplast
ribosomes may be able to accommodate larger distances
between the ribosome recognition site and translational start
sites than bacterial ribosomes. For example, in the Chlamydomonas rpsl2 gene, a canonical Shine-Dalgarno sequence is
found at position -55 upstream of the initiator codon (364).
The variability of the Shine-Dalgarno sequence raises the
question whether initiation from this sequence proceeds as in
eubacteria for Shine-Dalgarno sequences close to the AUG
codon and occurs by transient binding and "scanning" for
more-distant Shine-Dalgarno sequences (306). In tobacco the
mRNAs for those chloroplast genes lacking Shine-Dalgarno
sequences either show only a trinucleotide sequence for potential base pairing (atpB) or contain out-of-frame initiator
codons between the potential recognition sites and the respective in-frame start codons (rpsl6, rpoB, and petD [532]).
In Euglena chloroplasts, mRNA-rRNA recognition seems to
proceed by somewhat different rules, because the putative
anti-Shine-Dalgarno sequence CUCCC differs from the canonical CCUCC sequence and actually forms the 3' terminus of
the 16S rRNA rather than being located several bases from the
end (592). Since only about half of the Euglena chloroplast
mRNAs contain Shine-Dalgarno sequences, two modes of
initiation complex formation have been postulated (527, 677).
In one class of mRNAs, complex formation is facilitated by a
Shine-Dalgarno-like sequence. However, in the second class
the A+U content of the region 5' to the initiator AUG is 90%
or greater and this portion of the mRNA is relatively unstructured, making potential start sites in this region readily accessible to small subunits. Koo and Spremulli (318, 319) have
studied formation of initiation complexes in vitro with transcripts containing the 5' untranslated leader region of the
Euglena rbcL mRNA, which is A+U rich and contains no
Shine-Dalgarno sequence. Introducing a Shine-Dalgarno sequence into this region enhanced initiation only slightly.
Deletion and/or modification of the leader region demonstrated that a minimum of about 20 nt is required to form the
initiation complex in vitro and that the full 55-nt length is
necessary for full activity in complex formation (318). The
primary sequence of the region seems less important for
initiation than does its length. The native 55-nt sequence has
only weak secondary structure, and modification of the sequence to create increased secondary structure within about 10
nt of the AUG codon diminished formation of the initiation
complex significantly (319). Koo and Spremulli concluded that
the major determinant of initiation in those Euglena mRNAs
with no Shine-Dalgarno sequence is presence of the AUG
codon in an unstructured region of mRNA that is accessible to
the 30S subunit.
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HARRIS ET AL.
and for the tufA gene were all found to be maximal at the
beginning of the light period (51, 350). However, EF-Tu
mRNA decreased to almost undetectable levels in the second
half of the light period. Activity of the pea chloroplast EF-G,
encoded by a nuclear gene, is also light regulated but at the
level of translation (1).
Termination
Chloroplast tRNAs and Aminoacyl-tRNA Synthetases
The properties of chloroplast aminoacyl-tRNA synthetases
have been summarized by Steinmetz and Weil (593). These
enzymes are encoded in the nucleus. Most are distinguishable
from their cytoplasmic counterparts and will charge only
chloroplast or prokaryotic tRNAs efficiently. These enzymes
have unusually high molecular masses (75 kDa or greater) and
can be found as monomers, homodimers, heterodimers, or
heterotetramers depending on the enzyme.
The structure and codon recognition patterns of chloroplast
tRNAs and the organization of their cognate genes have been
extensively reviewed elsewhere (397-399, 593, 616). Genes
encoding individual chloroplast tRNAs are highly conserved in
different species of land plants and are similar in structure and
sequence (ca. 70% sequence identity) to prokaryotic tRNA
genes but have low homology to those of eukaryotic cells.
However, the 3'-terminal CCA triplets of chloroplast tRNAs
are added posttranscriptionally, as occurs for all eukaryotic
cytoplasmic tRNAs but for only about one-third of bacterial
tRNAs. Isoaccepting tRNAs for a given amino acid are
encoded by different chloroplast genes, but these tRNAs are
charged by the same chloroplast tRNA synthetases. Some
chloroplast tRNA genes are preceded by prokaxyotic-like
promoter sequences, but such sequences are absent upstream
of other chloroplast tRNA genes, which may thus possess
alternative promoters, possibly internal to the coding region
(227, 229, 616).
The tobacco chloroplast genome contains 30 tRNA genes,
23 of which are single and 7 of which are duplicated in the
inverted repeat. Rice has the same set of tRNA genes as
tobacco, but the inverted repeat extends through the tRNAH1S
gene, found in the single-copy region adjacent to the inverted
repeat in tobacco. In liverwort there are 31 chloroplastencoded tRNA genes, with the extra gene being tRNAAxgCCG,
but in Euglena gracilis there are only 27 (243, 558, 616).
(444).
One tRNAGlUuc has a special function in chlorophyll
biosynthesis as well as participating in protein synthesis, while
the other two species have a U*UG anticodon specific for
glutamine and are converted from Glu-tRNA01n to GlntRNAGJn by a specific amidotransferase activity present in
chloroplast extracts (398, 616). This mischarging mechanism
has also been described in several gram-positive bacteria (398).
The chloroplast genomes sequenced to date encode a typical
initiator tRNA"cICAu, and all employ the three classical
termination codons (UAA, UAG, and UGA). However, genes
for tRNAs recognizing the codons CUU/C (Leu), CCU/C
(Pro), GCU/C (Ala), and CGC/A/G (Arg) are absent from the
chloroplast genomes of tobacco and rice. Since all 61 sense
codons are used in the three sequenced land plant chloroplast
genomes, this deficit in specific tRNAs requires that the
tRNAs either be imported or be read by the "two-of-three"
mechanism used in animal mitochondria (174, 716) or by
four-way wobble (480). In the absence of import in Euglena
chloroplasts, one of the last two mechanisms would have to
pertain to seven of the eight codon families (243). In land plant
chloroplasts, two-of-three or four-way wobble seems to be used
for tRNAMIaUda,GC, tRNAProU*GC, and tRNAA`gICG, which can
read respectively all four alanine (GCN), proline (CCN), and
arginine (CGN) codons (488). The first two tRNAs contain a
modified U (U*) in the anticodon. The problem of decoding
the six leucine codons is solved somewhat differently. Two of
the leucyl-tRNAs translate the UUA and UUG codons (488).
The remaining tRNAeUUAM7G translates all four CUN
codons for leucine apparently by a U * N wobble mechanism
(489).
In tobacco, rice, and liverwort, six of the chloroplast-encoded tRNA genes possess introns which must be removed
from the primary transcript during processing (398). In tobacco these introns range in size from 503 bp (tRNAeuuAA)
to 2,526 bp (tRNALYSJuu) (616). Many land plant chloroplast
tRNAs are singly transcribed, although a cotranscribed, tricistronic tRNA gene cluster has been identified in tobacco (398)
and the two tRNAs found in the spacer between the 16S and
23S rRNA genes are transcribed as part of the rRNA operon
precursor (see below). Cotranscription of tRNA gene operons
is the usual case in Euglena gracilis. RNase activities thought to
be involved specifically in tRNA processing have been identified in chloroplast extracts (225, 226, 727).
PLASTID GENES FOR rRNAs
Phylogenetic Conservation
All chloroplast genomes examined contain genes for the
16S, 23S, and 5S RNAs of the chloroplast ribosome. Table 1
lists species for which sequences have been published. Chloroplast rRNAs are highly conserved at the sequence level and
are most closely related to eubacterial sequences, which include those of cyanobacteria (210, 219, 236, 512, 709). For
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
Termination of translation in bacteria involves the hydrolysis
of peptidyl-tRNA and release of the completed protein from
the ribosome when the ribosome reaches one of the three
termination codons (261). Termination requires the action of
two release factors, RF-1, which is specific for UAA and UAG,
and RF-2, which is specific for UAA and UGA. A third release
factor, RF-3, stimulates the activities of RF-1 and RF-2. The
same three codons are used for translation termination in
chloroplasts (35, 36), with UAA being by far the most frequent
(70% in land plant sequences surveyed by Bonham-Smith and
Bourque [36]) and UGA being rare (9%). UAA is also
overwhelmingly preferred as the stop codon in Chlamydomonas chloroplast genes (247). Bonham-Smith and Bourque (35)
noted that UGA was never used as a stop codon in Marchantia
chloroplast genes and proposed that a modification of the 16S
rRNA in this species prevents recognition of UGA as a
termination signal. No reading frame with homology to any of
the genes encoding bacterial termination factors has been
identified in a chloroplast genome, nor has isolation of these
factors been reported.
Several chloroplast tRNAs have unusual features. TIwo
different tRNAIle species are found in plant chloroplasts. The
major species (tRNAIle1, encoded in the spacer between the
16S and 23S genes) recognizes the codons AUU and AUC,
while a minor species (tRNAIle2) recognizes AUA. However,
the gene encoding the latter tRNA contains a CAU anticodon,
which normally would recognize AUG for methionine. One
possible explanation is that the C residue is modified in some
way posttranscriptionally. In E. coli the C of the homologous
tRNA is modified to lysidine, a novel type of cytidine with a
lysine residue, which allows it to recognize the AUA codon
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
705
TABLE 1. Plastid and cyanobacterial rRNA sequences published or submitted to GenBank
Taxon
16S rRNA
Anabaena sp.
Anacystis nidulans
Antithamnion sp.
Astasia longa
Chlamydomonas moewusii
Cyanophora paradoxa
Daucus carota
Epifagus virginiana
Euglena gracilis
Euglena gracilis bacillaris
Glycine max
Helianthus annuus
Marchantia polymorpha
Nanochlorum eucaryotum
Nicotiana plumbaginifolia
Nicotiana tabacum
Ochromonas danica
Ochrosphaera sp.
Olisthodiscus luteus
Oryza sativa
Oscillatoria sp.
Palmaria palmata
Pisum sativum
Porphyra purpurea
Porphyridium sp.
Prochloron sp.
Pylaiella littoralis
Pyrenomonas salina
Sinapis alba
Spinacia oleracea
Spirodela oligorhiza
Synechococcus lividus
Zea mays
23S rRNA
Alnus incana
Anacystis nidulans
Antihamnion sp.
Astasia longa
Chlamydomonas eugametos
Chlamydomonas frankii
Chlamydomonas gelatinosa
Chlamydomonas geitleri
Chlamydomonas humicola
Chlamydomonas indica
Chlamydomonas iyengarii
Chlamydomonas komma
Chlamydomonas mexicana
Chlamydomonas moewusii
Chlamydomonas pallidostigmatica
Chlamydomonas peterfii
Chlamydomonas pitschmanii
X59559
X03538; X00346, K01983 (partial)
X54299
X14386
X15850
J01395, X03269
X12742, X05694, X03848
X65099
X65100
X65688
X65689
X16579
X58864
X56806
X52985
M63813, M63814
M62775, M62776
M64522, M64526, M64531, M64536
M19493 (partial)
X73670
M81884, X62099
V00159, X12890, X05005, X70810
X00536 (partial)
X07675, X06428, M37149 (partial)
X73893
X04465
X76084
M82900, X70938
J01452, J01453, V00165, V00166, Z00044
X53183
X65101
M82860, X15768
X15901
X58359, X58360, X58361 (partial)
Z18289
M37430
X51598
M16874, M16862, M30826 (partial)
L07257, L07258
X63141
M21373, X14873, X14874
X55015
M15915, X04182
J01440, M21453 (partial)
X00014, X00015 (partial)
X67091, X67092, X67093 (partial)
M10720, Z00028
M75722
X00512, X00343 (partial)
X54299 (partial)
X14386
Z17234
X68905-X68909
Z15151
X68891, X68892
X68921, X68922
X68893-X68898
X68886, X68886
X68927-X68929
X68910-X68912
X68913-X68918
X68899-X68904
X68887, X68888
Z15152
Reference(s)
356
333, 647, 697
384
569
140
137
722, 724, 725
281
281
280
280
279
702, 703
130
383
63
681-683, 692
548
287
395
435, 712, 714
217, 243, 529, 530, 549
152
110, 673
77
312, 472, 473
553
476, 729
560, 561, 645, 646
705
281
108, 109
265
698, 699
573
602
79
557, 617, 618
516
34
555, 660, 665
404, 405
382
502
56, 409
302
38
554
351
126, 334
384
569
200, 657, 658
658
658
658
658
658
658
658
658
658
658
658
658
Continued on following page
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
Chlamydomonas reinhardtii
Chlorella ellipsoidea
Chlorella kessleri
Chlorella mirabilis
Chlorella protothecoides
Chlorella sorokiniana
Chlorella vulgaris
Conopholis americana
Cryptomonas 1
Cyanidium caldarium
Cyanobacteria (miscellaneous spp.)
GenBank accession no(s).
706
MICROBIOL. REV.
HARRIS ET AL.
TABLE 1-Continued
Epifagus virginiana
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Olisthodiscus luteus
Oryza sativa
Palmaria palmata
Pisum sativum
Pylaiella littoralis
Spinacia oleracea
Spirodela oligorhiza
Zea mays
4.5S rRNA
Acorus calamus
Allium tuberosum
Alnus incana
Apium graveolus
Codium fragile
Commelia communis
Conopholis americana
Dryopteris acuminata
Gossypium hirsutum
Hordeum vulgare
Jungermannia subulata
Ligularia calthifolia
Lycopersicon esculentum
Marchantia polymorpha
Marsilia quadrifolia
Mnium rugicum
Nicotiana tabacum
Oryza sativa
Osmunda regalis
Pisum sativum
Spinacia oleracea
Spirodela oligorhiza
Triticum aestivum
Zea mays
J01398, X01977, X16687, X16686
X68889, X68890
X68919, X68920
X68923-X68926
M36158; X05693, X03848 (partial)
X52737 (partial)
X59768
X14504 (partial)
X54300 (partial)
M19493 (partial)
M81884, X62099
X13310, X12890
M13809, X04465, X01647
J01446, Z00044
X15768 (partial)
X15901
Z18289
M37430
X61179, M21373 (partial)
M21453, X04977 (partial)
X00012, X00013 (partial)
Z00028, X01365
M36166
M35406
M75719
M35404
M35276
M35407
X58863
X01523
X63124
M35405, M57605
M13808
M36165
M33098
X04465, M13809
X51641
M35056
J01446, V00161, J01891, J01451, X01277, Z00044
X15901
X51978
M37430
M10757, X04977
J01439
M10541
M19943, Z00028, X01365
346, 521
658
658
658
726
394
703
128
384
287
435, 712, 714
549, 730
312, 473
560, 561, 627
108
265
573
602
405, 581
11, 409
304
148
31
738
284
738
176
738
703
623
440
80, 738
691
31
739
472, 473, 691
421
652
560, 561, 624, 625
265
421
602
11, 332
303
696
147, 148, 601
5S rRNA
Alnus incana
Anacystis nidulans
Astasia longa
X00343, X00757, M23834
X14386
Chlamydomonas reinhardtii
Chlorella ellipsoidea
Conopholis americana
Cyanophora paradoxa
Cycas revoluta
Dryopteris acuminata
Euglena gracilis bacillaris
Euglena gracilis
Ginkgo biloba
Glycine max
Gossypium hirsutum
Jungermannia subulata
Juniperus media
X03271
X04978
X58863
M32451, M33030
X12787
X00758
X00536
K02483, X12890
X51979
X16736
X63124
X00667
Lemna minor
Lupinus albus
Marchantia polymorpha
X02714
X65030
M75719
X00666, X04465
284
94, 125
569
550
724
703
411, 412
743
629
152
243, 296
421
23
440
728
663
144
327
472, 473, 728
Continued on following page
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Chlamydomonas reinhardtii
Chlamydomonas starrii
Chlamydomonas zebra
Chlamydomonas sp.
Chlorella ellipsoidea
Coleochaete orbicularis
Conopholis americana
Cryptomonas (F
Cyanidium caldarium
Cyanophora paradoxa
Reference(s)
GenBank accession no(s).
Taxon
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
707
TABLE 1-Continued
Taxon
Spirodela oligorhiza
Synechococcus lividus
Vicia faba
Zea mays
J01451, M10360, M15995, X01277, Z00044
X15901
X63200
X05551
M37430
L07259, L07260
144,
265
421
146
602
516
664
380
580
112,
303
111,
663
147,
K03159, X02637
X61179
V00169, X05876
J01439
X02731
M19943, Z00028
example, primary sequence homology is generally over 70%
for chloroplast or cyanobacterial 16S rRNAs compared with
that of E. coli and greater than 80% for chloroplast 16S rRNA
compared with cyanobacterial 16S rRNAs. Gray (219) recognized eight noncontiguous conserved primary sequences in 16S
rRNA interspersed among nonconserved sequences. The predicted secondary structures of these molecules are even more
conserved, and virtually all of the approximately 45 helices
postulated for the E. coli 16S rRNA (62, 462) are present in
chloroplast 16S rRNAs of Euglena gracilis, Chlamydomonas
species, tobacco, and maize (232, 512; also see below). Compensating base substitutions are often seen on the complementary sides of predicted stem structures, strengthening the
supposition that these structures are functional in vivo. Because of this high degree of structural conservation, rRNA
genes have found extensive use in phylogenetic studies (78,
219, 232, 235, 236, 342, 710). Comparative analyses of 16S (54,
210) and 5S (144, 380, 663, 743) rRNA sequences support both
the probable origin of chloroplasts from endosymbiotic cyanobacteria and the hypothesis that land plants derive from one
branch of chlorophyte algae. Van de Peer et al. (665) have
compared 16S and 18S sequences from eukaryotic, archaebacterial, eubacterial, plastid, and mitochondrial ribosomes. Although their analysis focused largely on mitochondrial origins,
their data also support the common ancestry of cyanobacteria
and plastids.
General Characteristics of Chloroplast rRNA
Gene Organization
As in the eubacteria, chloroplast rRNA genes are normally
arranged in an operon transcribed in the order 16S-23S-5S
(Fig. 2) (114, 320). In land plants, including some but not all
ferns, approximately 95 nt homologous to the 3' terminus of
the E. coli 23S molecule constitutes a 4.5S rRNA molecule,
separated from the remainder of the 23S gene by a transcribed
spacer, whereas in prokaryotes, all algae so far examined,
mosses, and the liverwort Marchantia polymorpha, the equivalent sequence is part of the 23S gene (47, 320). In C. reinhardtii,
the sequences homologous to the 5' portion of the 23S gene of
bacteria and plants are divided into 7S and 3S rRNAs,
separated by short spacers that are removed from the precursor rRNA posttranscriptionally (137). The large subunit rRNA
of C. eugametos comprises species (a and ,B) equivalent to the
C. reinhardtii 7S and 3S rRNAs and two larger species (ry and 8)
which together are equivalent to the remainder of the 23S
molecule (656).
560, 561, 624-626
491, 492
113
601
16S rRNA
The secondary-structure model of 16S rRNA based on
comparative sequence analysis (231, 232, 236, 449, 463, 468)
suggests a functional division into distinct 5', central, and 3'
domains, corresponding in E. coli to residues 26 to 557, 564 to
912, and 926 to 1391, respectively, followed by a "3' minor
domain" from ca. 1401 to 1542 (Fig. 3; for a numbered E. coli
sequence diagram in similar format to the tobacco sequence
shown in Fig. 3, see references 231 and 235). Each of these
domains comprises helices and loops whose secondary structure is phylogenetically conserved (219, 236). Models for the
tertiary structure of the E. coli 30S subunit have been constructed based on studies of RNA-RNA and RNA-protein
cross-linking, immunoelectron microscopy, and neutron diffraction (58-61, 463, 465, 596). Functional analyses involving
mutants, binding of tRNA and antibiotics, and assembly of
ribosomal proteins with RNA in vitro indicate that codonanticodon recognition involves the 3' domain and terminal 3'
minor domain. Three regions of the 16S molecule (E. coli nt
518 to 533, 1394 to 1408, and 1492 to 1505) that show a
particularly high degree of primary sequence conservation
appear to have tertiary interactions related to decoding (468).
tRNA bound in the A site interacts specifically with the 3'
domain and with residues in the "530 loop" (see reference 465
for review), whereas P-site-bound tRNA protects five sites in
the central and 3' domains that are proposed to be clustered in
tRNA
168
lie Al
23S
_uI
tRNA
165
5s
IE
cyanobacteria, most algae
23S
I
4.5S 5S
land plants
tRNA
165
IleAla
7S 38
23S 5'
23S 3' 5S
C. relnhardtll
FIG. 2. Arrangement of the rRNA operons in land plants and
algae, showing conservation of tRNAIle and tRNAMa within the spacer
between the 16S and 23S genes and variation in the species that
constitute the 23S molecule. In land plants, the tRNA genes are split
by introns, whereas in all algae examined to date they are uninterrupted. The region corresponding to the 3' end of the eubacterial 23S
rRNA is a separate 4.5S rRNA in angiosperms, gymnosperms, and
some (but not all) ferns. Internal transcribed sequences and one or
more introns interrupt the 23S genes of Chlamydomonas species (658).
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
Nicotiana tabacum
Oryza sativa
Picea excelsa
Pelargonium zonale
Pisum sativum
Porphyra purpurea
Porphyra umbilicalis
Prochloron sp.
Pylaiella littoralis
Spinacia oleracea
Reference(s)
GenBank accession no(s).
708
MICROBIOL. REV.
HARRIS ET AL.
UA
a^o
GA
a
central domain
AA
a
CMnGAA A c^^c
GUc 'aGGUGGCCUUUAAGGG-cCA
CGA
A U
a-C
A U
-a
ca0-C
spr
GO
0
U.G
G-C
C - GA
U - AC
0-C
u a
C-Q
c-a
U
AA
ACA
cc
ACCC
GGCGOUGGA CU A AAGC
AACCCUG0
I .II I .II II IIIIIlIi
11I1II1I1
UCGOGACC
CU
CUGCCGCCU
A
UAA
GA UUUUUC
A
a
A
3' domain
CAC
0.
G~~~~~A
GU /.UAG
A0!
A
helix 17
5' domain
i
sr
0
5,
nr
A
GUC ACOGGAAGUG
I - I I In I I I I- a
COO U0ACCUUUoU
a
G a C
helix 6
3' minor domain
tobacco 16S rRNA
FIG. 3. Secondary structure of tobacco 16S rRNA, showing the major functional domains and sites of antibiotic resistance (Table 2; sr,
streptomycin; spr, spectinomycin; nr, neamine/kanamycin). Sequence from the Ribosomal Database Project, courtesy of Robin Gutell.
the tertiary structure. Many of the same sites, which are all in
highly conserved regions of the 16S molecule, also interact with
antibiotics that block protein synthesis at the level of the 30S
subunit (424, 467, 537; also see below).
The principal regions in which the secondary structures of
chloroplast 16S rRNAs deviate from the E. coli model are in
the 5' domain between nt 198 and 220 (numbering according
to the E. coli sequence [462]), where chloroplast rRNAs have
a shorter helix 10 than E. coli does, and between 455 and 477,
where E. coli has a well-defined helix (the upper part of helix
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
^Aa GA G G
AaUUCUCCU~AA
A-U
C
-
CHLOROPLAST RIBOSOMES AND
VOL. 58, 1994
17 of Brimacombe et al. [59]) that is lacking in cyanobacteria
and chloroplasts. Helix 6 is also shorter in chloroplast and
cyanobacterial 16S rRNAs than inE. coli. Raue et al. (512)
noted eight regions where secondary structure is conserved but
primary sequence is highly variable. These eight regions are
also sites of variation in secondary structure when the 16S
rRNAs of chloroplasts and eubacteria on the one hand are
compared with small-subunit rRNAs of mitochondria and
eukaryotic cytoplasmic ribosomes on the other.
23S rRNA
709
teria and plastid rRNAs, as does domain V. The break
between the 23S rRNA and 4.5S rRNA of land plants occurs in
domain VI.
5S rRNA
Their short length and relatively high degree of evolutionary
conservation have madeSS rRNA molecules frequent subjects
for phylogenetic studies (see e.g., references 117, 270, 580, 663,
664). They have also proved useful for computer modeling of
secondary and tertiary structure, including chemical reactivity
and accessibility of bases, and possible protein binding (67,
524, 525, 693). A numbering scheme applicable to both prokaryotic and eukaryoticSS rRNAs, proposed by Erdmann and
Wolters (157), defines five loops (a to e) and five helices (A to
E). In a compilation of sequences in the Berlin RNA Databank, Specht et al. (583) included representations of the
common secondary structure of eukaryotic and prokaryotic SS
rRNAs, which are differentiated into five structural groups
primarily on the basis of variability in one (D) of the five
helices. PlastidSS rRNAs are grouped in this classification with
those of eubacteria and land plant mitochondria (mitochondria of other taxa lackSS rRNA). Plastid and cyanobacterial SS
rRNAs are distinguished from those of most other eubacteria
and mitochondria by a single-base insertion in helix C and a
deleted base in loop c (157). Of the 121 nt of the typical SS
rRNA, 110 are identical in nearly all angiosperms and gymnosperms, 73 are conserved in ferns and liverworts as well, and 29
are identical in all plastids so far sequenced with a few singular
exceptions. The colorless flagellate Astasia longa and the red
alga P. umbilicalis are somewhat divergent compared with
Euglena gracilis and P. purpurea, respectively; 4 nt are altered
in one or both of the two parasitic plants Conopholis americana
and Epifagus virginiana compared with all other angiosperms;
and the sequence submitted to GenBank for cotton, Gossypium hirsutum (440), is missing 2 nt but is otherwise identical
to that of tobacco in all but two residues. Vogel et al. (671)
reported that SS rRNA from spinach chloroplasts could be
incorporated into biologically active 50S ribosomal subunits
assembled in vitro from Bacillus stearothermophilus proteins
and 23S rRNA.
Introns in rRNA Genes
A survey of 23S rRNA genes from 17 Chlamydomonas
species representing most of the taxonomic groups defined on
morphological and biochemical grounds (159, 538) revealed a
total of 39 group I introns inserted at 12 different positions,
some of which were unique to Chlamydomonas species (656658). However, no correlation was found between intron
distribution and a phylogeny for these 17 species based on
primary sequence of their 23S genes. Most of the intron
insertion sites identified in this study are in highly conserved
regions of the genome, which tend to be exposed in the
assembled ribosome. This is also true of the single intron in the
16S gene of C. moewusii, which lies within the 530 loop, a part
of the translational fidelity domain. In contrast, internal transcribed spacers, which have also been identified in rRNA genes
of bacteria and organelles, occur within regions of variable
primary sequence and secondary structure (224). When these
sequences are processed out of the pre-rRNA molecule, the
mature sequence is not religated, resulting in a fragmented
rRNA. Three internal transcribed spacers, found at equivalent
positions in the Chlamydomonas taxa studied by Turmel et al.
(656-658), result in fragmentation of the 23S rRNA into four
mature rRNA species, ao, ,, -y, and &.
The single group I intron in the 23S gene of C. reinhardtii
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
The secondary-structure model for the E. coli 23S rRNA
published by Gutell and Fox (233) consists of six domains
comprising a total of 95 helices (Fig. 4; for a numberedE. coli
sequence diagram in similar format to the tobacco sequence
shown in Fig. 4, see references 234 and 235). Domain V is the
principal site of tRNA binding to the 50S subunit (60, 426).
The central loop of this domain is involved in the peptidyltransferase center and is the site of mutations conferring
resistance to erythromycin, lincomycin, and chloramphenicol
(see below). Some tRNA interactions are found in domains II
and IV. When bound to the P site, tRNA also interacts with the
3' terminus of the 23S molecule (426). EF-G binds specifically
to position 1067 in the 23S molecule, a region identified with GTP
hydrolysis (465). EF-Tu protects residues in the 2660 loop.
Rau6 et al. (512) identified 18 variable regions in 23S RNAs
based on comparisons of eubacterial, organelle, archaebacterial, and eukaryotic large-subunit rRNAs, including the cyanobacterium Anacystis nidulans and chloroplast 23S rRNA
from Chlorella ellipsoidea, Marchantia polymorpha, tobacco and
maize. Of these 18 variable regions,5 are significantly different
in chloroplasts compared with E. coli, while in the remaining
13 regions, chloroplast rRNAs resemble those of eubacteria
but may differ from those of archaebacteria, mitochondria, and
eukaryotic cytoplasmic ribosomes. Somerville et al. (581) have
published a secondary-structure map of the 23S rRNA from
the brown alga Pylaiella littoralis which resembles the cyanobacterial (Anacystis) molecule much more closely than it
resembles those of land plants or green algae. Cladistic analysis
of the 23S rRNA sequence produced a tree in which cyanobacterial and plastid sequences were clearly delineated from all
other eubacterial sequences and in which the chromophyte
algae (as represented by Pylaiella littoralis) and Euglena gracilis
formed a common branch.
In domain I, cyanobacterial and chloroplast 23S rRNAs lack
helix 8 of E. coli (nt 131 to 148, variable region V1) and have
an insertion between helices 13 and 14 (E. coli nt 271 to 365,
variable region V2) which can be folded into a helix (512). In
domain II, variable regions V4 and V7 (nt 636 to 655 and 1020
to 1029, respectively) are highly conserved among eubacteria
and chloroplasts, while 3 nt (nt 931 to 933) in E. coli V6 are
replaced by a loop of 5 to 20 nt in chloroplasts. Region V8 (nt
1164 to 1185) is conserved in E. coli, Anacystis nidulans, and
most chloroplast 23S rRNAs but is the site of a possible 243-nt
intron in Chlorella ellipsoidea (726). Gutell and Fox (233) have
suggested that this insertion may actually be a part of the
rRNA rather than the only known instance of an intron
inserted in a variable rRNA region.
Domain III comprises variable regions V9 to V12, of which
Vii (E. coli nt 1521 to 1542) is the most diverse in chloroplast
23S rRNAs. Some (but not all) chloroplast rRNAs have lost
part of helix 54, and helix 55 in Chlorella ellipsoidea and Z.
mays contains insertions compared with E. coli; however, in
other chloroplast genomes, this helix is similar in size to that of
E. coli. Domain IV shows strong conservation among eubac-
PROTEIN SYNTHESIS
710
MICROBIOL. REV.
HARRIS ET AL.
AAAUUac
cu
A
AB
BAA
U-A
G
eUAAGAAG
I II I
I
*I
VI I
tcc A AUUUC a
A
I II I
I
-
AcUoUUUC%cccuu OGAAUBCAAA
A
u
c
c
GTPase
center
Ue
c
a UUA UCOB
G
UA
ABCC a
OAA
Cu
AGGCGC
,,|"III
0UC0CB
_UBAAG
A
U-A
U A
u-C
-c
u~~~~~~~~~
A~~~~~~~~
a
u
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
A
A
AU
aAU
u
u
0-C
0-C
O-C
A-U
-1
B
6-C
A
A
0
U0
ViOA
BA%
GOCC
BUC CC0ABzG0ACQ%%.IA
ZqGCCCCCUUBUUBa
°scU
r
Buu
CUC
AcC
IIIIII,I*I
I
I1111
I
AA
CA
V9
0AU
aa4AusUC
UBUC GBOA
AAABBCPUA
Aa CCBA CUAAAU
UG.LCACAG
A
ACC
A
A AAAf
GU
CAU
V7
C
II
UUBG
111111-
A
'ac GUUUA
u AB-U
AAC
1G1
A[q
OCCUCCU'
AAC
U
A
UB'
C-B
V12
III
~~~domain
C
A
A .UE
C CA
_sC-B
c
U AA
uuC-Gc
UI-C
_ _Ca
I f
3'fn
bAA
V6
domain I
V3
domain 11
e AA
Aa
CAA
c
u
C=U
a-B
AA
U-A
B-C
C-B
tobacco 23S rRNA, 5'
V2
AAC-BGBUUBU
a
oil
11|1
A
-QU
11,
AAA'
0-2
._
FIG. 4. Secondary structure of tobacco 23S rRNA, showing major functional domains and sites of antibiotic resistance (Table 2). Variable
regions are numbered according to the system of Raue et al. (512). Sequence from the Ribosomal Database Project, courtesy of Robin Gutell.
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
711
UC
U * G
C-a
C-C
UCG-C
a-C
A
AG
C uu V5
AICUA
LL
C,1
3UGG
A
G-CA
domainIV
UCACCTf
C
CU U-
UAGAG
c-a
U-A
U-A
C-a
c-a
G
GGA
GA
a-Cu
G
GA
0U
u
U-A
V13
A
A
u.G
tu
a
V16
a
G-CUA Accuu U
UCUCGGAC
G-CC
C
I I * I°I
-II
G
U
-UGACAG
A
G0-Cc
aC
U-A
-
c-a
C
-
a
G aa
A CCA
o
A
A
A
A
cC-O cU
G
U-A
GC
Gu
UC- aU
GOA AG
CG
U-A
C
I-C
U
AA- U
Uuca
c
U:
U-A
U
-c
C
II
C
a
G AU
C
1 G*U GU
c -Ga
U
G
A-AA
AU :
:
C
U-A
U-A0
G
G-CUA
U-A
CG-C
U
AGUC
CAa
U-AA A
A
aUu
A
A
C
AUA
GaO
A
ACG
GU
aUUC
AC UGC.
I III
ACG
aC
G_.C
CC
AC-G GAU
AU
C
AA C
A
peptidyl
GGCUGAUCUUCCCCACCU
It
C
1I.
1i1i1iI
transferase caUC GAAC A a
domain VI
Ac
UU
u
C
u
3A
Ac
cA
UC
5' 4.5S
A
UC
CAUGG
UGUGGCUG U
AAGCCACC
UUAU
A-UA
BC-U
A
CAUU
-U
C-G
a-*U
'A
UtU G0GACCUUGUA U
C
A
U-A
tobacco 23S rRN IA, 3
a
Ua-C
C-a
A
A
c
CA- U
U%GCCGA Gc
CC--G
U. a
C=a
ACGGCGAG
11111
A
A
aG
G
A
G-C
_A
a
~~~U
C
Aa-c
u
GUaA
a
0C -GU
Ac
.A
'C
C-G
C=G
C' CU
UUG
Aa
C0
A
U
GA
A-U
U
aG
C-C
U-A
CGU
(522) is mobile (142) and encodes a double-stranded nuclease
(I-CreI) which has been purified and shown to have a 19- to
24-bp recognition sequence in this gene (143, 638). The
enzyme makes a 4-bp staggered cut just downstream of the
intron insertion site and will tolerate single- and even multiplebase-pair changes (143). This intron can undergo autocatalytic
splicing in vitro (637). The ac-20 nuclear gene mutant of C.
reinhardtii, which was initially characterized as deficient in
chloroplast ribosomes (see reference 247 and references therein), has been found to accumulate unspliced precursor rRNA
molecules, as well as unspliced precursors of the chloroplastencoded psbA gene (258, 259).
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
domain IV
A
-C
712
HARRIS ET AL.
The 23S rRNA gene of C. eugametos, a species now thought
to be only distantly related to C. reinhardtii, contains six group
I introns and three internal transcribed spacers (657). One
optional 955-bp group I intron in the 23S gene of C. eugametos
also appears to be mobile and is transmitted to all progeny of
crosses with the interfertile species C. moewusii, which lacks
this intron (347). The 402-bp group I intron in the 16S rRNA
gene of C. moewusii likewise can be transmitted in crosses to
The 16S-23S Spacer
The spacer regions between the 16S and 23S rRNA genes in
chloroZlasts and cyanobacteria contain tRNAIleGAU and
as do the E. coli rmA, mD, and rmH operons
tRNA aUGcm
(301, 436, 697, 735). In E. coli and cyanobacteria, the 16S-23S
spacer is short (<550 bp), but in land plants and charophyte
algae it is 1 to 2 kb or more, largely because of the presence of
type II introns in the two spacer tRNA genes (110, 311, 320,
394, 628). In all other algae so far examined, these spacer
tRNAs are uninterrupted (108, 216, 384, 405, 551, 725). In C.
1,100-bp region between the 3' end of the 16S
dispersed repeat elements in
direct and inverted orientations, which are capable of pairing
to generate extensive secondary structure in the precursor
RNA (551). Similar repeat elements are found elsewhere in
intergenic regions of the chloroplast genomes of C. reinhardtii
and the interfertile species C. smithii, and variations in their
numbers are responsible for most of the restriction fragment
length polymorphisms between the chloroplast genomes of
these isolates (50, 250, 486). The absence of these repeats in
chloroplast rRNA operons of other organisms, including C.
eugametos and C. moewusii, and their variation in number in
the 16S-23S spacer region between C. reinhardtii and C. smithii
suggest they are not essential for processing of the rRNA
reinhardtii,
an
gene and tRNAIle contains short
precursor.
Although the 16S and 23S rRNA genes in the plastid
euglenoid flagellate Astasia longa are
highly homologous to those of Euglena gracilis, the spacer
between these genes appears to lack tRNAIle and tRNAAla
(569). The chloroplast genome of Chlorella ellipsoidea was also
reported to lack the spacer tRNAAla (724), but subsequent
analysis has shown that the rRNA operon in this alga has been
genome of the colorless
disrupted by an inversion of a 5-kb region with a breakpoint
between the two tRNAs, so that the 5S, 23S, and tRNAMa
genes constitute a second operon on the opposite strand from
the 16S and tRNAIle genes (723, 725).
tRNAs Flanking the rRNA Operons
Genes encoding tRNAs are also often found in regions
flanking the rRNA operons, but their presence and identity are
much more variable than for the two tRNA genes in the
16S-23S spacer. There is a tRNAVa" proximal to the 5' end of
the 16S rRNA gene in all land plants examined (114). This
gene, which precedes the promoter for the rRNA operon, is
not present in C. reinhardtii or C. moewusii, nor is it found
upstream of any of the E. coli rm operons or in any of the
cyanobacterial sequences to date. In Euglena gracilis, the
equivalent tRNAVal is in a gene cluster distant from the rRNA
operons (477), and a pseudo-tRNAIle is found 5' to the 16S
gene (479).
In land plants the 5S rRNA gene is typically followed by a
tRNAN9 gene in the same orientation and by a tRNA,sn gene
on the opposite strand (118, 297, 298, 305, 557). In maize,
primer extension experiments have shown that the tRNA'9
gene, which is separated from the 5S gene by a 252-bp spacer,
is cotranscribed with the rRNA operon (118). This operon and
the tRNA In gene, which is distal to tRNAArg by 253 bp on the
opposite strand, are thought to share a common terminator
region consisting of a palindromic sequence which can be
folded into hairpin structures on both strands.
Antibiotic Resistance Mutations in the
Chloroplast rRNA Genes
Many antibiotics that inhibit bacterial protein synthesis bind
specifically to the 16S or 23S rRNA molecules (102, 424, 425),
and mutants resistant to these antibiotics have been shown to
result from single-base-pair changes in evolutionarily conserved regions of the genes encoding these RNAs in bacteria,
mitochondria, and chloroplasts (Table 2). Streptomycin resistance can result from changes at several nucleotides clustered
in three sites in the 16S chloroplast rRNA molecule of land
plants and green algae (equivalent to E. coli residues 13, 523 to
525, and 912 to 915). Although these three sites are widely
separated in the primary sequence, they interact with the same
subset of ribosomal proteins and are thought to be in close
proximity in the assembled 30S subunit of E. coli (603).
Spectinomycin resistance has been shown to result from mutations at the bases of the chloroplast 16S rRNA equivalent to
E. coli residues 1191 to 1193 and at the base equivalent to
residue 1064, which pairs with 1192. Neamine and kanamycin
resistance in C. reinhardtii can result from mutations at the
chloroplast 16S rRNA nucleotides equivalent to E. coli residues 1408 and 1409. In E. coli, binding of aminoglycoside
antibiotics to this region has been demonstrated (424, 717),
and site-directed mutagenesis of these and neighboring bases
has been used to obtain a number of mutants (116). Because
the E. coli genome has seven rm operons, antibiotic resistance
mutations must be selected by expression of cloned rRNA
operons on high-copy-number plasmids (570, 603). In contrast,
an efficient copy correction mechanism involving the inverted
repeat ensures that newly occurring 16S mutations can spread
to both rRNA cistrons in the chloroplast genome (50).
Erythromycin resistance mutations in the large subunit
rRNA are known in bacteria, in mitochondria of Saccharomyces cerevisiae and mammalian cells, and chloroplasts at the
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
isolates of the sibling species C. eugametos that lack this intron
(140). Transmission of these introns is often accompanied by
coconversion of flanking DNA polymorphisms. The mobile
intron in the 23S gene encodes a double-stranded DNA
endonuclease activity (I-CeuI) which has a 19-bp recognition
site centered around the insertion site. I-CeuI produces a
staggered cut 5 bp down from the insertion site (200, 406, 407).
The 23S rRNA gene of C. humicola has a group I intron,
ChLSU-1, inserted at a site in the peptidyltransferase loop and
encoding a putative 218-amino-acid endonuclease (96). Introns have been found at this site only in a few Chlamydomonas
species (658).
Turmel et al. (658) discuss the alternative possibilities for
transfer of group I introns from one site to another within a
genome. Intron-encoded endonucleases could effect such a
transfer at the DNA level (139); alternatively, a reversal of
self-splicing followed by reverse transcription of the recombined RNA could occur, followed by integration into DNA by
homologous recombination. The latter mechanism requires
only a short target site that can pair with the 5' intron sequence
called the internal guide sequence (718) and would be consistent with the position of intron insertion sites in exposed rRNA
regions in the ribosome in the Chlamydomonas species examined by Turmel et al. (658).
MICROBIOL. REV.
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
713
TABLE 2. Antibiotic resistance mutations in chloroplast rRNA and ribosomal protein genes compared with analogous mutations in E. coli
and mitochondria
Taxon'
Nucleotides
Reference(s)
16S rRNA mutations to streptomycin resistance
E. coli wild type
E. coli mutant
E. coli mutant
C. reinhardtii wild type
C. reinhardtii mutant
E. coli wild type
E. coli mutant
Nicotiana plumbaginifolia wild type
N. plumbaginifolia mutant
Nicotiana tabacum wild type
N. tabacum mutant
C. reinhardtii wild type
C. reinhardtii mutant
C. eugametos wild type
C. eugametos mutant
E. coli wild type
E. coli mutant
E. coli mutant
E. coli mutant
E. coli mutant
E. coli mutant
E. coli mutant
Euglena gracilis wild type
E. gracilis mutant
Mycobacterium tuberculosis
M. tuberculosis resistant isolate
Nicotiana plumbaginifolia wild type
N. plumbaginifolia mutant
N. tabacum wild type
N. tabacum mutant
N. tabacum mutant
C. reinhardtii wild type
C. reinhardtii mutant
C. reinhardtii mutant
C. reinhardtii mutant
905 UAAAACUCAAAUGA
905 . .
905.
G.
905 .
U
905 .
C
905
. ...
G
905 .
...
869 UGAAACUCAAAGGA
869.
U.
858 UAAAACUCAAAGGA
858.
G.
854 UGAAACUCAAAGGA
854.
U.
853 UGAAACUCAAAGGA
853.
A.
853.
U.
849 UGAAACUCAAAGGA
849.
U.
849 .
C
849
.G
16S rRNA mutations to spectinomycin resistance
N. tabacum wild type
N. tabacum mutant
N. tabacum wild type
N. tabacum mutant
N. tabacum mutant
N. tabacum mutant
C. reinhardtii wild type
C. reinhardtii mutant
C reinhardtii mutant
C. reinhardtii mutant
E. coli wild type
E. coli mutant
E. coli mutant
E. coli mutant
Zea mays (naturally resistant)
N. tabacum wild type
N. tabacum mutant
1006
1006
1133
1133
1133
1133
1118
1118
1118
1118
1186
1186
1186
1186
1132
1326
1326
16S rRNA mutations to neamine and kanamycin resistance
C. reinhardtii wild type
C. reinhardtii mutant
C. reinhardtii mutant
1332 CGCCCGUCACACCAUGGA 1349
137
251
1332 ...............G.1349
1332
251
1349
........
23S rRNA mutations to erythromycin and/or lincomycin
resistance
C. reinhardtii wild type
C reinhardtii mutant
C. reinhardtii mutant
E. coli wild type
E. coli mutant
2007 CUGGACAGAAAGACCC 2022
2007
2022
2007
2022
2050 CAAGACGGAAAGACCC 2065
2050
2065
.
.........
......
21
21
21
22
22
534
534
482
482
481
481
485
485
.....C
......
918
918
918
918
918
918
918
882
882
871
871
867
867
866
866
866
862
862
862
862
66
493
493
137
251
66
420
729
643, 644
646
184
137
251
199
199
66
431
343
493
37
493
343
217
428
131
131
729
643, 644
646
160
184
137
251
251
251
GCUGUCGUCAGC 1017
646
......
1017
182
GGAUGACGUCAAGU 1146
646
.....
1146
620
...........U.1146
620
.......
182
1146
GGAUGACGUCAAGU 1131
137
1131
.......
249, 251
1131
.......
249, 251
.......
1131
249, 251
GGAUGACGUCAAGU 1199
64
...........U.1199
26, 387, 570
...... .. ...G .1199
26, 387
...........A.1199
26, 387
GGAUGAGGCCAAGU 1145
554
GUUCCCGGGCCUUGUAC 1341
646
....... ... ..
620
1341
....
..
.....
.....
.........
.......
.....
........
......
.......
.....
346
251
251
65
158
Continued on following page
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
JUGAAGAGUUUGAUCAUG
A.
.
C.
AUGGAGAGUUUGAUCCUG
5 .
G.
517 GCCAGCAGCCGCGGUAAU
517 ......C...........
465 GCCAGCAGCCGCGGUAAU
465.
U.
464 GCCAGCAGCCGCGGUAAU
U
464 .
.......
468 GCCAGCAGCCGCGGUAAU
468
C. ..........
GCCAGCAGCCGCGGUAAU
4
4
4
5
714
HARRIS ET AL.
TABLE 2-Continued
..
Reference(s) 2
570
.
.............. 2065
132
.
.............. 2065
99
CUGGACAGAAAGACCC
99
........G.....
......99
See 100
GCAGACGGAAAGACCC 1958
See 100
. . G....... 1958
65
CAGUUCGGUCCCUAUC 2616
667
2616
..........u
346
CAGUUUGGUCCAUAUC 2574
251
2574
..........U
251
..........G..... 2574
199
CAGUUUGGUCCAUAUC
199
..........
See 100
CAGUAUGGUUCCUAUC 2790
2790
See 100
.
........ G
100
2790
..........
Nucleotides
Taxona
2050
2050
1943
1943
2601
2601
2559
2559
2559
.....
.....
.....
2775
2775
2775
.....
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
E. coli mutant
E. coli mutant
Nicotiana plumbaginifolia wild type
N. plumbaginifolia mutant
N. plumbaginifolia mutant
Saccharomyces cerevisiae mitochondria wild type
S. cerevisiae mutant
E. coli wild type
E. coli mutant
C. reinhardtii wild type
C. reinhardtii mutant
C. reinhardtii mutant
C. moewusii wild type
C. moewusii wild type
S. cerevisiae mitochondria wild type
S. cerevisiae mutant
S. cerevisiae mutant
MICROBIOL. REV.
23S rRNA mutations to chloramphenicol resistance
E. coli wild type
E. coli mutant
C. reinhardtii wild type
C. reinhardtii mutant
S. cerevisiae mitochondria wild type
S. cerevisiae mutant
S. cerevisiae mutant
65
2499 CUCGAUGUCGG 2509
158, 425
2509
....
2499
346
2509 CUCGAUGUCGG 2519
2519
208
2509 .....
See 158
2672 CUCGAUGUCGA 2682
.2682
See 158
..
2672
See 158
2682
2672 .....
S12 mutations to streptomycin resistance and dependence
E. coli wild type
E. coli mutant (sr)
E. coli mutant (sr)
E. coli mutant (sr)
E. coli mutant (sr)
C. reinhardtii wild type
C. reinhardtii mutant (sr)
E. coli wild type
E. coli mutant (sd)
E. coli mutant (sr)
E. coli mutant (sd)
E. coli mutant (sd)
C. reinhardtii wild type
C. reinhardtii mutant (sd)
N. plumbaginifolia wild type
N. plumbaginifolia mutant (sr)
N. tabacum wild tpe
N. tabacum mutant (sr)
38 TTTPKKPNSA
38 .... N.
Q.
38 . Q..
38 .... R.
38 .... T.
38 TVTPKKPNSA
38 .... T.
83 GGRVKDLPGV
..
83 .S
83 .... R.
L
83 .
D.
83.
83 GGRVKDLPGV
L
83 .
83 GGRVKDLPGV
83 .... R.
83 GGRVKDLPGV
.S
83
a
....
..
....
...
47
47
47
47
47
47
47
92
92
92
92
92
92
92
92
92
92
92
707
188
190
188
190
364
364
707
285
188
662
285
364
364
276
276
561
191
sr, streptomycin resistance; sd, streptomycin dependence.
positions equivalent to E. coli nt 2057 to 2058 (the yeast rib3
locus) and 2611 (yeast rib2) (Table 2). Some of the erythromycin-resistant mutants of C. reinhardtii are cross-resistant to
lincomycin. A lincomycin-resistant mutant of Nicotiana plumbaginifolia has also been identified at the base equivalent to E.
coli nt 2032. Chloramphenicol resistance in C. reinhardtii
results from a nucleotide substitution at a position equivalent
to E. coli nt 2504 (208). Chloramphenicol resistance mutations
at this site are also known in mitochondria of yeast (the rbl
locus) and mammals. All three regions of conserved sequence
together form a loop known to be involved in peptidyltransferase activity in E. coli (464).
Chloroplast antibiotic resistance mutations have been used
as markers in generation of transgenic tobacco plants by using
somatic cell fusions (427) and in chloroplast transformation of
Chlamydomonas species (48, 49, 453) and of tobacco (390, 619)
by using biolistic techniques.
RIBOSOMAL PROTEINS
Number and Nomenclature
Recent reviews provide an overview of chloroplast ribosomal proteins and the genes that encode them (36, 377, 379,
606, 608, 609, 615). For a concise summary of structure and
function of individual ribosomal proteins, with emphasis on the
E. coli ribosome, see the review by Liljas (358). Lindahl and
Zengel (360) provide a review of bacterial genes for ribosomal
proteins. Chloroplast ribosomal proteins were initially identified from various plants and algae by one-dimensional and
two-dimensional gel electrophoresis and were numbered according to their migration on these gels, a function of charge
and/or molecular mass, depending on the gel system. Natural
variations in the physical properties of ribosomal proteins
themselves, together with differing electrophoretic conditions
used for their separation, have meant that no two numbering
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
Organization of Chloroplast Ribosomal Protein Genes
The first suggestion that chloroplast genomes might encode
chloroplast ribosomal proteins came from labeling experiments carried out in the presence of inhibitors specific for
either chloroplast or cytoplasmic protein synthesis. These
studies led to the then remarkable conclusion that in land
plants, Euglena gracdiis, and C. reinhardtii about one-third of the
chloroplast ribosomal proteins were themselves synthesized- on
chloroplast ribosomes, with the remainder being made on cytoplasmic ribosomes and imported (121, 156, 181, 239, 495, 547).
With a few notable exceptions, the same subset of ribosomal
proteins is encoded in the chloroplast genome of each land
plant examined, while marked variations occur in certain algal
groups (see below). The genes encoding many of these proteins are arranged in clusters that are clearly remnants of the
ribosomal protein operons of eubacteria (Fig. 5) (see references 36, 377, 606, and 608 for additional discussion). The
Porphyra plastid genome has the most complete version of
these operons found to date (Fig. 5; Table 3) (514, 517). Most
of the same genes are also present in the cyanelle genome, but
the operon has been broken into three pieces (598). In land
plant chloroplasts the largest cluster contains the genes for
ribosomal proteins L23, L2, S19, L22, S3, L16, L14, S8, L36,
and S11 and the RNA polymerase gene rpoA in the same order
that they appear in the E. coli S10, spc and a operons, which
are part of the str cluster (Fig. 5; see Table 3 for references). A
similar organization of genes encoding ribosomal proteins is
seen in the Marchantia mitochondrial genome (630). The rps4
and rpsl4 genes are also found in chloroplast genomes of land
plants but are relocated outside the ribosomal protein cluster.
In some legumes, rp122 has been removed from this cluster and
relocated to the nucleus (193), and in a number of dicots the
chloroplast rp123 gene is disrupted and probably nonfunctional
(see below). The rp122 gene is also missing from this operon in
Chlamydomonas species (43, 277). In Euglena gracilis (242) and
in both C. reinhardtii and C. moewusii (43, 277), the ribosomal
protein gene cluster also contains rplS, which does not appear
to be present in the chloroplast genomes of land plants.
However, the Euglena operon lacks rpsll, which is now in a
separate operon with rps4 (242, 597). The Chlamydomonas
operons lack rps3, but open reading frames with homology to
rps3 are found elsewhere in the chloroplast genome (see
below). In C. moewusii, the large ribosomal protein cluster has
been disrupted by a rearrangement such that rp123, rpl2, and
rpsl9 are separated from rplJ6, rpll4, rplS, and rps8 by about 42
kb (43). The genes encoding S17, L24, and L15, which are part
of these operons in bacteria, have been identified in the
nuclear genomes of certain land plants (153, 196, 640). The
remaining genes of these E. coli ribosomal protein operons
(encoding proteins L17 and L30) have not been identified with
plastid equivalents thus far.
In E. coli, the genes encoding S12, S7, and the elongation
factors EF-G and EF-Tu constitute a fourth operon in the str
cluster (Fig. 5). This operon has undergone several alterations
in the course of plant evolution. It persists intact in cyanobacteria (422, 641), but the fiusA gene encoding EF-G is absent
from all chloroplast genomes analyzed so far and has presumably been relocated to the nucleus. In Cyanophora paradoxa,
the cyanelle str operon includes rpsl2, rps7, tufA, and rpslO,
which are processed from a primary transcript into two dicistronic mRNAs (68, 69, 368). The rpslO gene is also downstream from tufA in Porphyra and Cryptomonas species (517).
In the Euglena chloroplast, the rpsl2 and rps7 genes constitute
one operon and the tufA gene remains adjacent but is separately transcribed (430). In land plants, where tufA is a nuclear
gene (15), the rpsl2 gene has been split, with the second and
third exons remaining proximal to rps7 and the first exon
encoded separately downstream from rpl20 (183, 187, 649).
Lew and Manhart (352) have recently reported that the rpsl2
gene is also split in a green alga, Spirogyra maxima. This alga is
believed to represent a relatively early stage in the charophyte
lineage leading to land plants. The rpsl2 mRNA is assembled
by trans-splicing (264, 313, 737). In three species of the
angiosperm genus Anemone, the second rpsl2 intron has been
lost secondarily, in conjunction with expansion of the inverted
repeat and several inversions within the chloroplast genome
(269).
In two Chlamydomonas species, the rpsl2 operon has been
further disrupted. In C. reinhardtii, the uninterrupted rpsl2
gene (364) is separated from tufA by about 40 kb and is
cotranscribed with the psbJ and atpI genes encoding photosynthetic proteins (253, 572). The entire rps7 gene is located in the
other single-copy region about 50 kb away, 5' to and cotranscribed with the atpE gene (253). In C. moewusii, rpsl2, rps7,
and tufA are also widely separated; both rps7 and rpsl2 have
been completely sequenced and are uninterrupted (655).
Most of the remaining chloroplast-encoded genes for ribosomal proteins are transcribed either separately or in operons
that also contain genes for photosynthetic proteins (606, 608).
The rp133 and rpsl8 genes are cotranscribed in land plants,
whereas the corresponding genes in E. coli are each part of a
different operon. The rpl21 gene, which is monocistronic in the
Marchantia chloroplast genome (312), has not been found in
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
schemes are the same. Even the well-characterized ribosomal
proteins of E. coli are not numbered according to their
migration on two-dimensional sodium dodecyl sulfate-polyacrylamide gels. Since most of the chloroplast ribosomal
proteins identified on gels have not yet been correlated with
sequenced genes, organism-specific terminologies are sometimes used, e.g., the numbering system of Mache et al. (378)
and Dorne et al. (119, 120) for spinach, the system of Capel
and Bourque (73) for tobacco, and that of Schmidt et al. (547)
for C. reinhardtii. When used here, such designations will be
given in quotation marks as "L-13," etc. However, in cases in
which equivalence has been established, designations of the
chloroplast ribosomal proteins and the genes encoding these
proteins have been changed to indicate the E. coli ribosomal
proteins to which they correspond. For example, seven of the
ribosomal proteins from chloroplast ribosomes of spinach have
been purified by Schmidt et al. (540) and shown by N-terminal
sequencing to be equivalent to seven E. coli proteins (S12, S16,
S19, L20, L32, L33, and L36), whose homologs are encoded by
chloroplast DNA. Those chloroplast and nuclear genes encoding chloroplast ribosomal proteins corresponding to those of E.
coli are designated rps- or rpl- followed by numbers equivalent
to the similar bacterial ribosomal protein designation (S1 to
S21 for small-subunit ribosomal proteins and Li to L36 for
large-subunit ribosomal proteins [241, 606]). Thus, rps4 encodes protein S4 and corresponds to E. coli rpsD, rpl2 encodes
protein L2 (E. coli rplB), etc.
Previous estimates of the number of chloroplast ribosomal
proteins in the small and large subunits have been in the range
of 22 to 31 and 32 to 36, respectively (73, 119, 156, 495, 547),
i.e., at least as many as in E. coli, in which 21 and 33 proteins
have been identified in the small and large subunits, respectively. Part of the variability in these estimates is undoubtedly
the result of differing isolation and electrophoretic conditions.
In some circumstances these factors may cause certain proteins, particularly those of higher molecular weight, to be
excluded from gels (see references 510 and 547 for discussion).
715
716
MICROBIOL. REV.
HARRIS ET AL.
S10
str
E. coil operons
812
LI
fE tf
18D
810
123
810L225183 IL16
Cyanophora
L EJuf
812D
810
L3 L2 81L22
Porphyra
81 IEI
810
18
L4
L23 L2
Euglena
C. relnhardtll
83 I L16
8
A
EjJiJ1 83 16 12
A
812j[E E.J
i]
Ri~JEE]
Marchantla
812'
1!
Nicotlana
8
i
819
1
alpha
apC
814 88
16118
15ER|
Porphyra
114
Euglons
E1
rEli
88
16
116
85
IE130 &K1S lIlI 136 I
1~~~~
8131111 || S4 IiFPOAII 117 I
ElbElJ_rpo
85
88
188
ELE16
E
1L16
123123T12~J[ 19[GITi
S i3
| 16
i~jr~I3I j1
E coil operons
EjE7
83
EREEJ~~
rpo
_JE
C. relnhardtll
EE1
Marchantla
_136 |
Epifagus
Nicotlana
ES
FIG. 5. Conservation of ribosomal protein gene clusters in chloroplast genomes, showing retention of some (but not all) genes of the closely
adjacent str, S10, spc, and a operons of E. coli (12), in Cyanophora paradoxa (598), P. purpurea (514, 517), Euglena gracilis (243), C reinhardtii (43,
277), Marchantia polymorpha (471), Epifagus virginiana (712, 714), and Nicotiana tabacum (560). Shaded boxes indicate genes that have been lost
from the corresponding operon but have been identified elsewhere in a given plastid genome. For example, rps7 and tuf4 are present in the C
reinhardtii chloroplast genome but have become separated from rpsl2. In Cyanophora paradoxa and P. purpurea, the operon begins with the rpl3
gene (A) and ends with the rpsl2, rps7, tufA, and rpslO genes (517, 598). The rpsl2 gene in land plants is split, and the 3' portion of the gene remains
proximal to rps7.
the Euglena, rice, or tobacco chloroplast genomes (243, 265,
560) and has been identified as a nuclear gene in spinach (408,
578). Conversely, rpsl6 is a chloroplast gene in all angiosperms
so far examined and in Euglena, Cyanophora, and Porphyra
species (Table 3) but is absent from the Marchantia and Pinus
thunbergii chloroplast genomes (614, 654).
In E. coli and Bacillus subtilis, as well as in the cyanobacterium Synechocystis sp., the genes encoding Li, L10, Lll, and
L12 are clustered (539, 564). The rpll, rplll, and rp112 genes
also form a cluster in the cyanelle genome, but rpllO is
apparently missing (32). The rpoB and rpoC genes, which are
part of the same cluster in E. coli, were found elsewhere in the
Synechocystis genome and in the cyanelle genome. None of
these four ribosomal protein genes has been found in any land
plant chloroplast genome, but rpl12 is now known to be a
chloroplast gene in Euglena gracilis, located some distance
from the rpoB and rpoC genes (243).
Correspondence of Chloroplast Ribosomal Proteins to
Bacterial Ribosomal Proteins
Of the 54 ribosomal proteins that constitute the E. coli
ribosome, the chloroplast equivalents of 44 have been identified by sequencing of nuclear or chloroplast genes from one or
more organisms (Table 3). Derived amino acid sequence
identities for these proteins with their equivalents in E. coli are
mostly in the range of 35 to 55%, with S12 showing considerably greater conservation (Table 3). In addition, at least three
distinct genes for chloroplast ribosomal proteins that show no
obvious sequence similarity with any bacterial ribosomal protein have been found in the nuclear genomes of pea and
spinach (192, 290, 741).
In general, the chloroplast-encoded ribosomal proteins show
greater immunological cross-reactivity with bacterial ribosomal
proteins than those encoded in nuclear genes (510). The
chloroplast-encoded proteins also show somewhat greater
sequence identity to their counterparts fromE. coli than do the
nucleus-encoded ones (Table 3). Subramanian et al. (608)
made the interesting point that of 15 ribosomal proteins that
can be individually eliminated by mutation in E. coli without
total loss of viability (103, 104), the equivalent of only one, L33,
is chloroplast encoded in land plants. They suggest that
location of particular chloroplast ribosomal protein genes to
the nuclear or chloroplast genome may be related to the
essential roles of these proteins in ribosome assembly or function.
In the following section we discuss each ribosomal protein in
turn, briefly describing what is known about its function and
structure in bacteria and indicating the chloroplast equivalents
that have been identified. Table 3 provides a summary of
references for sequence information to complement this text.
Proteins of the Small Subunit
Protein SI is essential for mRNA binding in E. coli and may
play an important role in initiation of translation of mRNAs
that lack a Shine-Dalgarno sequence (604, 666). The gene
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
Epifagus
Cyanophora
129
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
717
TABLE 3. Chloroplast and cyanobacterial ribosomal proteins that have been identified by gene or protein sequence
Proteina
Taxon
GenBank accession no(s).
E.
Locationa colib
N.
tabacumb Reference(s)
%S %I %S
Si
S2
Porphvra
purpurea
-a oeraea
Spinacia oleracea
-Spra
X16004, X75651
X64567 (partial)
X61798, M81884
X70810, Z11874
X04465
Z00044
X15901
X05917, X03912
X05916
X53651
M35396
X17318, X52270
49 26 59c 38c 517
48 22 100 100 178
C
C
C
C
C
C
C
C
C
C
C
52 31 56
C
C
66
58
57
63
61
58
61
66
61
84
59
59
48
38
35
45
41
37
42
47
40
71
39
39
65
92
60
83
100
87
94
70
95
60
86
87
33 566
634
49 598
85 435,712,714
40 88, 243
73 659
100 560, 561
79 265
87 97, 278
50 517
92 278
42 536
78 267
79 282, 587, 588
S3
Chlamydomonas reinhardtii 5' X66250
Chlamydomonas reinhardtii 3' X66250
M30487
Cyanophora paradoxa
M81884
Epifagus virginiana
Euglena gracilis
X70810, Z11874, M37463
Gracilaria tenuistipitata
M32638
Marchantia polymorpha
X04465
Nicotiana tabacum
Z00044
X15901
Oryza sativa
Porphyra purpurea
X13336
Spinacia oleracea
Zea mays
Y00340, M31336
C
C
C
C
C
C
C
C
C
C
C
C
44
57
72
60
69
64
67
64
66
68
65
65
25
36
51
35
51
46
43
39
40
51
42
40
49 25 172, 366
56 34 172, 366
67 47 423
84 75 712,714
58 35 88, 243
65 43 294
76 62 186
100 100 560, 561
83 70 265
69 46 517
95 89 742
84 72 417
S4
Chlamydomonas reinhardtii
Chlorella ellipsoidea
Cryptomonas 4)
Cyanophora paradoxa
C
C
C
C
C
C
C
C
C
C
C
C
59
65
64
63
56
56
61
58
61
62
58
59
38
44
44
41
35
35
38
36
38
38
38
38
64 48 277, 511
66 52 734
72 58 127
74 59 32
85 76 712, 714
70 51 243
83 76 659
100 100 560, 561
89 80 265
72 56 517
95 92 22, 742
88 79 610
C
C
64 42
65 39
423
517
C
57 28
517
Epifagus virginiana
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
Spinacia oleracea
Zea mays
S5
Cyanophora paradoxa
Porphyra purpurea
S6
Porphyra purpurea
S7
Anacystis nidulans
Astasia longa
Chlamydomonas moewusii
Chlamydomonas reinhardtii
Cryptomonas 4)
Cuscuta reflexa
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Glycine max
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
Spirodela oligorhiza
Spirogyra maxima
Spirulina platensis
D10997
X51511
M81884
X70810, Z11874, M22010
X04465
Z00044
X15901
M16878
X01608
M30487
X17442
X14385, X75652
X53977 (partial; see text)
X52912
X72584
X52497
M81884
X70810, X06254, X00480
X07675, X05013
X04465
Z00044, M19073
X15901
X04508 (partial)
L07932
X15646
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
69
48
60
56
69
62
67
62
62
63
66
62
60
67
54
26
38
37
49
43
49
43
40
43
43
43
43
48
72
50
64
63
70
100
71
95
62
99
88
100
92
72
66 48 82
69 55 72
52
29
42
44
55
98
53
91
41
97
78
100
85
58
422
565
655
509, 519
122
237
326
712, 714
243, 430
672
659
560,561
265
517
498
71 352
54 72
Continued on following page
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Astasia longa
Conopholis americana
Cyanophora paradoxa
Epifagus vitginiana
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Pisum sativum
Porphyra purpurea
Spinacia oleracea
Spirulina platensis
Triticum aestivum
Zea mays
X66135, M82923
%I
C
N
718
MICROBIOL. REV.
HARRIS ET AL.
TABLE 3-Continued
N.
E.
GenBank accession no(s).
Taxon
Protein'
Location"
colib tabacumb Reference(s)
%S %I %S %I
S8
Zea mays
M17841
C
60 43 92
Astasia longa
X16004, X75651
C
C
C
C
C
C
C
C
c
C
C
C
C
60
65
69
68
62
62
67
65
34
44
46
46
38
48
46
42
62
72
53
62
41
51
37
41
c
c
c
c
62 42
62 41
64 44
122
598
243
517
C
C
C
71 52
71 50
72 49
122
68, 451, 452
517
C
C
C
C
C
C
C
C
C
C
72
71
58
72
71
72
72
72
72
72
S9
S10
Sil
X13336
X06734
Cryptomonas 4D
Cyanophora paradoxa
Euglena gracilis
Porphyra purpurea
X52912 (partial)
Cryptomonas 4D
Cyanophora paradoxa
Porphyra purpurea
X52912
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Pisum sativum
Porphyra purpurea
Spinacia oleracea
Zea mays
S12
X16548
M30487
M81884
X70810, Z11874
X04465
Z00044
M60180 (partial)
X15901
Anacystis nidulans
Chlamydomonas reinhardtii
Cryptomonas 4D
Cuscuta reflea
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Glycine max
Marchantia polymorpha
Nicotiana plumbaginifolia
Nicotiana tabacum
Oryza sativa
Pinus contorta
Porphyra purpurea
Spinacia oleracea
Spirodela oligorhiza
Spirogyra maxima
Spinulina platensis
Triticum aestivum
Zea mays
X70810
X52143, M35206
M81884
X70810, Z11874, M22010
X04465
Z00044
X15901
X15645, X05029
X03496
M35831
X17442
M29284
X52912
X72584 (partial)
X52497
M81884
X70810, X00480, X06254
X07675, X05013
X04465, X03661, X03698
L12250, L12366
X03481, Z00044
X15901
L28807 (partial)
(partial)
X04508 (partial)
L07931, L07932
X15646
X54484 (partial)
X60548, M17841, M17842
S13
Cyanophora paradoxa
Porphyra purpurea
S14
Astasia longa
Chlorella ellipsoidea
Chlorella-like alga
Cyanophora paradoxa
X16004, X75651
D10997
M74441, M81884
Epifagus virginiana
X61798
X70810, Z11874, X15240
Euglena gracilis
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
53
54
38
51
55
52
54
55
54
52
64 38
69 53
67 47
67 47
89 84
64 44
78 59
100 100
86
68
89
86
72 55 598
90 83 712, 714
69 44 243, 477
89 79 186, 659
100 100 560, 561
87 74 265
93 84 504, 506
74 55 517
99 90 571
88 73 401
82 74 89
76 68 84
82 73 90
83
77
82
78
81
79
79
79
77
67
69
70
71
71
71
67
88
92
85
98
94
100
- d
94
80 73 88
81 73 90
82 74 88
C
C
79 67 93
C
C
71 54
73 52
C
C
C
C
C
C
62
65
64
65
56
61
76
47
79
79
566
277
69
423
712, 714
88, 243
186
560, 561
715
265
517
742
400
46 68
50 67
48 65
46 71
39 94
42 61
81 422
78 364
84 122
238
84 326
90 712, 714
73 243, 430
98 672
92 187, 659
100 276
d 183, 560, 561
89 265
89
80 517
540
498
87 352
81 72
218
89 204, 687
598
517
566
734
6
598
435, 712, 714
88, 243
Continued on following page
55
52
52
54
90
46
Downloaded from http://mmbr.asm.org/ on March 6, 2016 by PENN STATE UNIV
Chlamydomonas reinhardtii
Cyanophora paradoxa
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oenothera ammophila
Oryza sativa
Porphyra purpurea
Spinacia oleracea
Zea mays
85 204
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
719
TABLE 3-Continued
E.
Proteina
Taxon
GenBank accession no(s).
X04465
Z00044
X15901, X13208
X05394
S15
S16
Reference(s)
X04131
Y00359, M16559
C
C
C
C
C
C
C
58
56
56
57
56
54
56
44
41
40
38
40
40
40
82 75 659
100 100 560, 561
92 87 95, 265
85 79 344
70 56 517
90 90 307
92 87 523,586
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Secale cereale
Zea mays
X04465
Z00044
X15901
X14811
X52614
C
C
C
C
C
53
61
58
59
60
36
36
36
38
41
72 58 312
100 100 560, 561
82 71 265
81 69 501
86 77 170
Cyanidium caldarium
Hordeum vulgare
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
Sinapis alba
Solanum tuberosum
Zea mays
X62578
X52765
C
C
C
C
C
C
C
C
59
62
60
66
58
62
39
38
37
39
42
39
S17
Arabidopsis thaliana
Pisum sativum
Porphyra purpurea
J05215, Z11151
M31025
N
N
C
61 34 72e 55e 196, 640
54 29 100 100 195, 196
69 49 54e 39e 517
S18
Chlamydomonas reinhardtii
Cyanophora paradoxa
X17498
M81884
X70810, Z11874
X04465
Z00044
X15901
C
C
C
C
C
C
C
C
C
53
69
58
61
58
56
55
69
55
34
47
34
37
38
37
34
48
34
63 41 348
68 54 163
86 81 712, 714
70 48 134
88 74 186
100 100 560, 561
79 72 265
72 51 517
75 70 686
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
63
78
83
65
71
75
77
75
75
65
44
67
70
47
57
54
62
56
56
45
76 57
65 45
66 43 211
81 62 277
85 68 163
84 83 712, 714
72 54 88, 243
97 92 584
88 80 186
100 100 745
100 100 560, 561, 612
84 70 265
3
88 84 448
76 60 517
454
97 92 635, 745
82 70 415
Cyanophora paradoxa
Porphyra purpurea
C
C
53 34
51 33
32
517
Cyanophora paradoxa
C
C
N
65
62
64
61
32
517
300
539
Epifagus viginiana
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
Zea mays
S19
Astasia longa
Chlamydomonas reinhardtii
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Glycine max
Marchantia polymorpha
Nicotiana debneyi
Nicotiana tabacum
Oryza sativa
Petunia hybrida
Pisum sativum
Porphyra purpurea
Sinapis alba
Spinacia oleracea
Zea mays
S20
Z00044, X03415
X15901
X13609
Z11741 (partial)
X60823
X56673
X75653
X17498
M81884
X70810, Z11874, M37463
X06429
X04465
Z00044, V00163
X15901
M35955, M37322 (partial)
X59015
X17331 (partial)
X13336, X00797
Y00141
63 41 385
90 86 556
100 100 560, 561
87 82 265
71 51 517
87 81 450
138
63 37 90 84 293
73 55
78 62
S2lf
Ll
Porphyra purpurea
Spinacia oleracea
Synechocystis strain PCC
X73005
45
41
43
46
6803
L2
Astasia longa
X75653
C
66 51 71
53 211
Continued on following page
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Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Pisum sativum
Porphyra purpurea
Spinacia oleracea
Zea mays
N.
tabacumb
Locationa col
%S %I %S %I
720
HARRIS ET AL.
MICROBIOL. REV.
TABLE 3-Continued
Proteina
Taxon
X17498
M81884
X70810, Z11874, M37463
X06429 (partial)
X04465
X00798
Z00044
X15901
M35944, M37322 (partial)
X59015
X65615
X00797
(partial)
Zea mays
X53066, X12851, X62070
L3
Cyanophora paradoxa
Porphyra purpurea
X17498
L4
L5
L6
no(s).
Locationa
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
C
E.
colib
N.
tabacumb Reference(s)
%S %I %S
%I
70
68
64
68
53
52
47
52
60
61
93
55
64
60
66
64
49
43
48
49
68
67
66
63
50
50
48
44
65 49
75
76
96
72
277
163
712, 714
88, 243
584
81 73 186
91 88 745
100 100 560, 561
93 90 265
3
94 93 448
73 59 517
97 97 455
90 85 745
46
93 90 299
C
C
62 45
63 45
161
517
Porphyra purpurea
C
60 38
517
Astasia longa
X16004, X14384, X75651
Chlamydomonas reinhardtii
X16548
Cyanophora paradoxa
Cyanophora paradoxa
M30487
Euglena gracilis
X70810, Z11874, X17051
Porphyra purpurea
C
C
C
C
C
C
66
76
76
76
69
74
44
51
51
52
44
54
566
277
69
423
517
Cyanophora paradoxa
Porphyra purpurea
X16548, M30487
C
C
63 38
58 41
517
Arabidopsis thaliana
Z11509, Z11129
X14019
N
N
C
88, 243
69, 423
L7 (see L12)
L8 (see L10)
L9
L10
Pisum sativum
Porphyra purpurea
Synechococcus sp.
Synechocystis strain PCC
6803
X63765
D10716
53
54
61
56
57
Synechocystis strain PCC
X53178
53 26
32
34
30
36
34
82e
100
55e
58e
69e
100
33e
34e
640
192
517
439
62~ 38e 388
539, 564
6803
Lll
Arabidopsis thaliana
Cyanophora paradoxa
Porphyra purpurea
Spinacia oleracea
Synechocystis strain PCC
N
C
C
X56615
X73005
N
X68046 (a)
X68046 (b)
X68046 (c)
N
N
N
6803
L12
Arabidopsis thaliana
Arabidopsis thaliana
Arabidopsis thaliana
Cyanophora paradoxa
Euglena gracilis
Nicotiana sylvestris
Nicotiana tabacum
Nicotiana tabacum
Porphyra purpurea
Secale cereale
Secale cereale
Spinacia oleracea
C
X70810
S93166
X62368
X62339
N
N
N
X68325
X68340
J02849
N
N
N
C
C
63
71
70
63
75
51
55
54
52
61
93C
75C
80c
100
82C
69
64
69
68
66
69
70
70
74
70
69
75
46
40
86
71
86
46
47 63
47
48
48
49
58
45
44
53
88C
63c
65c
100
69C
543
32
517
579
539
75 543, 689
59 543, 689
75 543, 689
39 32
63 44 243
99 99 354
99 99 155
100 100 155
70 49 517
82 70 544
80 68 544
89 78 201
Continued on following page
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Chlamydomonas reinhardtii
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Glycine max
Marchantia polymorpha
Nicotiana debneyi
Nicotiana tabacum
Oryza sativa
Petunia hybrida
Pisum sativum
Porphyra purpurea
Sinapis alba
Spinacia oleracea
Triticum aestivum
GenBank accession
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
VOL. 58, 1994
721
TABLE 3-Continued
Proteina
GenBank accession no(s).
Taxon
Synechocystis strain PCC
Locationa
X53178, X67516
E.
N.
coli'
tabacumb
Reference(s)
%S %I %S
%I
78 62 70
45 539, 564
6803
L13
Porphyra purpurea
Spinacia oleracea
J04461
66 51 69C 57C 517
71 54 100 100 490
77
80
76
83
80
Chlamydomonas reinhardtii
Cyanophora paradoxa
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oenothera ammophila
Oryza sativa
Porphyra purpurea
Spinacia oleracea
Vigna unguiculata
Zea mays
X14062
M30487
X70810, Z11874
X04465
Z00044
M60179, M60180 (partial)
X15901
X13336
M80799 (partial)
X06734
C
C
C
C
C
C
C
C
C
C
C
L15
Arabidopsis thaliana
Pisum sativum
Z11507, Z11508
Z11510
N
N
61 41 76e 68e 640
63 44 100 100 640
L16
Chlamydomonas reinhardtii
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Gracilaria tenuistipitata
Marchantia polymorpha
Nicotiana tabacum
Oenothera ammophila
0ryza sativa
Porphyra purpurea
Spinacia oleracea
Spirodela oligorhiza
Vigna unguiculata
Zea mays
M13931
M30487
M81884
C
C
C
C
C
C
C
C
C
C
C
C
C
C
79
76
76
73
72
75
78
57
54
50
53
60
56
56
76
72
76
75
54
55
53
54
L18
Cyanophora paradoxa
Porphyra purpurea
M30487
C
C
62 49
65 45
423
517
L19
Cyanophora paradoxa
Porphyra purpurea
Synechocystis strain PCC
C
C
69 46
69 47
72 56
598
517
542
C
C
C
C
C
C
C
C
C
C
C
56
66
72
60
55
33
46
53
41
29
55
68
71
81
54
27
44
52
77
31
54
58
54
62
60
26
31
29
33
32
54C
57C
55C
52C
32C 385
30C 598
53 31 60
62 44 70
L14
X70810, Z11874
M32638
X04465
Z00044
M60179 (partial)
X15901
X13336
X03834
M80799 (partial)
Y00375, X06734 (partial)
57
58
60
58
55
88 71
89 69
85 63
94 80
100 100
80 54 93
80 60 85
82 58 94
85
67
88
80 53 92
81
82 69
88 70
90 81
77 65
77 65
90 79
100 100
90
81
96
90
86
68
90
85
372
423
88, 243
186
560, 561
715
265
517
742
8
400
373
423
712, 714
88, 243
294
186
560, 561
715
265
517
742
497
8
400, 418
L17f
X72627
6803
L20
Astasia longa
Chlamydomonas reinhardtii
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Glycine max
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
Zea mays
L21
L22
X75653
X62566
X17063
M81884
X70810, Z11874, Y00143
X07676 (partial)
X04465
Z00044
X15901
X60548
Spinacia oleracea
M57413, M64682
C
C
C
C
N
Astasia longa
X75653
M30487, X17498
C
C
Cyanidium caldarium
Cyanophora paradoxa
Marchantia polymorpha
Porphyra purpurea
Cyanophora paradoxa
X04465
211
736
69
712,714
243, 396
673
64 45 76 57 186
63 41 100 100 560, 561
59 41 78 67 265
69 47 64 46 517
58 41 81 71 687
30c 312
32C 517
100 100 340, 578
34 211
47 163, 423
Continued on following page
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C
N
722
MICROBIOL. REV.
HARRIS ET AL.
TABLE 3-Continued
N.
E.
Proteina
GenBank accession
Taxon
no(s).
Locationa
colib tabacumb Reference(s)
%S %I %S %I
X70810, Z11874, M37463
M32638
X04465
Z00044
X15901
M60953
M60951, M60952
Arabidopsis thaliana
Astasia longa
Chlamydomonas reinhardtii
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
Sinapis alba
Spinacia oleracea
X66414
X75653
Triticum aestivum
Zea mays
L24
Nicotiana tabacum
Pisum sativum
Spinacia oleracea
Porphyra purpurea
C
C
C
C
C
C
N
C
C
59
59
59
54
53
50
58
66
47
38
40
41
36
32
35
43
49
28
C
C
C
C
C
C
C
C
C
C
C
C
50
38
53
42
46
48
51
46
50
25
18
31
17
25
23
26
28
25
97 95 374
42 21 211
55 39 277
53 32 88, 243
77 55 186
100 100 560, 561
94 84 265
63 36 517
98 96 455
635
51 26 94 83 46
51 26 93 84 419
N
N
N
C
64
56
58
51
38
34
34
33
C
D26101 (partial)
C
C
C
C
185
363
185
185
185
73 59 100 100 154
77 58 77 61 185
185
74 61 69 57 517
185
X68078
N
57 36
731
Y00329
X70810, Z11874, M37463
X04465
Z00044
X15901
X65615
X07462 (pseudogene?)
X12850
X07864
X14020
M58522
52 42
64 42
68 54
100 100
70 54
78 67
72 53
66 48
66 52
100 100
86 78
76 61
61 49
88, 243
295
186
560, 561
265
193
193
517
416
153
192
75
517
L25f
L27
Calyptrosphaera sphaeroidea
Chlamydomonas reinhardtii
Chrysochromulina alifera
Chrysochromulina hirta
Cyanidium caldarium
Nicotiana tabacum
Pleurochrysis carterae
Pleurochrysis haptonemofera
Porphyra purpurea
Porphyridium cruentum
D26097 (partial)
N-terminal amino acid sequence only
D26096 (partial)
D26099 (partial)
D26098 (partial)
M75731
D26100
D26102 (partial)
N
C
C
C
N
L28
Nicotiana tabacum
L29
Porphyra purpurea
C
51 24
517
L31
Porphyra purpurea
C
60 37
517
L32
Astasia longa
Brassica rapa
Euglena gracilis
Lycopersicon esculentum
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
Vicia faba
Zea mays
L30f
L33
Cyanophora paradoxa
Epifagus virginiana
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Porphyra purpurea
X16004, X75651
Z26332
X70810
D17805 (partial)
X04465
Z00044 (as ORF55)
X15901
C
C
C
C
C
C
C
C
X51471
X64099
X17498
M81884
X04465
Z00044
X15901
C
C
C
C
C
C
C
C
56 38 55 45 568
48 15 85 83 582
48 30 50 35 243
668
43 18 74 61 186
46 18 100 100 733
47 22 67 56 265
44 20 57 48 517
52 26 83 68 256
43 18 74 61 688
60
52
56
52
60
59
42
37
44
37
42
43
78 62
93 85
80 71
100 100
82 73
67 50
163
712,714
186
560, 561
265
517
Continued on following page
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L23
Euglena gracilis
Gracilaria tenuistipitata
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Pelargonium zonale
Pisum sativum
Porphyra purpurea
Zea mays
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
VOL. 58, 1994
723
TABLE 3. Chloroplast and cyanobacterial ribosomal proteins that have been identified by gene or protein sequence
E.
Proteina
Taxon
GenBank accession no(s).
Locationa
N.
colib tabacumb Reference(s)
%S %I %S %I
Zea mays
X56673
Cyanophora paradoxa
Porphyra purpurea
L35
Cyanophora paradoxa
Porphyra purpurea
Spinacia oleracea
X17063
Astasia longa
Cryptomonas 'F
Cyanophora paradoxa
Epifagus virginiana
Euglena gracilis
Marchantia polymorpha
Nicotiana tabacum
Oryza sativa
Pisum sativum
Porphyra purpurea
Spinacia oleracea
Zea mays
X16004, X75651
X62348 (partial)
L36
CS-S5, PSrp-1, "S22" or "S30"g Spinacia oleracea
Spinacia oleracea
M60449
57 38 81
C
C
49 40
60 49
C
C
N
55 38 61C 45c 69
52 36 67C 50c 517
64 42 100 100 577
C
68 46 73
X03496
M35956
C
C
C
C
C
C
C
C
C
X59270, X15344
M55322
598
517
C
C
M81884
X70810, Z11874
X04465
Z00044
X15901
Y00468, X15645
N
N
78
81
73
86
86
89
84
81
84
89
62
57
51
62
62
68
62
59
62
68
75 686
92
95
84
95
100
95
97
95
97
95
57 566
124
76 598
92 712, 714
65 88, 243
86 186
100 560, 561
92 265
86 505, 506
70 517
95 571
92 402
28, 741
290
"S31" or SCS239"
Spinacia oleracea
PsCL189
Pisum sativum
X14021
N
192
"L40999
Spinacia oleracea
M58523
N
75
541, 674
PsCL25M
Pisum sativum
X14022
N
192
a Proteins Si through S21 and LI through 136 are named by reference to similar sequences in E. coli, and the location of the gene encoding them (N, nuclear; C,
chloroplast or cyanelle) is given for all eukaryotic species. A few additional chloroplast ribosomal proteins with no obvious similarity to E. coli proteins have been
identified and appear at the end of the table.
b The percent similarity (%S) and percent identity (%I) to the E. coli and tobacco proteins or other reference land plant proteins were calculated by the gap routine
of the Genetics Computer Group sequence analysis package.
c Tobacco sequence not available; spinach used instead for comparison.
d The
complete tobacco genome sequence (Z00044) has a stop codon in the terminal exon encoding the S12 protein, whereas the sequence by Fromm et al. (183)
(X03481) shows a full-length protein comparable to that from other chloroplast genes. The Swissprot sequence (P06309) omits the terminal residue (Tyr) of the first
exon of this protein. The composite sequence with these corrections made is identical to that for N. plumbaginifolia and was used for the comparisons given here.
I
Tobacco sequence not available; pea used instead for comparison.
f No equivalent found so far in chloroplasts.
g Proteins for which no equivalent appears to exist in E. coli.
h
Small, basic protein found in spinach ribosome preparations.
encoding this protein is absent from the completely sequenced
chloroplast genomes of tobacco, rice, Marchantia polymorpha,
and Euglena gracilis (243, 558) but appears in the Porphyra
purpurea chloroplast genome (514). A nuclear gene encoding
this protein has been identified in spinach (178, 179) and
shown to have a light-independent, leaf-specific pattern of
expression under the control of a negative nuclear factor, SlF,
that down-regulates its promoter (740). Hahn et al. (240)
reported that monoclonal antisera to E. coli Si reacted with a
chloroplast protein of spinach. Polyclonal antisera to two
chloroplast-synthesized ribosomal proteins of C. reinhardtii
("S-7" and "S-11" [547]) reacted with E. coli Si (510), as did
antisera to mixed chloroplast ribosomal proteins of spinach
(119). Subramanian et al. (608) also suggested the presence of
a chloroplast Si homolog in maize on the basis of affinitybinding experiments with a matrix-bound poly(U) column.
In E. coli the S2 protein interacts primarily with the 3'
domain of the 16S rRNA in the 960 loop region and can be
cross-linked to proteins S3, S5, and S8 (500, 595, 599). The rps2
gene encoding a ribosomal protein homologous to E. coli S2
has been found in chloroplast genomes from diverse species
(Table 3), typically mapping between the rpoB and rpoC genes
encoding subunits of RNA polymerase and the atpI and atpH
genes encoding ATP synthase subunits. The deduced amino
sequences of S2 proteins from land plants are highly conserved
(Table 3), and those of three monocots (wheat, rice, and
maize) are nearly identical to one another. A nuclear DNA
sequence in spinach with substantial homology to a portion of
the chloroplast rps2 gene is thought to be an example of
"promiscuous DNA," i.e., a DNA sequence found in more
than one genetic compartment (85).
Protein S3, like S2, interacts with nucleotides in the 960 and
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L34
C
724
HARRIS ET AL.
ending with rps8 (Fig. 5) but is separated from this operon by
exon 1 of the psaA gene and two tRNA genes, tmM and trnG
(277). In Euglena gracilis, rps4 is transcribed together with
rpsll (242, 597). In the alga Cryptomonas 'F, rps4 is close to
rbcL on the same strand and is flanked by tRNAArg on the
opposite strand (127), whereas in Cyanophora paradoxa,
tRNA et and tRNAG'Y are adjacent to rps4 but on the
opposite strand (32, 598).
In E. coli, the S5 protein is part of the recognition complex
(466) and is the first protein of the small subunit whose crystal
structure has been determined (from B. stearothermophilus
[507, 508]). The protein appears to be a somewhat elongated
molecule with two distinct domains. Mutations affecting amino
acids 20 to 22 of E. coli S5 can confer spectinomycin resistance,
whereas mutations at amino acids 104 and 112 have a ram
phenotype and suppress streptomycin dependence mutations
in protein S12 (508). Some of the latter class of mutants are
also neamine resistant (721). These two conserved regions of
the S5 protein are thought to be the sites of its interaction with
rRNA (508). Genes encoding a protein with homology to E.
coli S5 have been sequenced from the cyanelle genome of
Cyanophora paradoxa (368, 423) and from the P. purpurea
chloroplast genome (517). No equivalent gene has been found
in any land plant chloroplast genome, however, nor does it
appear in the chloroplast genome of Euglena gracilis.
The S6 ribosomal protein of E. coli is implicated in mRNA
and tRNA binding and in termination (465, 632), and it
appears to be a component of the platform region of the 30S
particle (432, 622). A plastid equivalent of S6 is known so far
only from Porphyra purpurea (517).
In E. coli, protein S7 interacts with several clusters of
nucleotides in the 3' domain of 16S rRNA, in proximity to S9,
S1O, and S19 (57, 136, 465, 499), and is one of the initiating
proteins of 30S assembly (255). Binding of S7 to 16S riRNA is
a prerequisite to assembly of S9 and S19. As discussed above,
the gene encoding S7 is transcribed together with that for S12
in bacteria and in the chloroplast genomes of most plants and
algae examined (Fig. 5), the principal exceptions so far being
Chlamydomonas species. In C. reinhardtii, the protein encoded
by rps7 corresponds immunologically to the protein that
Schmidt et al. (547) identified as "S-20" (509). Although
derived amino acid sequence identity between chloroplasts and
bacteria is lower for S7 than for S12 (Table 3), antibodies to E.
coli S7 do cross-react with a corresponding small-subunit
protein from spinach chloroplast ribosomes (18).
In E. coli, S8 is an RNA-binding protein that is essential
early in assembly of the 30S subunit and interacts with a highly
conserved site in the central domain of 16S rRNA, designated
by Oakes et al. (466) as the platform ring (also see references
141, 437, 465, and 622). It is associated with proteins S15 and
S17 (57). It also has a key role in translational regulation of the
spc operon in E. coli (719). S8 is moderately conserved
phylogenetically and can be identified with equivalents in
eukaryotic ribosomes (410, 708). The rps8 gene is chloroplast
encoded (Table 3) and is one of at least three genes of the
bacterial spc operon that remain linked in chloroplast genomes
(Fig. 5). Most plastid S8 proteins have a central 4- to 7-aminoacid insertion compared with the E. coli protein, followed by a
highly conserved C-terminal region.
Protein S9 interacts with S7 and S19 in the 3' domain of the
E. coli ribosome (57, 499). Bartsch (18) obtained cross-reactivity of antibody to E. coli S9 with a spinach chloroplast
ribosomal protein, but the gene encoding this protein has not
been found in any of the land plant chloroplast genomes so far
sequenced and is presumed to be nucleus encoded. However,
an rps9 gene does appear in the chloroplast genomes of
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1050/1200 regions of E. coli 16S rRNA (465) and appears from
immunoelectron microscopy studies of the 70S ribosome to
reside near the site to which the polypeptide release factor
RF-2 binds (632). The rps3 gene encoding the equivalent
protein has been sequenced from several chloroplast genomes
(Table 3), where it has been found between rp122 and rp116, as
is true for the corresponding genes in the S10 operon of E. coli
(Fig. 5). In most algae and plants the rps3 gene is uninterrupted, but in Euglena gracilis it contains two introns, one (102
nt) belonging to the group III class (as defined by Christopher
and Hallick [87]; also see reference 86) and the other (409 bp)
being a "twintron" consisting of a 311-nucleotide group II
intron within a 98-nt group III intron (92). Splicing proceeds
sequentially, with the internal 311-nt intron being excised first.
In the chloroplast genome of C. reinhardtii, there is no gene
equivalent to rps3 in the expected location between rp122 and
rp116 (277). However, Fong and Surzycki (172) found a long
open reading frame between the rpoB and rpoC genes, whose
5' and 3' ends would encode a protein with substantial
homology to S3. The central portion of the predicted product
of this open reading frame has no homology to S3, however,
and the DNA sequence does not contain recognizable splice
junctions that would suggest that this region is in fact an intron.
Liu et al. (366) found that this open reading frame is also
present in several other Chlamydomonas species. After transformation of C. reinhardtii cells with a construct containing this
open reading frame interrupted by the bacterial aad antibiotic
resistance gene, the only resistant cells recovered were heteroplasmic for the interrupted and native forms of the gene. In
contrast to transformants in which the same construct was
inserted into other regions of the genome, no homoplasmic
cells containing only the interrupted gene could be obtained,
strongly suggesting that this gene is not only functional but also
essential to cell growth. No single transcript spanning the
whole gene could be detected, however, and the gene product
has not been identified (366).
In E. coli, S4 is one of the primary rRNA-binding proteins
that initiate assembly of the 30S subunit (255, 465) and is
associated with the 5' domain of 16S rRNA, at a junction of
several helices. Together with S5 and S12, S4 participates in a
region designated by Oakes et al. (466) as the recognition
complex on the basis of its demonstrated involvement in
codon-anticodon recognition and translational accuracy. This
region involves the 530 loop, the 900 loop region, and the 5'
end of the 16S molecule which pairs with the region around
residue 912 (Fig. 3). Homologs of all three of these proteins
have been identified in yeast cytoplasmic ribosomes and appear to have similar functions (4). Mutations in the gene
encoding S4 in E. coli suppress streptomycin dependence
mutations in the gene for S12 and increase translational
ambiguity (ram mutants [7, 189, 335, 336, 475). The chloroplast
gene encoding ribosomal protein S4 has been sequenced from
a number of plants and algae (Table 3) and shows a high
degree of conservation in its first 25 amino acid residues and in
a large block of approximately 120 residues in the central
portion of the protein. The C. reinhardtii S4 protein is somewhat longer than all others examined so far, having two
internal insertions and a 22-amino-acid C-terminal extension
(511).
In land plants, rps4 appears to be transcribed singly under
control of its own promoter and is not part of an operon with
other ribosomal protein genes (608). In tobacco, rice, and
Marchantia polymorpha, the rps4 gene is in the large singlecopy region and is preceded by tRNAThr on the same strand
and followed by tRNAser on the opposite strand. In C.
reinhardtii, rps4 follows the large ribosomal protein operon
MICROBIOLE REV.
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
the 16S rRNA and is probably close to S4 in the assembled 30S
subunit (594). Montesano-Roditis et al. (432) have localized
S16 to the 30S body near its junction with the platform, on the
surface facing the 50S particle. In various angiosperms, S16 is
encoded by a chloroplast gene (Table 3), but the rps16 gene is
absent from the Marchantia chloroplast genome (471). It is
found, however, in the plastid genome of the red alga Cyanidium caldarium (385). In tobacco, the rpsl6 gene has an
860-bp intron with boundary sequences similar to the introns in
rpsl2, rp12, and several tobacco tRNA genes (559). The rpsl6
genes of mustard (450), barley (556), and maize (293) also
contain introns, but that of Cyanidium caldarium is uninterrupted (385).
S17 is one of the primary assembly proteins in E. coli and
binds to 16S rRNA in the 5' domain (213, 255, 465, 594). It is
one of only three chloroplast ribosomal proteins of the small
subunit to date for which a nucleus-encoded gene has been
cloned and sequenced (Table 3) (606). This protein contains a
highly conserved region which can be identified in both
bacterial (S17) and eukaryotic (Sli) ribosomal proteins. Comparison of the deduced amino acid sequences of the equivalent
chloroplast S17 and cytosolic Sli ribosomal proteins from
Arabidopsis thaliana with E. coli S17 supports the notion that
chloroplast S17 is derived from a prokaryotic endosymbiont
and not from duplication of the eukaryotic S11 gene (196). The
presence of an rpsl7 gene in the cyanelle genome of Cyanophora paradoxa (368) and in the chloroplast genome of Porphyra purpurea (514) is consistent with this hypothesis.
Proteins S18 and S6 assemble coordinately in the bacterial
ribosome to form part of the platform ring in the central
domain (432, 466, 622). The chloroplast gene encoding S18 has
been found to be part of an operon with rp133 in the completely
sequenced chloroplast genomes of tobacco, rice, and Marchantia polymorpha, as well as in Cyanophora paradoxa, but it
is absent from this operon in Euglena gracilis (Fig. 5). The
angiosperm S18 proteins have N-terminal extensions compared with E. coli, Marchantia polymorpha, and Cyanophora
paradoxa, containing various numbers of repeats of a hydrophilic heptapeptide (686). A C-terminal extension found in the
S18 proteins of rice and maize is missing from this protein in
tobacco (561, 686).
The S19 protein of E. coli interacts with proteins S7, S9, and
S14 and with several helices in the 3' domain of the 16S rRNA
molecule (57). The gene encoding S19 was the first chloroplast-encoded ribosomal protein gene to be identified and
sequenced (612, 745). In plants with the "typical" chloroplast
inverted-repeat structure, the rpsl9 gene and the adjacent rp12
and rp122 genes are located at or near the boundary between
the inverted repeat and the large single-copy region. In tobacco (560) and Marchantia polymorpha (186), rpsl9 is entirely
within the large single-copy region but near the inverted-repeat
junction, whereas in rice (433) the whole gene is within the
inverted repeat. Zurawski et al. (746) found that the first 48
codons of rpsl9 in spinach were in the inverted repeat, with 44
codons homologous to the 3' end of the E. coli gene being
present only on one side of the large single-copy region.
Thomas et al. (635, 636) showed that this complete copy of the
gene was expressed, whereas the rpsl9' sequences beginning in
the other side of the inverted repeat and extending for 66
codons into the adjoining unique sequence region (745) were
not transcribed. The rpsl9 gene also straddles the boundary of
the inverted repeat in Spirodela oligorhiza (494) and in mustard
(454).
S20, which was also identified in early ribosome studies in E.
coli as L26, is a primary RNA-binding protein that interacts
with the 5' domain of the 16S rRNA (255,594). Deletion of the
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Euglena (243), Porphyra (517), and Cryptomonas (122) species
and in the cyanelle genome (598). Overall, the C-terminal
portions of the S9 proteins appear more highly conserved than
the N-terminal portions.
S10 is a late-assembly ribosomal protein of the 3' domain in
E. coli 16S rRNA (465). A gene encoding a homolog of S10 has
been found in the cyanelle genome (68, 451, 452), where it
maps downstream of the petFI gene. Sequences encoding an
S10 protein have also been found in Cryptomonas D (122) and
in Porphyra purpurea downstream of the tufA gene (517).
In E. coli, Sl1 interacts with S6 and S18 in the platform
region of the 30S subunit (466). S11 is highly conserved
phylogenetically, with homologs also identified in eukaryotic
ribosomes (401, 708). There is some variability in length
among Sli proteins, localized to the N-terminal regions. In
chloroplast genomes of land plants, the rpsll gene is part of
the large ribosomal protein operon that terminates in rpoA
(Fig. 5). In Euglena gracilis, in which it is in a separate operon
with rps4, the rpsll gene contains two group III introns (597).
S12 appears to be the most highly conserved of all the small
subunit proteins. The C. reinhardtii S12 protein is sufficiently
similar to its bacterial counterpart that the rpsl2 gene from this
alga can be expressed in E. coli cells and the resulting protein
can assemble and function in the E. coli ribosome (364). In E.
coli, S12 interacts with two regions of the 16S rRNA, the 530
loop and 900 stem-loop. Mutations affecting either the S12
protein or the 16S rRNA regions with which it associates can
confer streptomycin resistance in E. coli by reducing misreading induced by the drug (Table 2). Streptomycin resistance
mutations have also been found at evolutionarily conserved
sites in the S12 proteins or 16S rRNA of Chlamydomonas
species, Euglena gracilis, and tobacco, and streptomycin dependence mutations affecting the S12 protein have been found in
bacteria and in C. reinhardtii (Table 2). Streptomycin-dependent E. coli mutants exhibit hyperaccurate proofreading and
reduced efficiency of binding of EF-Tu (25, 102, 150).
In E. coli, S13 appears to be located at the head of the 30S
subunit, near the center of the surface that faces the 50S
subunit (432). It has been reported to cross-link to S7 and S19
in the 3' domain of the 16S rRNA (599). Genes encoding a
cognate protein have been identified in the cyanelle genome
(598) and in the Porphyra chloroplast genome (517) but have
so far not been reported to occur in other algae or land plants.
The late-assembly ribosomal protein S14 interacts with the
3' domain of 16S rRNA in E. coli (465). The chloroplastencoded Euglena rpsl4 gene is part of the large ribosomal
protein cluster as it is in E. coli, downstream from rp136 and a
tRNAIle gene (457), whereas in other chloroplast genomes it is
found outside this cluster. In land plants, the rpsl4 gene is
located in the chloroplast genome downstream from the psaA
and psaB genes encoding reaction center proteins of photosystem 1 (81, 82, 307, 496, 560). In Cyanophora paradoxa, the rpsl4
gene is upstream of open reading frame ORF512 andpsaA and
is transcribed divergently from these two genes (598). In
Porphyra purpurea, rpsl4 is flanked by petF and petG (514).
S15 is an early-assembly protein in E. coli that interacts with
the central domain of the 16S rRNA, together with S6, S8, and
S18 in the platform ring (57, 151, 438, 465, 466, 622). In
tobacco and liverwort, the rpsl5 gene is in the small single-copy
region of the chloroplast genome (312, 560), whereas in three
monocots (rice [265], rye [501], and maize [170]) it is in the
inverted repeat, very close to the boundary with the small
single-copy region. This gene is missing from the chloroplast
genomes of Euglena gracilis (243) and Porphyra purpurea (517)
and from the cyanelle genome (32, 598).
In E. coli, S16 is a protein associated with the 5' domain of
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HARRIS ET AL.
rpsT gene encoding S20 in E. coli results in increased misreading of all three nonsense codons and a deficiency in assembly
of 30S and 50S subunits to form 70S monomers (534). An rps2O
gene has been identified in the cyanelle genome (32) and in the
Porphyra chloroplast (517).
E. coli S21 interacts with the central domain in the platform
ring (466). No equivalent protein has been identified so far in
the chloroplast ribosome.
families and documented six independent losses of this intron
among dicotyledons.
The L3 and L4 proteins of E. coli both bind to the 23S rRNA
molecule and have been identified with analogous proteins in
archaebacterial and eukaryotic ribosomes (215, 708). Genes
encoding an L3 protein have been sequenced from the Cyanophora cyanelle genome (161) and from the Porphyra chloroplast genome (517). Neither an rp13 nor an rpl4 gene has been
found in the completely sequenced chloroplast genomes of
tobacco, rice, Marchantia polymorpha, or Euglena gracilis
Bartsch (18) found a cross-reaction between antibody to E. coli
L3 and a spinach chloroplast ribosomal protein which has not
been further characterized.
Genes encoding a protein corresponding to the 5S RNAbinding protein LS of E. coli have been found in the Euglena,
C. reinhardtii, Porphyra, Astasia, and Cyanophora plastid genomes (Table 3). However, no equivalent gene has been found
in any land plant chloroplast genome. Antibody to Chlamydomonas chloroplast ribosomal protein "L-13" (547) reacts with
E. coli LS and with a ribosomal protein of Anabaena sp. (510).
A weak reaction was also seen to a spinach protein ("LIO"),
whose site of synthesis is uncertain (121). The Chlamydomonas
"L-13" protein is known to be synthesized in the chloroplast
(547), suggesting that this is the product of the chloroplastencoded rplS gene sequenced by Huang and Liu (277).
TheE. coli L6 protein binds to domain VI of 23S rRNA (90).
Genes encoding an equivalent protein have been found in the
cyanelle genome of Cyanophora paradoxa (69) and the Porphyra chloroplast genome (514).
The protein originally identified as L7 in E. coli is in fact the
aminoacetylated form of L12, and L8 is a complex of L7/L12
and L10 (358).
Protein L9 of E. coli is an elongated protein with distinct
terminal domains which is associated with the protuberance
formed by protein Li and the region of the 23S rRNA to which
it binds (57, 213, 266). Genes encoding a protein equivalent to
E. coli L9 have been sequenced from the nuclear genomes of
pea (192) and Arabidopsis thaliana (640) and from the Porphyra chloroplast genome (517). The E. coli L9 protein crossreacts slightly with antibody to the acidic chloroplast ribosomal
protein "L-30" from C. reinhardtii (510).
E. coli protein L10 (L8) forms the base of the ribosomal
stalk in a pentameric complex with two dimers of L7/L12 and,
like L7/L12, appears to be a universal constituent of eubacterial, eukaryotic, and archaebacterial ribosomes (708). A cyanobacterial gene encoding this protein has been found (539,
564) but no chloroplast equivalent has yet been identified.
Presumably, chloroplast L10 is encoded by a nuclear gene in
plants.
L1i is an early-assembly protein that constitutes part of the
GTPase center in the E. coli ribosome (528) and also has been
identified in eubacterial, eukaryotic, and archaebacterial ribosomes (708). Nuclear genes encoding a chloroplast L1 homolog have been cloned from spinach andArabidopsis thaliana
(543, 579, 606), while plastid genes have been identified in
Porphyra purpurea (517) and Cyanophora paradoxa (32). In E.
coli, L1i has the most extensive posttranslational modification
(nine methyl groups) of all ribosomal proteins (708); the same
modifications occur in the spinach chloroplast Lii in the
corresponding amino acid residues, located in conserved sequence contexts (607). Mutations in Bacillus megaterium and
B. subtilis conferring resistance to the antibiotic thiostrepton
cause the loss of Lii from the ribosomes (16, 101). Lli does
not bind thiostrepton itself in solution but enhances thiostrepton binding to 23S rRNA (102, 639). Bacterial thiostreptonresistant mutants with altered 23S rRNA have also been found
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Proteins of the Large Subunit
In E. coli, ribosomal protein Li forms a prominent ridge on
the large subunit (177, 466, 599) and has been demonstrated to
bind to nt 2100 to 2200 on the E. coli 23S rRNA, a region that
shows a high degree of conservation among chloroplast 23S
sequences. The gene encoding this protein is present in the
cyanelle genome (32) and in the Porphyra chloroplast genome
(517) but is absent from the completely sequenced plastid
genomes of land plants. Antibodies to E. coli Ll cross-reacted
with a spinach chloroplast ribosomal protein (8). cDNAs
encoding chloroplast Li have been cloned from the nuclear
genomes of pea, spinach, and Arabidopsis thaliana, and the
nuclear gene has been isolated and characterized from Arabidopsis thaliana (300).
In E. coli, the L2 protein binds to domain IV of the 23S
rRNA molecule, and cross-links specifically to nt 1818 to 1823
(744), in a stem-loop structure that is part of the peptidyltransferase center and is conserved in chloroplast 23S rRNAs.
Site-directed mutagenesis of a conserved region in the E. coli
L2 protein outside the 23S binding site has been used to
produce temperature-sensitive mutants that are impaired in
assembly of the 50S subunit (526). The L2 protein is encoded
in the chloroplast genomes of all land plants and algae so far
examined (Table 3). The L2 protein itself is moderately
conserved, and its equivalent has been identified in eukaryotic
ribosomes (708). The C. reinhardtii protein "L-1," which is
synthesized in the chloroplast (547), appears to be encoded by
the rpl2 gene since "L-1" antibodies cross-react with E. coli L2
(510). Kamp et al. (292) showed that the N-terminal amino
acid of the L2 protein in spinach is N-methylalanine, the first
demonstration of methylation of a chloroplast ribosomal protein. Several ribosomal proteins of E. coli are methylated, but
L2 is not among these. The maize rpl2 gene begins with an
ACG codon, which is edited to AUG at the transcript level
(321). The 3'-terminal ends of the deduced L2 amino acid
sequences for spinach and Nicotiana debneyi published by
Zurawski et al. (745) appear to lack homology to the corresponding regions from other chloroplast and bacterial L2
proteins. However, if a single-base insertion is made after the
amino acid 226 of the spinach gene (changing the sequence
CCC ACG GGG GTG GTG ... .[Pro Thr Gly Val Val.1..].. to
CCN CAC GGG GGT GGT ... .[Pro His Gly Gly Gly... .], the
reading frame is shifted to specify 45 additional amino acids
that resemble the consensus sequence much more closely. The
corresponding change in the N. debneyi sequence produces a C
terminus identical to that of N. tabacum as determined by
Shinozaki et al. (561). The rp12 genes of tobacco, spinach, rice,
and maize are located in the inverted-repeat region, but those
of Marchantia polymorpha and C. reinhardtii are in single-copy
DNA. The spinach, C. reinhardtii, and Euglena genes are
uninterrupted, whereas those of many other land plants contain a single group II intron (133). The intron insertion sites
are identical in the Nicotiana, rice, and Marchantia genes, and
the introns themselves have a high degree of nucleotide
sequence identity. Downie et al. (133) determined the distribution of the rpl2 intron in 390 species from 116 angiosperm
MICROBIOL. REV.
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CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
protease digestion, suggesting that it remained on the ribosome surface
(203).
L14 in E. coli is a late-assembly protein and does not bind
directly to 23S rRNA (458). Antibody-binding studies suggest
that in B. stearothermophilus this protein is located on the
surface of the 50S subunit (599). Genes encoding proteins with
a high degree of homology to E. coli L14 have been found in
chloroplast genomes of all plants and algae examined, except
in the parasitic plant Epifagus virginiana, in which a pseudogene is present instead (714) (Table 3).
In E. coli, both L15 and L16 are late-assembly proteins that
are associated with the peptidyltransferase center but seem to
be nonessential for ribosome function. Fully active ribosomes
lacking both these proteins, as well as L30, can be reconstituted
in vitro by modifying the conditions of the reconstitution
procedure (175). Nuclear genes encoding chloroplast ribosomal protein L15 have been reported from Arabidopsis thaliana and pea (640), and no rpll5 sequences have been identified
in any chloroplast genome to date (Table 3). The spinach
chloroplast homolog of L15 is significantly larger than its
counterpart in E. coli, owing to extensions at the N-terminal
and probably also the C-terminal ends (291).
In contrast to L15, ribosomal protein L16 is encoded by a
chloroplast gene located in a conserved operon in all species
examined (Table 3; Fig. 5). In land plants, the rpll6 gene is split
into two exons (e.g., 498), whereas in Chlamydomonas reinhardtii (373) and Gracilaria tenuistipitata (294), it is uninterrupted. The Euglena gene contains three introns (86, 93).
Antibodies to a chloroplast-encoded Chlamydomonas protein
("L-17") cross-react with E. coli L16, with spinach "L24," and
with an Anabaena protein that comigrates with E. coli L16
(510).
Protein L17 of E. coli has been shown to bind 23S rRNA
(358). A mitochondrial homolog has been identified in Saccharomyces cerevisiae (708), but no corresponding chloroplast
protein has been found. However, proteins of similar charge
and size were seen on two-dimensional electrophoresis of
ribosomal proteins from C. reinhardtii and Anabaena sp. (510).
Antibodies to E. coli L17 were also observed to cross-react with
a chloroplast ribosomal protein from spinach (18).
Protein L18, which is highly conserved in bacteria, binds to
5S rRNA and is associated with the peptidyltransferase center
(91). Genes encoding a ribosomal protein equivalent to E. coli
L18 have been found in the cyanelle genome of Cyanophora
paradoxa (423) and in the Porphyra chloroplast genome (517).
Spinach ribosomal protein "CS-L13" is a homolog of E. coli
L22 (see below), with N- and C-terminal extensions that have
no sequence homology with the 5S-binding proteins of E. coli
but show some structural similarity to L18 (651).
A gene encoding a protein equivalent to E. coli L19 has been
found in the Porphyra chloroplast genome (514) and in the
cyanelle genome (598). Little is known about the function of
this protein in either bacterial or chloroplast ribosomes.
An equivalent of the early-assembly, RNA-binding protein
L20 of E. coli is encoded in chloroplast genomes of plants and
algae and in the cyanelle genome of Cyanophora paradoxa
(Table 3).
Protein L21 of E. coli can be cross-linked to the 5' domain
of the 23S rRNA molecule and, together with L4, may have a
second contact to the 23S molecule in the adjacent domain (57,
481). The gene encoding L21 is chloroplast encoded in Marchantia polymorpha and in the red algae Cyanidium caldarium
and P. purpurea (Table 3) but is absent from the chloroplast
genomes of rice, tobacco, and Euglena gracilis. A spinach
nuclear gene encoding L21 has been found to contain four
introns in its central region (340, 578). Two transcription start
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(149, 533). McElwain et al. (413) have isolated a thiostreptonresistant mutant of C. reinhardtii whose chloroplast ribosomes
are resistant to the drug in vitro. The large subunits of the
mutant ribosomes lack a cytoplasmically synthesized protein
("L-23") that, on the basis of size and immunological criteria,
appears to be the equivalent of the E. coli L1i protein. In
pulse-labeling experiments, this Chlamydomonas mutant synthesizes small amounts of protein "L-23," but the protein fails
to assemble into chloroplast ribosomes. The mutation shows
Mendelian inheritance, suggesting that rplll is a nuclear gene
in C. reinhardtii.
The acidic protein L7/L12 is one of the most intensively
studied ribosomal components (57, 474, 708). Four L12 molecules are present in each ribosome of E. coli, together with
one L10 polypeptide, forming the stalk of the 50S subunit and
interacting with elongation factor EF-G which binds near the
base of the stalk. The homologous protein was identified in
spinach chloroplasts by direct sequencing of tryptic peptides
(19) and was predicted to have a tertiary structure similar to
that of its counterpart in E. coli (271, 345). cDNA clones
encoding this protein have been isolated and sequenced from
the nuclear genomes of several land plants (Table 3), and the
gene has been cloned and characterized from Arabidopsis
thaliana and spinach (689). In Arabidopsis thaliana (689), L12
is encoded by a multigene family with one silent and two
functional genes, the functional genes both being closely linked
to cytosolic tRNA genes (this is the first such case identified for
a chloroplast ribosomal protein [607]). However, L12 is encoded by a chloroplast gene in Euglena gracilis and by a
cyanelle gene in Cyanophora paradoxa. The derived amino acid
sequence of the cloned spinach gene includes three amino
acids that were apparently overlooked in the primary sequence
of the corresponding protein published by Bartsch et al. (19).
Sibold and Subramanian (564) have compared the spinach and
bacterial sequences with the L12 protein of the cyanobacterium Synechocystis sp. Like the E. coli protein, spinach L12 is
present in multiple copies per ribosome, but it lacks the
N-terminal acetylation seen in the bacterial protein (19).
Giese and Subramanian (202) reported that the transit
peptide sequence of a spinach gene for L12 contains two ATG
codons, each in a consensus initiation context, that would yield
the same mature peptide after transport into chloroplast and
N-terminal cleavage. Genes for L13, L35, and the novel
protein Psrp-1 have similar duplicated ATGs. Experiments in
which the 5' part of the L12 gene was fused to a reporter gene
demonstrated that both codons can be used in vitro and in
spinach protoplasts, with about 25% of initiations occurring at
the second codon. Such an arrangement may enhance translational efficiency. However, Elhag et al. (155) found that both
L12 cDNAs from tobacco had only a single ATG, corresponding to the first ATG of the spinach gene.
The L13 protein of E. coli interacts with the 5' domain of the
23S rRNA molecule, in proximity to L4, L21, L28, and L29
(57). A nuclear cDNA clone encoding a chloroplast ribosomal
protein equivalent to E. coli L13 has been identified in spinach
(490, 609), and a chloroplast gene for this protein has been
found in Porphyra purpurea (517). The spinach protein has
54% deduced amino acid identity with that of E. coli over the
142 amino acid residues that can be aligned, but it is preceded
by 52 residues at the N terminus with no homology to any
known protein. Upstream of this sequence are 47 amino acids
which appear to be a transit peptide. The chloroplast protein
also has a C-terminal extension with no homology to E. coli
L13. However, spinach L13 translated in E. coli from cDNA
constructs was found to be incorporated into functional ribosomes (203). The N-terminal extension was removable by mild
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HARRIS ET AL.
L23 are found in ribosomes from eubacteria, organelles,
archaebacteria, and cytoplasmic ribosomes of eukaryotes (513,
708). The equivalent cytoplasmic ribosomal proteins (called
L25 proteins) have an extended amino terminus and a carboxy
terminus that resembles the archaebacterial L23 protein more
than the eubacterial one.
Sequences with relatively low homology to the gene encoding E. coli L23 have been found in the "S1O"-like operons in
chloroplast genomes of a number of plants (Table 3; Fig. 5).
While these rp123 sequences are in the same position as the E.
coli gene for L23 in this operon, not all the chloroplast
sequences form continuous open reading frames and some
may be pseudogenes (45, 732, 746). The rp123 genes of spinach
and four related dicots appear to have sustained a 14-bp
deletion approximately in the center of the coding sequence,
creating two overlapping open reading frames with homology
to the two halves of the tobacco gene (635, 746). Transcripts
for both reading frames could be detected in vivo by S1
mapping in spinach (635). However, no radioactive peptides
corresponding to these transcripts were seen on two-dimensional electrophoresis of the products of a coupled transcription-translation system. Furthermore, when chloroplast ribosomal proteins of a size close to those expected for the
chloroplast rpl23 gene products, either singly or spliced, were
subjected to N-terminal sequencing, none of the sequences
obtained corresponded to the predicted sequence of the split
rp123 gene. Bubunenko et al. (70) have recently reported that
chloroplast ribosomes of spinach contain no protein that
cross-reacts with the product of the functional chloroplast rpl23
gene of maize but do contain a protein with strong homology
to the L23 equivalent of eukaryotic cytoplasmic ribosomes.
This is the first suggestion that a nuclear gene encoding a
cytoplasmic ribosomal protein has been substituted for a
nonfunctional chloroplast gene.
In Epifagus virginiana the plastid rpl23 sequence is also a
pseudogene (714). However, Yokoi et al. (732) found that the
tobacco rpl23 gene, which does have a continuous open reading
frame, appears to be functional, since the N-terminal sequence
of a 13-kDa protein from the 50S ribosomal subunit exactly
matches that predicted from the chloroplast rp123 gene. The
rp123 genes from three monocots (rice, wheat, and maize) are
also uninterrupted, and their derived amino acid sequences are
virtually identical to one another. In rice an rp123 gene is
located in the inverted repeat, but an open reading frame with
homology to rpl23 is also present in the large single-copy
region between rbcL and petA (265). Analysis of the corresponding region in wheat (Triticum aestivum) and two closely
related plants,Aegilops squarrosa andA. crassa, has revealed an
apparent rp123 pseudogene in wheat andA. crassa but not inA.
squarrosa, whose chloroplast genome seems to have sustained
a deletion in this region as a result of illegitimate recombination between short direct repeats (45, 46, 469). Wheat has a
length polymorphism just downstream of this gene compared
with A. crassa, also apparently the result of an illegitimate
recombination event between relics of short repeats. Sequences with strong homology to the chloroplast rpl23 genes
and pseudogenes have also been detected in mitochondrial
DNA of rice and maize (45).
The rpl23 gene is missing from the corresponding operon of
the cyanelle genome (32, 598). In Euglena gracilis, the rp123
gene is in the expected position at the start of the "S10" operon
but is interrupted by three group III introns (243). An uninterrupted rp123 gene has been sequenced from the chloroplast
genome of C. reinhardtii, in the expected position at the start of
the "S10" operon (277). However Randolph-Anderson et al.
(510) found that antibody to C. reinhardtii "L-29," a cytoplas-
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sites were identified, one which appears to be constitutive and
the other which appears to be induced only in leaf tissue (340).
The spinach L21 protein (formerly "CS-L7" [378]) is considerably longer than its homologs from E. coli and Marchantia
polymorpha, having extensions at both the N and C termini.
The carboxyl-terminal extension contains seven Ala-Glu repeats, creating a region of high negative charge, and the
protein as a whole is acidic, in contrast to E. coli L21, which is
basic. However, this protein can be incorporated into E. coli
ribosomes assembled in vivo (71, 685). The spinach L21
protein shows greater homology to E. coli L21 than it does to
the chloroplast-encoded Marchantia protein, prompting Martin et al. (408) to hypothesize that spinach L21 arose either by
duplication of a nuclear gene for a corresponding protein of
the cytoplasmic ribosome or by transfer of a mitochondrial
gene, rather than by transfer of a chloroplast gene to the
nucleus. A mitochondrial origin seems unlikely, since no gene
encoding the equivalent of L21 has so far been identified in a
mitochondrial genome of any plant (371).
Protein L22 binds to 23S rRNA early in assembly of the 50S
particle in E. coli and is one of only five proteins both necessary
and sufficient to formation of the core precursor particle RI*
(459). Equivalent proteins have been identified in archaebacteria and cytoplasmic ribosomes (381, 708). The rp122 gene is
found in chloroplast genomes of all land plants so far examined, with the exception of two unrelated groups of angiosperms, the legumes and the parasitic plant Epifagus virginiana
(193, 485) (Table 3). A nuclear gene encoding L22 has been
cloned from pea (193). In this gene, the exon encoding the
putative N-terminal transit peptide is separated by an intron
from the conserved structural gene. Gantt et al. (193) speculated that the transit peptide sequence may have been acquired
by a form of exon shuffling. The rp122 gene is also missing from
the relic of the S10 operon in the C. reinhardtii chloroplast
genome (277) but is found in the expected location in the
plastid genomes of Euglena gracilis and the red algae Gracilaria
tenuistipitata and Porphyra purpurea (86, 295, 514) and in the
cyanelle genome (163, 423).
The spinach rp122 gene encodes a protein with a central
region homologous to all L22 proteins but has N-terminal and
C-terminal extensions with structural similarity to the E. coli
L18 and L25 proteins on the basis of hydropathy profiles (651,
741). The spinach L22 protein binds to SS rRNA, protecting
three nonoverlapping binding sites (76, 651). In E. coli, however, L22 does not bind SS rRNA but L18 and L25 do. These
observations suggest the interesting possibility that the spinach
L22 protein ("CS-L13") serves the composite functions of all
three of these proteins. Carol et al. (76) have shown that the
L22-like central domain of the spinach protein is required for
SS binding, so that this domain appears to have a function
lacking in the E. coli protein. However, both the spinach and E.
coli L22 proteins bind erythromycin. The monocots rice and
maize have L22 proteins with similar 29-residue N-terminal
extensions, which, however, have little homology to the spinach
extension. N-terminal extensions are lacking in the L22 proteins of tobacco, Marchantia, Euglena, and Gracilaria species;
the tobacco protein has a C terminus that is longer than that of
Marchantia polymorpha but considerably shorter than that of
spinach.
The position of L23 in the E. coli ribosome has been
controversial, with cross-linking and immunoelectron microscopy studies giving conflicting results (91, 447). Kruft et al.
(328) propose that it has an elongated structure, with the
N-terminal domain close to L29 at the base of the 50S subunit
and the C-terminal domain on the ribosomal surface close to
the peptidyltransferase center. Proteins equivalent to E. coli
MICROBIOL. REV.
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
tive (103). A nuclear gene encoding a protein with sequence
similarity to E. coli protein L28 has been isolated from tobacco
(731). The "L-31" protein of C. reinhardtii chloroplast ribosomes was observed to comigrate with E. coli L28, but immunological cross-reactivity was not tested (510).
E. coli protein L29 also can be cross-linked to the 5' domain
of the 23S molecule (57) but associates with the ribosomal
particle early in the assembly process (459). L29 appears in the
same ribosomal neighborhood as proteins L2, L4, L15, and
L34 (676). A gene encoding an equivalent chloroplast protein
has so far been found only in Porphyra purpurea (514).
Protein L30 of E. coli assembles late and can be eliminated
by mutation (103, 459). An equivalent protein has been
identified in archaebacteria (708) but so far not in chloroplasts.
L31 is a late-assembly protein in E. coli (358, 459) and is known
so far only from the Porphyra chloroplast genome.
E. coli L32 also associates with the ribosome late in the
assembly process (459). Genes encoding L32 have been found
in the chloroplast genomes of several plants and algae (Table
3). However, this gene is missing from the Epifagus chloroplast
genome (714). Deduced amino acid similarity to the E. coli
gene is low (Table 3), but hydropathy plots suggest that the
plant and bacterial proteins are similar in conformation (733).
The N-terminal portions of the chloroplast L32 proteins are
highly conserved in amino acid sequence, whereas the Cterminal ends are variable in sequence and in length.
The E. coli L33 protein can be cross-linked to 23S rRNA at
positions 2422 to 2424 (481) and to proteins Li and L27 (676).
Mutants of E. coli lacking L33 are viable but cold sensitive
(103). The rp133 gene is chloroplast encoded in land plants and
Porphyra purpurea and has also been sequenced from the
cyanelle genome (Table 3) but is missing from the Euglena
chloroplast genome (243).
Protein L34 has been characterized in a number of eubacterial species but has not yet been identified in chloroplasts
except for those in Cyanophora and Porphyra purpurea. In the
E. coli ribosome, it is found in a neighborhood with proteins
L2, IA, L15, and L29 (676).
Protein L35, formerly designated ribosomal protein A in E.
coli (675), is encoded in the nuclear genome of spinach (577)
but in the chloroplast genome of P. purpurea (514) and in the
cyanelle genome of Cyanophora paradocxa (69).
L36, the product of the E. coli gene formerly designated secX
(675), is chloroplast encoded in all plants and algae so far
examined (Table 3). The high degree of conservation of the
amino acid sequence of the chloroplast L36 proteins compared
with E. coli (Table 3) suggests that this small protein may have
an important but as yet unknown role in the ribosome.
Chloroplast Ribosomal Proteins with No Obvious
Homology to Those of E. coli
Zhou and Mache (741) reported that spinach chloroplasts
contain relatively large amounts of a unique ribosomal protein,
"CS-S5." The deduced amino acid sequence of a full-length
cDNA clone for the nuclear gene encoding this ribosomal
protein shows no sequence similarity to any bacterial ribosomal protein (28, 741). Working independently, Johnson et al.
(290) characterized a 26-kDa protein from spinach chloroplast
ribosomes ("PSrp-1"), which appears to be identical to "CSSS." The DNA sequences determined by the two groups differ
in three nucleotides, one of which creates a frame shift that
changes the predicted C-terminal sequence. Direct sequencing
of protease-generated internal peptides supports the 236amino-acid sequence published by Johnson et al. (290). The
precursor form of this protein contains 302 amino acids.
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mically synthesized protein, cross-reacts with E. coli L23 and
with spinach ribosomal protein "L28." This antibody showed
no cross-reaction with Anabaena "L24," a protein which
comigrates with E. coli L23 on two-dimensional gels.
L24 is an early-assembly rRNA-binding protein in bacteria,
which, together with L3, is essential for initiation of assembly
of the 50S subunit but seems not to be essential either for late
stages of ribosome assembly or for translation in vivo. An E.
coli mutant lacking L24 can grow, albeit very slowly (257, 461).
A reading frame specifying L24 has been found in the chloroplast genome of P. purpurea, in the position expected based on
similarity to the E. coli spc operon (514), but this protein
appears to be nucleus encoded in land plants, and cDNAs
encoding it have been sequenced from pea (192), spinach (75,
339), and tobacco (153). The plant sequences have transit
peptides of about 70 amino acids, as well as highly conserved
C-terminal extensions.
L25 is a 5S-binding protein in E. coli (57). No exact homolog
has been identified in chloroplast ribosomes. However, in
spinach two chloroplast ribosomal proteins, L22 and "CS-12,"
have been shown to bind SS rRNA and may thus together serve
the same function as E. coli L5, L18, and L25 (76, 651) (see
above). The 5S-binding domain of spinach "CS-12" shows
structural similarity to that of L25.
The protein formerly designated as L26 of E. coli is now
identified as S20 (706).
L27 is a conserved protein that maps by immunoelectron
microscopy to the base of the central protuberance of the 50S
subunit of the E. coli ribosome and appears to be associated
with the peptidyltransferase center (57, 744). Plastid genes
encoding this protein have been sequenced from chromophyte
and rhodophyte algae (185, 517), but the gene appears to be
nucleus encoded in green algae and in land plants. Two cDNAs
encoding a protein homologous to E. coli L27 have been
sequenced from tobacco (154) and found to have differing
3'-flanking sequences, suggesting that the tobacco nuclear
genome encodes more than one L27 gene. The identity of
these cDNAs was confirmed by comparing the predicted amino
acid sequences with that determined for the purified L27
protein (154). N-terminal amino acid sequencing of the cytoplasmically synthesized ribosomal protein designated "L-18" in
C. reinhardtii (547) indicates that this protein is the E. coli L27
homolog (363), but the gene has not yet been cloned. Schmidt
et al. (545, 546) found that C. reinhardtii "L-18" is synthesized
as an 18.5-kDa precursor that undergoes a two-step processing
reaction. Conversion of the 17-kDa intermediate identified in
pulse-labeling experiments to the mature 15.5-kDa form requires chloroplast protein synthesis. Liu et al. (363) showed
that the 17-kDa intermediate specifically associates with a
ribosomal complex that migrates with the ribosomal large
subunit before being processed to the mature protein. This
suggests that the second processing step may be required for
maturation of the 50S ribosomal subunit. Antibody to C.
reinhardtii "L-18" cross-reacts with E. coli L27, with spinach
"L22" (terminology of Mache et al. [378]), and with an
Anabaena protein ("L23" [510]). Elhag and Bourque (154)
show the alignments of the tobacco L27 sequence with the
partial L27 sequences of C. reinhardtii (547) and spinach (607),
and with that of the yeast mitochondrial ribosomal protein
MRP7 (167). Elhag and Bourque (154) note that this is the first
example of a chloroplast ribosomal protein for which the
sequence of a presumably homologous mitochondrial ribosomal protein is known.
L28, which cross-links to the 5' domain of the 23S rRNA, is
added to the E. coli ribosome relatively late in assembly (57,
459), and mutants lacking L28 are viable although cold sensi-
729
730
HARRIS ET AL.
Lagrange et al. (339) proposed to designate this ribosomal
protein S22, since S21 is the highest-numbered protein of the
E. coli small subunit. Schmidt et al. (541) have proposed
alternatively that the numbers 22 to 29 be skipped and that this
protein be named S30 instead.
Schmidt et al. (541) and Wada et al. (674) have independently identified another novel protein in preparations of
spinach chloroplast ribosomes. Schmidt et al. described a basic
protein of about 7.5 kDa and gave it the designation S31. A
Comparative Analysis of Ribosomal Proteins
Sequence comparisons across phylogenetic lines can reveal
essential structural features of both RNAs and proteins. This
technique has been beautifully exploited in establishing conserved loops and helices in 16S and 23S rRNAs (see, e.g.,
reference 236) but has been less well developed to date in
analysis of ribosomal proteins. Golden et al. (213) have
recently reported the three-dimensional structure of ribosomal
protein S17 from B. stearothermophilus, based on nuclear
magnetic resonance spectroscopy, and Hoffman et al. (266)
have solved the crystal structure for protein L9 from this
bacterium. The comparative analysis presented in both these
papers includes the sequences for the homologous proteins
from pea and Arabidopsis thaliana, as well as the Cyanophora
S17 and Synechocystis L9 sequences. Conserved structural
residues and proposed rRNA-binding sites can be identified in
both proteins. Conservation of the length of an al-helix in the
L9 protein, for example, suggests that this helix has a structural
role, whereas variability in the central region of the protein
sequence is consistent with its occupying an exposed position in
the ribosome. Similar analyses should be possible with other
ribosomal proteins.
ASSEMBLY OF CHLOROPLAST RIBOSOMES
Subramanian (606) points out that the ribosomal proteins
encoded in land plant chloroplast genomes share the following
properties: (i) all are important proteins in early steps in
ribosome assembly as judged from comparison with assembly
maps of the E. coli 30S and 50S subunits (see, e.g., reference
707); (ii) their loss is likely to be lethal, since no E. coli mutants
lacking any of these proteins, with the exception of L33, have
been isolated; and (iii) all are basic or highly basic ribosomal
proteins, even though chloroplast ribosomes contain a much
larger number of acidic ribosomal proteins than E. coli ribosomes do.
The limited data available on chloroplast ribosome assembly
have been summarized for land plants by Mache (377). The
main observations on land plants and C. reinhardtii are as
follows. (i) Seven chloroplast ribosomal proteins, four of which
are made in the chloroplast, bind to chloroplast or E. coli 16S
rRNA, in agreement with the seven E. coli ribosomal proteins
known to bind to 16S rRNA (531). (ii) Two 5S rRNA-binding
proteins have been detected in spinach (L22 and "CS-12"
[651]), in contrast to three in E. coli (L5, L18, L25). However,
one of these chloroplast proteins, encoded by the rp122 gene,
has a central region of homology to other L22 proteins flanked
by long N- and C-terminal extensions (76). (iii) In C. reinhardtii, the second step of processing of "L-18," a homolog of
E. coli L27, occurs during ribosome assembly and may be
required for maturation of the 50S ribosome subunit (363). (iv)
The nucleus-encoded ribosomal protein "L-29" of C. reinhardtii is required for assembly of chloroplast-encoded ribosomal protein "L-13" (see below and reference 446).
Mutants with defects in chloroplast ribosome assembly have
been identified in C reinhardtii and map to seven nuclear and
two chloroplast loci (see reference 247 for a summary). Two
phenotypic classes are seen, one in which small subunits are
deficient but large subunits accumulate and one in which both
subunits are deficient. No mutant specifically deficient in large
subunits has been identified. Analysis of double-mutant combinations of five nonallelic nuclear mutations led to the
proposal that mutants deficient in both subunits were blocked
in steps common to the assembly of the two subunits, while the
mutants that accumulated large subunits were blocked only in
the assembly of small subunits (248). One of the mutants
deficient in both subunits, ac-20, has subsequently been shown
to be defective in its ability to splice an intron present in the
precursor of 23S rRNA (259). Since expression of the mutant
defect apparently occurs after processing of the primary rRNA
transcript, these observations suggest that inability to process
pre-23S rRNA properly results in a deficiency of large subunits, which in turn prevents small subunit assembly.
Two Chlamydomonas allelic nuclear mutations, cr-6 and
cr-7, cause production of ribosomal large subunits that sediment abnormally on sucrose gradients, assemble into monomers less efficiently than those from wild-type cells, and show
reduced capacity for protein synthesis in vivo (446). Large
subunits of chloroplast ribosomes from these two mutants lack
two proteins, one of which ("L-29") is made in the cytoplasm
and the other ("L-13") is made in the chloroplast. The primary
defect appears to be an inability to make "L-29," which
prevents assembly of "L-13" into the 50S subunit. Immunologically, "L-29" is related to E. coli L23 and to a lesser extent to
L7/L12, while "L-13" is related to E. coli L5 (see above and
reference 510). Assembly of L5 into the E. coli 50S subunit
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sequence of 43 of the estimated 60 amino acids constituting
this protein showed no homology to any known E. coli
ribosomal protein or to any other sequence available in public
databases, nor did it correspond to the derived amino acid
sequence of any coding region in a published chloroplast DNA
sequence. However, the sequenced region was shown to have
42% identity to the unpublished sequence of a small basic
protein isolated from the bacterium Thermus thermophilus.
Wada et al. (674) described a 5-kDa protein, SCS23, with no
apparent homology or immunological cross-reactivity to any E.
coli ribosomal protein. The N-terminal sequence of this protein is similar to that published by Schmidt et al. (541).
Two cDNAs isolated from pea encode ribosomal proteins of
moderate size with no recognizable similarity to any ribosomal
protein of E. coli (192). The PsCL18 gene encodes a protein of
145 amino acids, including a transit sequence of approximately
50 amino acids, and the PsCL25 gene specifies a protein of 104
amino acids, of which about 30 amino acids constitute a transit
sequence. Typical of ribosomal proteins, the deduced amino
acid sequences of both PsCL18 and PsCL25 have a high
content of lysine and arginine residues, and a consequent high
net positive charge, but differ in the distribution of these
charged amino acids. PsCL18 has a highly charged, highly basic
carboxyl end, whereas the carboxyl terminal of PsCL25 contains mostly uncharged amino acids with four aspartic acid
residues constituting the only charged species. No E. coli
ribosomal protein has a carboxyl terminus resembling either of
these nucleus-encoded chloroplast ribosomal proteins from
pea. A protein similar to PsCL18 has been isolated from
spinach and designated L40 (75, 339). This protein appears to
be encoded by a single-copy nuclear gene and to contain 142
amino acids with 54% sequence identity to pea CsL18. This is
a slightly lower sequence identity than is seen between other
nucleus-encoded ribosomal proteins of higher plants, e.g., S17,
L12, and L15 (Table 3).
MICROBIOL. REV.
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
VOL. 58, 1994
origin.
SYNTHESIS OF THE COMPONENTS OF
CHLOROPLAST RIBOSOMES
Biogenesis of chloroplast ribosomes requires expression of
both nuclear and chloroplast genes encoding different ribosomal proteins, as well as chloroplast genes encoding the
component rRNAs. The mechanisms by which the appropriate
stoichiometry of these components is achieved from genes
present in vastly different copy numbers remain poorly understood (229, 377, 379). In general, nuclear gene expression in
plants tends to be controlled at the level of transcription and to
be subject to light regulation, whereas chloroplast gene expression is largely regulated posttranscriptionally. Pool sizes of
some components may also be controlled by proteolysis.
Furthermore, chloroplast genes encoding ribosomal components appear to be regulated differently from those encoding
proteins of the photosynthetic apparatus (207, 253, 365). In
this section we will discuss transcription and splicing of rRNAs,
transcription and translation of genes encoding ribosomal
proteins, and posttranscriptional and translational regulation
of chloroplast gene expression.
Transcription of rRNA Genes
As in bacteria, chloroplast rRNA genes are thought to be
transcribed as large precursor molecules that subsequently
undergo several processing steps to generate the mature
rRNAs (114). Relatively little is known, however, about the
specific enzymes and cleavage steps that are involved. Although 5S rRNA sequences are not detected in the primary
transcript, S1 and primer extension experiments suggest that
the 5S gene is indeed cotranscribed with the 16S and 23S genes
and that the 5S rRNA is rapidly cleaved from the initial
precursor (10, 601). Possible promoter sequences have been
found between the 4.5S and 5S rRNA genes in some plants,
suggesting that separate 5S transcription might occur, but
these sequences are not present in many plants and do not
seem to be active in vitro (10, 146). Likewise, the tRNA'g
following the 5S gene in land plants is thought to be cotranscribed with the rRNAs (118). However, the tRNAVal upstream
of the 16S gene in many plants lies distal to the identified
transcription start sites for the rRNA operon and thus is not
part of the primary transcript.
Possible processing sites of the primary rRNA transcript
have been identified by Si and reverse transcriptase mapping
(118, 601; see also reference 114). Experiments so far suggest
that cleavage at the various sites does not occur in a precise
order. The 5'- and3'-terminal precursor sequences of the 16S
and 23S RNAs can form double-stranded stem structures
similar to those of the E. coli rRNA genes, leading to the
suggestion that these molecules may be processed by an RNase
III-like endonucleolytic cleavage (114). Vera et al. (669) have
found that tobacco chloroplast ribosomes contain a minor
fraction of 16S rRNA molecules in which a 30-nt leader
sequence containing the putative RNase III site is still present,
suggesting that the final maturation of the 16S rRNA may
actually take place within the ribosome.
Processing of the tRNAs of the spacer between the 16S and
23S genes requires the ribozyme RNase P (679), but other
processing reactions specific to plant chloroplast rRNAs have
not been well characterized to date. Additional processing of
the mature 23S rRNA of land plants may occur, leading to
hidden breaks at specific stem-loop sites. Thus 23S rRNA
isolated under denaturing conditions typically appears as several short species rather than a single intact molecule. Delp
and Kossel (114) suggest that this fragmentation is real, not an
artifact of preparation, and that it may be necessary for some
structural or functional requirement of the chloroplast ribosome.
There are conflicting data regarding whether chloroplast
rRNA genes are transcribed by a different RNA polymerase
from that used to produce mRNAs (229, 283, 320, 349, 642).
Chloroplast genomes typically contain genes homologous to
the rpoA, rpoB, and rpoC genes, which encode RNA polymerase subunits of bacteria, but appear to lack a gene for rpoD,
which encodes the principal cr factor of the bacterial RNA
polymerase (24, 171, 614, 653). However, immunological studies suggest that the chloroplast RNA polymerase complexes do
contain a-like factors (642, 653). Expression of the chloroplastencoded RNA polymerase genes in Euglena chloroplasts resulted in activity of a soluble RNA polymerase fraction capable
of transcribing tRNA and mRNA genes, whereas transcription
of rRNA genes required a membrane-bound fraction (226,
244, 361). However, soluble RNA polymerase from spinach
chloroplasts appears to be able to transcribe both rRNA and
protein-coding genes in vitro (55). Fractionation of RNA
polymerase activities from spinach suggests that a 110-kDa
component may represent a core enzyme active as a single
polypeptide chain, which shows no immunological similarity to
E. coli RNA polymerase subunits and is thus probably not the
product of the chloroplast rpoB gene (349). Further evidence
for a second, presumably nucleus-encoded RNA polymerase
activity in chloroplasts comes from the observation that the
plastid genome of the parasitic plant Epifagus virginiana lacks
the rpo genes but is nevertheless transcribed (115, 435, 713,
714). Also, some plastid genes in heat-bleached leaves of rye
and barley plants and the albostiians mutant of barley are
transcribed, although these leaves lack functional chloroplast
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does not depend directly on the presence of either L7/L12 or
L23 (707).
Chloroplast and nuclear mutations causing complete or
nearly complete loss of chloroplast ribosomes from white
tissues and seedlings have also been identified in land plants
(39) and have been very useful in probing the function of the
chloroplast protein-synthesizing system. Barkan (17) has recently described transposon-induced nuclear mutations in
maize that impair chloroplast protein synthesis. Seedlings of
these mutants are paler green than those of the wild type and
are photosynthetically inactive, although they do accumulate
nucleus-encoded proteins of the light-harvesting complex. One
mutant appears to be blocked specifically in processing of 16S
rRNA.
Complete assembly of ribosomal subunits has been detected
in isolated spinach chloroplasts, implying either that a pool of
unassembled nucleus-encoded ribosomal proteins exists in
plastids or that ribosomal proteins can be released from
preexisting ribosomes and reutilized (121). Certain proteins,
e.g., the CS-S5 protein of spinach, can be found in high
concentrations in the chloroplast stroma (741). When rye
plants are grown at high temperature (32°C), plastid ribosome
formation is severely impaired (168, 169). Pools of a few
unassembled plastid ribosomal proteins were detected when
soluble extracts from leaves deficient in 70S ribosomes were
examined with antibodies raised against purified 50S and 30S
subunits. These antibodies were shown to react with about 17
of the 33 polypeptides of the 50S subunit and 10 of the 25
proteins of the 30S subunit. Feierabend and Berberich (168)
believe that these observations confirm the absence of plastid
ribosomes following bleaching and that the unassembled proteins detected by the antibodies are probably of cytoplasmic
731
732
HARRIS ET AL.
ribosomes and are thus unable to translate the mRNAs for the
rRNA gene and has a conserved and essential -35 sequence.
A 14-bp sequence that is recognized by polypeptides of 33 and
35 kDa has also been identified upstream of the 16S rRNA
initiation start site in spinach (13). This sequence is not found
upstream of chloroplast genes encoding mRNAs or tRNAs
and thus may have a role in differential regulation of rRNA
and protein-coding genes during chloroplast development.
Expression of rRNA genes appears to depend on both light
and developmental stage in plant seedlings (309, 442), but
steady-state levels of rRNA seem to be controlled more by the
rate of breakdown than by transcriptional regulation (114).
Bendich (21) has suggested that rRNA transcription is regulated primarily by gene dosage. However, in cells of C.
reinhardtii grown in the presence of 5-fluorodeoxyuridine, the
reduction in chloroplast DNA copies was mirrored by a
reduction in accumulation of chloroplast rRNA (208, 272).
There is indirect evidence that conserved stem-loop structures
and short open reading frames found between the promoter
and the start of the 16S coding sequence could be involved in
regulation of rRNA operon expression in spinach chloroplasts
(338).
Bisanz-Seyer et al. (27) observed the accumulation of 16S
rRNA and mRNAs for several chloroplast ribosomal proteins
during early development of spinach. The 16S rRNA, already
present in dry seeds, began to increase at the time of seed
germination 5 days after planting and continued to accumulate
thereafter. Most ribosomal protein mRNAs appeared at the
beginning of germination (5 days), but the rpsl9 and rp123
mRNAs appeared 2 days earlier. These two genes belong to a
large chloroplast ribosomal protein operon including parts of
the S10, spc, and a operons of E. coli. Interestingly, mRNAs
for several other ribosomal protein genes in this operon,
including rps3 and rp116, did not begin to accumulate until
germination. One explanation of these results is that the first
three genes in this operon, rp123-rp12-rpsl9, are transcribed
early and the whole operon is transcribed later. This hypothesis
predicts that rp12 transcripts should also be detected early, but
this was not examined with appropriate probes. Alternatively,
the entire operon may be transcribed early, but transcripts
distal to rpsl9 are initially degraded.
Gantt et al. (194) have presented additional evidence that
nuclear genes encoding chloroplast ribosomal proteins are
subject to light regulation. Pea seedlings grown in bright light
in the presence of the inhibitor norflurazon, which blocks
carotenoid synthesis, showed greatly decreased levels of
mRNA for nucleus-encoded ribosomal proteins compared
with seedlings grown with or without norflurazon in the dark.
Levels of mRNAs for other chloroplast components were
similarly diminished, but mRNAs for cytoplasmic ribosomal
proteins, histones, and other nonphotosynthetic proteins were
not affected.
Transcription of Chloroplast Genes Encoding
Ribosomal Proteins
Nuclear and plastid genes which cooperate in controlling
chloroplast biogenesis and function appear to be regulated by
very different mechanisms, although their gene products often
occur in equal stoichiometry within the multimeric thylakoid
complexes or chloroplast ribosomes. This may reflect the way
in which plant cells cope with large differences in ploidy levels
between nuclear genes (present in single copies or small gene
families) and chloroplast genes (present in hundreds or thousands of copies per cell). Nuclear genes encoding chloroplast
polypeptides are regulated largely at the transcriptional level in
response to environmental and developmental signals (for
reviews, see references 209, 329, and 443). In contrast, most
plastid genes appear to be transcribed at all times during
plastid development, and posttranscriptional regulatory mechanisms are thought to play major roles in modulating their
expression (see below).
All 21 of the ribosomal protein genes in the rice, tobacco,
maize, and Marchantia chloroplast genomes have been demonstrated to be transcribed (540), but not all have been shown
unequivocally to be translated into the corresponding polypeptides. N-terminal sequencing indicates that ribosomal proteins
S12, S16, S19, L2, L20, L32, L33, and L36 of spinach chloroplasts do indeed appear to be products of the corresponding
chloroplast genes (540). Most of the clusters of chloroplastencoded ribosomal protein genes that show striking homology
to bacterial ribosomal protein operons (631) (Fig. 5) are
probably functional transcriptional units (540). Multiple transcripts are typically found for individual ribosomal protein
genes in these clusters, and these may arise from processing of
larger polycistronic transcripts (470, 605). In C. reinhardtii, no
single large mRNA has been detected for the ribosomal
protein gene cluster that begins with the rp123 gene, but,
rather, a series of transcripts of different lengths have been
observed, including some probably monocistronic transcripts
and others corresponding to two or more genes (362; see also
reference 253).
Christopher and Hallick (87, 88) published a detailed characterization of the organization and transcription of the large
ribosomal protein operon in Euglena gracilis. The primary
transcript of this operon includes 11 genes encoding ribosomal
proteins, a tRNA gene, and an open reading frame encoding a
highly basic protein of unknown function (88, 243). An 8.3-kb
mRNA from which all introns have been removed by splicing
is then processed stepwise into transcripts containing one or
more genes.
Tonkyn and Gruissem (648) examined the relative expression levels of the intact S10 operon from spinach and the
partial S10 operon that begins in the opposite inverted repeat
but ends in an rpsl9' pseudogene as discussed above. Because
the upstream regulatory regions of these two operons are
included in the inverted repeat in spinach and are therefore
identical, Tonkyn and Gruissem predicted that these operons
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plastid-encoded rpo genes (164, 262, 263).
In land plant chloroplasts, promoter sequences preceding
the transcription start sites of rRNA operons do not differ
significantly from the -10 and -35 consensus sequences of
plastid protein-coding genes and are typically 50 to 200 bp
upstream of the 16S rRNA genes (229). The resemblance to
promoter sequences of protein-coding genes implies that a
single-core RNA polymerase might be able to transcribe all
classes of RNAs, a notion that is also supported by the
demonstration that a chimeric gene consisting of the 16S
promoter fused to the bacterial aadA gene encoding spectinomycin and streptomycin resistance is expressed in chloroplast
transformants of tobacco (621). This construct was edited by
site-directed mutagenesis to eliminate upstream AUGs in the
mRNA, and a synthetic leader sequence containing a ribosome-binding site was attached. The aadA gene was followed
by the 3' region of the chloroplast psbA gene. However,
deletion analysis with chloroplast transformants in which putative promoter regions were fused to a reporter gene has led
to the identification of two classes of chloroplast promoters in
C. reinhardtii (310). Promoters of the first class, such as atpB,
lack a conserved -35 sequence, and deletion of this region has
no effect on relative rates of transcription or the transcription
initiation site. The second class of promoters includes the 16S
MICROBIOL. REV.
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
Posttranscriptional Regulatory Mechanisms
Affecting Chloroplast mRNAs
Recent reviews by Rochaix (520), Gruissem and Schuster
(228), and Gruissem and Tonkyn (229) provide excellent
summaries of the current literature dealing with the processing, stability, and translational control of chloroplast mRNAs
in general, although relatively little of this literature is specific
to genes encoding ribosomal proteins. Two generalizations
emerge from these reviews. First, nuclear gene products control expression of chloroplast-encoded mRNAs. On the basis
of analysis of nuclear nonphotosynthetic mutants of C. reinhardtii, several different gene products may be required for
expression of a given chloroplast mRNA (520). Second, specific proteins bind to inverted repeat regions present in the 5'
and 3' untranslated leaders of chloroplast mRNAs that are
capable of forming thermodynamically stable stem-loop structures (105, 229). Although the 3' untranslated leaders appear
to function in stabilization and processing of mRNAs rather
than as transcript terminators in land plants, there is some
evidence that they serve as terminators for chloroplast transcripts in C. reinhardtii (30). Experiments are currently under
way in several laboratories to demonstrate the functional role
of individual binding proteins in mRNA stability and translation as well as to decipher the signal transduction pathway
leading to the expression of these proteins. For example,
Nickelsen and Link (456) have described a 54-kDa protein
from mustard chloroplasts that binds to a conserved sequence
in the 3'-flanking regions of the tmK and rpsl6 genes and
appears to have endonucleolytic activity that may be involved
in RNA 3'-end formation and mRNA stability.
Development of reliable protocols for chloroplast transformation in C. reinhardtii (48) and tobacco (390), coupled with
the ability to express foreign reporter sequences in the chloroplast, has allowed the functional dissection of the 5' and 3'
untranslated leaders for the first time (84, 214, 535, 591, 621).
Detailed consideration of the genetic basis for translational
regulation in chloroplasts and mitochondria and a model
depicting the role of a multiprotein translation complex bound
to the 5' untranslated leaders of organelle mRNAs in modulating the translational regulation are presented in a recent
review (207).
Membrane Binding of Chloroplast Ribosomes
Thylakoid-bound polysomes have been characterized in
chloroplasts with respect to their physical status and physiological function (see references 40, 41, and 286 for reviews).
High-salt washes of isolated thykakoids remove 30 to 45% of
the membrane-bound RNA while addition of puromycin releases up to 80% of the bound RNA. By analogy with the
rough endoplasmic reticulum, these results suggest that between one-third and one-half of the polysomes found on
thylakoids are attached electrostatically to the membranes and
the rest are held by both electrostatic forces and nascent
polypeptide chains. The electrostatic binding of chloroplast
polysomes predicts the presence of a ribosome receptor similar
to the ribophorin-containing receptor found on the rough
endoplasmic reticulum (503) but missing from the bacterial
cytoplasmic membrane. Other components of the system for
synthesizing eukaryotic secretory proteins, such as a signal
recognition particle and a docking protein, have not been
demonstrated in chloroplasts. The fraction of membranebound polysomes observed can be markedly enhanced by
pretreating the cells with antibiotics such as chloramphenicol
and erythromycin that inhibit transpeptidation.
Freimann and Hachtel (180) examined the distribution of
mRNAs on free and membrane-bound chloroplast polysomes
of broad bean (Vicia faba). They used the criteria of release of
the associated mRNA by high salt alone or high salt plus
puromycin, together with gene-specific probes, to distinguish
mRNAs electrostatically bound to thylakoids from those engaged in cotranslational protein synthesis. Three classes of
mRNA were recognized. (i) The rbcL mRNA encoding the
large subunit of Rubisco was the only mRNA associated solely
with stromal polysomes. However, other authors have reported
that rbcL mRNA is also found associated with thylakoid
membranes (252). (ii) Thylakoid polysomes containing
mRNAs for six genes encoding integral membrane proteins
appeared to synthesize their products in a cotranslational
fashion. These mRNAs were released only by high salt plus
puromycin. (iii) Thylakoid polypeptides encoded by seven
other genes were assumed to be incorporated posttranslationally because their mRNAs were found on stromal polysomes or
polysomes bound electrostatically to the thylakoid membranes.
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might be expressed at the same level and that a nonfunctional
product of the rpsl9' gene might accumulate. In fact, they
found that the rpsl9' transcript was present at very low levels
if at all and that the rp12 mRNA that is translated appears to be
transcribed from the gene copy located in the complete
operon. However, transcription of the intact operon can be
initiated from several different promoters, suggesting that it
may be subject to developmental regulation.
A number of genes encoding ribosomal proteins are part of
mixed clusters that also contain genes encoding components of
the photosynthetic apparatus. Stahl et al. (587) demonstrated
that such a mixed chloroplast gene cluster in maize containing
genes encoding four subunits of the ATP synthase (atpI, atpH,
atpF, and atpA) and the gene encoding ribosomal protein S2
(rps2) produces a total of 12 transcripts, including a major
species of 6,200 nt containing mRNAs of all five genes. They
suggest that this plastid gene cluster is "functionally organized
as an operon with additional regulatory features to allow for
increased accumulation of mRNAs for the thylakoid components."
The analogous operon in Euglena gracilis, containing rps2,
atpI, atpH, atpF, atpA, and rpsl8, was analyzed by Drager and
Hallick (134). Of these genes, all but atpH contain one or more
introns, comprising in aggregate nine introns of the group III
class unique to the genus Euglena and its colorless relative
Astasia (87, 565), seven introns with group II structure, and
one intron that matched neither category. Drager and Hallick
(134) found that all 17 introns are removed to yield a 5.5-kb
mRNA spanning all six genes, from which monocistronic
transcripts are then generated, presumably by endonucleolytic
cleavage. The unique 434-nt intron in the rpsl8 gene is a
complex twintron, consisting of four group III introns which
are removed in four sequential splicing reactions, some of
which can use multiple splice sites (135).
Chen et al. (83) found that the psaA, psaB, and rpsl4 genes
in rice are organized into a single transcriptional unit. A 5.2-kb
transcript hybridizing to probes for all three genes was observed in leaf tissue. Ribosomal protein L32 of the tobacco
chloroplast has been shown to be encoded by the gene
formerly identified as open reading frame ORF55 (733),
located in the small single-copy region. A primary transcript of
1,550 nt contains no other open reading frames and overlaps
the ndhF gene on the opposite strand (668). Vera et al. (668)
demonstrated that the rp132 promoter is located within the
ndhF coding region, the first instance so far of an internal
divergent promoter in the chloroplast genome.
733
734
HARRIS ET AL.
HOW ESSENTUIL IS CHLOROPLAST
PROTEIN SYNTHESIS?
Chloroplast protein synthesis has long been known to be
indispensable for survival of plants and algae that depend on
CO2 as their sole carbon source, since numerous proteins
required for photosynthesis are plastid gene products. However, as we learn more about the genes encoded in the plastid
genomes of algae such as Cyanophora, Cryptomonas, and
Porphyra species, some of which specify proteins required for
amino acid or fatty acid biosynthesis, the likelihood is increasing that chloroplast protein synthesis is also required for the
production of one or more essential proteins not involved in
photosynthesis. This viewpoint is supported by some, but not
all, analyses of plastid genome function in colorless plants. We
begin with cases that support the hypothesis that chloroplast
protein synthesis is essential and then turn to evidence that
makes the converse argument.
The colorless heterotroph Astasia longa is closely related to
Euglena gracilis and possesses a circular 73-kb plastid genome.
This genome is the counterpart of the larger (145-kb) Euglena
chloroplast genome, and the genes identified include the
rRNAs, tufA, and several tRNAs and ribosomal proteins
(565-569). The rbcL gene encoding the large subunit of the
enzyme Rubisco is the only photosynthetic gene so far detected
in the Astasia plastid genome. This polypeptide has been
immunoprecipitated from Astasia longa, suggesting that the
rbcL gene is transcribed and translated and that the plastid
protein-synthesizing system of this colorless flagellate must be
functional. Colorless, heterotrophic algae of the genus Polytoma, closely related to or derived from the genus Chlamydomonas, contain a plastid genome (ca. 200 kb) similar in size to
the C. reinhardtii chloroplast genome (574, 670). Plastid rRNA
genes are present and expressed in Polytoma species, leukoplast ribosomes have been isolated, and the tufA gene has been
identified. These results suggest that Polytoma species too have
a functioning plastid protein-synthesizing system (575, 576,
670).
Plastid genomes of the colorless plants Epifagus virginiana
(beechdrops) and Conopholis americana in the Orobranchaceae family of root-parasitic angiosperms have also been
examined (115, 702-704, 711, 712, 714). The 70-kb Epifagus
plastid genome has been completely sequenced and contains
only 42 genes (714). At least 38 of these genes encode
components of the plastid gene expression system (rRNAs,
tRNAs, and ribosomal proteins). Functional photosynthesis
genes and genes of the NADH dehydrogenase complex are
absent, although several photosynthetic pseudogenes have
been found. The Epifagus plastid genome contains only 17
tRNAs, suggesting that tRNAs must be imported if this plastid
protein-synthesizing system is to function. Genes specifying the
four RNA polymerase subunits encoded in the chloroplast
genomes of green plants are also absent. Although no experiments with Epifagus virginiana demonstrating synthesis of a
specific plastid-encoded protein have been reported, there are
several lines of indirect evidence suggesting that the plastid
protein-synthesizing system is functional. Wolfe et al. (714)
reported transcription of all eight rRNA and protein-encoding
genes so far examined and cited the following three evolutionary arguments in favor of function. (i) Plastid gene deletions in
Epifagus virginiana are not random but are skewed toward
photosynthetic genes. Although only 5% of photosynthetic
sequences have been retained with respect to tobacco, 80% of
the ribosomal protein sequences are present. (ii) Large open
reading frames are retained in the Epifagus plastid genome. If
these genes were nonfunctional, mutations, truncations, and
internal deletions would have been expected to occur, as is true
of pseudogenes in the Epifagus plastid genome. (iii) The
genera Conopholis and Epifagus share the loss of the photosynthetic and ndh genes, but their rRNA genes are strongly
conserved, suggesting that the evolution of these genes is
constrained by natural selection because they are functional.
Why might the protein-synthesizing systems of Epifagus
virginiana and other colorless plants be essential? The argument of Howe and Smith (275) that plastid protein synthesis
was retained in Epifagus species for the sole purpose of making
the chloroplast-encoded RNA polymerase subunits required
for transcription of the tRNAGIU gene necessary for porphyrin
synthesis (see, e.g., references 20 and 552) is invalidated by the
finding that the RNA polymerase subunit genes are absent
from the Epifagus plastid genome (714). However, one or more
other proteins essential for survival might be encoded and
translated in the Epifagus chloroplast. The best candidate is
clpP, which specifies one subunit of the plastid homolog of the
ATP-dependent Clp protease of E. coli. Perhaps this protease
is involved in processing chloroplast protein precursors into an
active form or in protein degradation.
The thesis that chloroplast protein synthesis is essential is
also supported by work on the genus Plasmodium, the malaria
parasite. This protozoan contains, in addition to its tiny (6-kb)
linearly reiterated mitochondrial genome, a 35-kb circular
DNA molecule that seems to be a residual plastid genome (see
references 273, 484, 700, and 701 for reviews). The 35-kb circle
possesses inverted repeats containing continuous rRNAs with
secondary structures quite similar to those predicted for E. coli
(166, 197, 198). It also encodes tRNAs, two subunits of a
eubacterial-type RNA polymerase, and at least four ribosomal
proteins (165).
Genetic evidence suggests that chloroplast protein synthesis
in C. reinhardtii is essential for survival. Hanson and Bogorad
(245) showed that cells carrying a nuclear mutation conferring
erythromycin resistance on chloroplast ribosomes underwent a
marked reduction in chloroplast ribosome content when
shifted from 25 to 15°C. Ribosome loss was accompanied by
loss of the ability of the mutant to grow at 15°C under all
conditions. Also, although several Chlamydomonas mutants
which have a reduced content of chloroplast ribosomes have
been isolated, none is completely deficient in chloroplast
protein synthesis (247-249, 446). Lastly, mutations with symmetric deletions of the psbA gene encoded within the inverted
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Other supporting evidence exists that such chloroplast-synthesized proteins as Dl, the reaction center polypeptide encoded
by the psbA gene, and the alpha and beta subunits of the CF1
portion of the ATP synthase are made, at least in part, on
thylakoid-bound polysomes (see reference 286 for a summary).
Membrane binding of polysomes may play an additional role
in translational regulation of chloroplast gene expression. In C.
reinhardtii, the distribution of chloroplast mRNAs varied
between the thylakoid and soluble fractions in cells growing
synchronously on a light-dark cycle (41). Thus, a striking
increase in the fraction of membrane-bound polysomes was
observed for both rbcL and psbA mRNAs in the light period.
Thylakoid binding may occur in the light phase because
translation is initiated. In contrast, Klein et al. (308) found that
the psaA, psaB, and psbA transcripts are primarily membrane
associated in dark-grown barley plants. The protein products
of these genes are made in the dark but are unstable in the
absence of chlorophyll (441). Jagendorf and Michaels (286)
correctly point out that the possible role of the thylakoid
membrane itself in translational regulation requires further
investigation.
MICROBIOL. REV.
VOL. 58, 1994
CHLOROPLAST RIBOSOMES AND PROTEIN SYNTHESIS
calli (98, 392).
Experiments with calli cultured from roots of haploid rice
plants derived from pollen grains provide convincing evidence
that plastid protein synthesis is not essential in this system
(246). Albino plants obtained in this way from barley and
wheat have long been known to contain large deletions in the
plastid genome (106, 107), but the deleted molecules form a
heterogeneous collection. By inducing callus cultures from
roots of albino rice plants, Harada et al. (246) obtained isolates
that were homoplasmic for different large deletions. Of five
that were characterized, four lacked the inverted repeat and
the plastid rRNA genes, so that none of these callus cultures
could carry out chloroplast protein synthesis, yet all five
retained one region in common which contained the tRNAGlu
gene. Harada et al. (246) suggest that this gene has been
retained because the tRNAGlu encoded by the gene is essential
for porphyrin biosynthesis. Similarly, heat-bleached leaves of
rye and oat lack chloroplast ribosomes but have substantial
amounts of tRNAGlU and chlorophyll synthetase activity despite their low chlorophyll level (262). Obviously, expression of
the tRNAGlU gene would require functioning of a nucleusencoded plastid RNA polymerase. Retention of small amounts
of plastid DNA in bleached Euglena mutants (254) is probably
not related to a general requirement for tRNAG'U in porphyrin
synthesis, since mitochondrial heme in this flagellate is made
via the animal-type 8-aminolevulinic synthetase pathway which
does not require tRNAGlU (268). In fact, the rRNA genes were
the only ones detected in these deleted plastid genomes.
The existing data currently suggest that chloroplast protein
synthesis may be essential for survival in Chlamydomonas and
Epifagus species but possibly not in other plants such as
tobacco, at least in tissue culture. The plastid-encoded tRNAGlu gene is essential for synthesis of all porphyrins in plants and
algae examined to date, with the exception of Euglena gracilis,
so transcription of this gene is crucial to survival. However, the
Epifagus results suggest that in this plant, at least, transcription
of tRNAGlU depends on a nucleus-encoded RNA polymerase.
CONCLUSIONS
Analysis of chloroplast sequences has been invaluable in
determining variable and conserved regions of the 16S and 23S
rRNA molecules and in predicting their secondary and tertiary
structures. Similar comparisons of ribosomal protein sequences are just beginning but will doubtless prove important
in years to come. Specific domains conserved over a wide
variety of organisms are likely to be important in ribosome
function or assembly. Sequence analysis of ribosomal proteins
in a diverse array of algae and land plants will allow further
refinements in understanding which domains are important for
ribosome function. Although no analysis of mitochondrial
ribosomal proteins has been included here, these will also be a
valuable comparative tool in such research. We hope that this
review will provide a useful starting point for investigations on
these topics.
ACKNOWLEDGMENTS
We thank Hans Bohnert, Donald Bryant, Robin Gutell, Claude
Lemieux, Xiang-Qin Liu, Michael Reith, Alap Subramanian, and
Monique Turmel for sharing unpublished data.
Our work described in this review was supported by NIH grant
GM-19427.
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