Download Genetic Dissection of Chloroplast Biogenesis and

Update on Chloroplast Biogenesis
Genetic Dissection of Chloroplast Biogenesis
and Development: An Overview1[W]
Barry J. Pogson and Verónica Albrecht*
Australian Research Council Centre of Excellence in Plant Energy Biology, Research School of Biology,
Australian National University Canberra, Acton, Australian Capital Territory 0200, Australia
The chloroplast is essential for photosynthesis and
the production of hormones and metabolites. As a
consequence, its biogenesis and development needs to
be coordinated with seedling growth to ensure optimal rates of photosynthesis without oxidative damage
upon seedling emergence. Studies into the processes
of biogenesis and development of chloroplasts have
shown how important chloroplast development during germination is for plant vitality, seed set, and
growth. Indeed, even if chloroplast development is
only impaired in cotyledons (the embryonic leaves of
germinating seedlings) with normal chloroplast development in true leaves, plant growth and yield can
be negatively impacted. Thus, it is necessary to understand the regulation and mechanism of chloroplast
development.
This review will concentrate on how chloroplasts differentiate, giving emphasis to current insights on the
different steps of chloroplast development as well as
into regulatory factors and molecular requirements for
chloroplast biogenesis and development gained from
genetic and mutagenic studies. Given the breadth of
the topic, we are restricted to citing examples of recent
articles and reviews, with a strong emphasis on Arabidopsis (Arabidopsis thaliana), because the majority of
the genetics studies have been performed on this
model plant.
DESCRIPTION OF CHLOROPLAST BIOGENESIS
AND DEVELOPMENT
Chloroplast biogenesis and development in seedlings can be described as the differentiation process
from the plastid progenitor, a proplastid, to a mature
chloroplast, whether direct or via the dark-grown
intermediate form known as an etioplast (Fig. 1). In
developed leaves, chloroplasts are further propagated
by fission in a similar way as observed in bacteria.
Chloroplasts are found in cotyledons, leaves, stems,
fruits, and flowers, depending upon the species and
stage of development. Due to the specialization of
1
This work was supported by the Australian Research Council
Centre of Excellence in Plant Energy Biology (grant no. CE0561495).
* Corresponding author; e-mail [email protected].
[W]
The online version of this article contains Web-only data.
www.plantphysiol.org/cgi/doi/10.1104/pp.110.170365
tissues the biogenesis and development of the chloroplasts differs between organs as well as between
species. For example, we have to distinguish between
seedlings with an epigaeic growth, having cotyledons
that first serve as storage organs but become photosynthetically active, to the hypogaeic seedlings, where
the cotyledons only serve as a storage organ and are
not photosynthetic. Herein, we only refer to chloroplast biogenesis and development in epigaeic seedlings.
That chloroplast development proceeds differently
in cotyledons and true leaves is demonstrated by
genetic studies. That is, chloroplast mutants have
been described that have the phenotype restricted to
one leaf organ, such as chlorotic true leaves, but green
cotyledons as in the variegated (var) and immutans
mutants (Liu et al., 2010). Conversely, the snowy cotyledon (sco) mutant group has chlorotic or bleached
cotyledons but green true leaves (Albrecht et al., 2006,
2008, 2010; Shimada et al., 2007). The sco and cyo1 (shiyo-u means cotyledon in Japanese) mutants are able to
develop almost normally on soil, but their vitality is
reduced compared with wild type as measured by
reduced seed set. Since all of the SCO genes identified
to date are unique and not only expressed in cotyledons but through the entire plant, we have to assume
that there is no redundancy with other members of the
gene family. Furthermore, the different SCO genes
encode proteins involved in complete different processes such as chloroplast protein translation (SCO1),
chloroplast protein folding (SCO2), or being associated with microtubules and the peroxisome (SCO3;
Albrecht et al., 2006, 2008, 2010). Thus, the observed
impairment in chloroplast development in cotyledons
seems to be due to a differential chloroplast development process between the plant organs rather than
redundancy of proteins in the true leaves. A third class
of mutants have a white cotyledon phenotype, but
require Suc to develop green true leaves. Once green
leaves have developed the plants can grow without
Suc and can be transferred to soil for propagation. To
this group belongs, among others, plastid type I signal
peptidase1, which will be discussed later (Shipman and
Inoue, 2009).
So how do plastids develop in seedlings after germination? In dark-germinated seedlings, the largely
undifferentiated proplastid can form an etioplast,
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Pogson and Albrecht
Figure 1. Chloroplast biogenesis and development in seedlings. PLB, Prolamellar body; PT,
prothylakoids.
which exhibits a characteristic lattice-like membranous structure known as the prolamellar body. The
prolamellar body contains the precursor of chlorophyll, protochlorophyllide, bound to its reducing
enzyme protochlorophyllide oxidoreductase (POR),
NADPH, lipids, a few proteins, and typically two
carotenoids, lutein and violaxanthin. From this latticelike structure prothylakoids emanate into the plastid
stroma. In angiosperms, light induces POR enzyme
activity to convert protochlorophyllide into chlorophyllide a, which is subsequently converted into chlorophyll a and b. Gymnosperms additionally have a
light-independent POR enzyme that catalyzes the
same reaction (Forreiter and Apel, 1993). Together
with the production of chlorophyll the internal membranous structure of the chloroplasts, the thylakoids,
develop along with the newly assembled photosystems for assimilating light for photosynthesis. Alternatively, proplastid to chloroplast differentiation in the
light proceeds directly. In some cases, chloroplasts can
also develop from other plastids such as chromoplasts,
though our focus here will be only on chloroplast
differentiation from proplastids.
Tight stoicheometric assembly of nuclear-encoded
and plastidic-encoded proteins together with chlorophylls and carotenoids is essential for photosynthesis,
both with respect to limiting oxidative damage and
ensuring optimal rates for protein synthesis. This
requires coordination between the two organelles at
the level of transcription, translation, import, protein
turnover, and metabolite flux—all of which is largely
controlled by plastid and nuclear factors (Fig. 2; see
“Plastidic and Nuclear Factors Required for Chloroplast Biogenesis and Development”). However,
photosynthesis proceeds within the context of the environment, cell, and leaf development, so environmental and cytosolic processes also influence chloroplast
biogenesis and development, which will be discussed in
“Nonplastidic Factors Required for Chloroplast Biogenesis and Development” and outlined in Figure 3.
PLASTIDIC AND NUCLEAR FACTORS REQUIRED
FOR CHLOROPLAST BIOGENESIS
AND DEVELOPMENT
Here, we provide a brief overview of different
processes identified by mutations in chloroplastic
and nuclear proteins that specifically affect aspects of
chloroplast biogenesis and development as shown in
Figure 2 (see also Supplemental Table S1 for further
information about the genes and corresponding citations).
Nuclear Gene Transcription
Upon illumination, one-third of the nuclear gene
transcription changes (Chen et al., 2010). Among the
genes dramatically up-regulated in the light are most
of the genes encoding chloroplast-targeted proteins,
reflecting that the vast majority of the several thousand chloroplast proteins are nuclear encoded. The
perception of light has been shown to require the
activation of the primary photoreceptors known as
phytochromes, such as phyA and phyB. Protein interaction partners of the phytochromes, PIFs or phytochrome interacting factors, are transcription factors
involved in this light-mediated transcription. Indeed,
the loss of either PIF1 or PIF3 results in delayed
development of the chloroplasts (Moon et al., 2008).
However, other transcription factors are also required
for chloroplast development. Indeed, transcription
factors that are directly involved in the transcription
of photosynthesis genes have been identified, such as
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Chloroplast Biogenesis
Figure 2. Processes required for chloroplast biogenesis and development. Numbers refer to sections in text.
the Golden2-like proteins (GLKs). In Arabidopsis, loss
of both GLK transcription factors leads to a pale mutant phenotype that can be complemented by overexpression of either of the two GLK proteins (Waters
et al., 2009).
Chloroplast Protein Import and Processing
Considerable progress has been made in deciphering the mode of protein import through the outer and
inner envelope (membranes) of the chloroplasts. The
majority of chloroplast-targeted proteins enter the
plastids via the translocon at outer envelope of chloroplast (TOC) and translocon at inner envelope of
chloroplast (TIC) translocon complexes at the outer
and inner envelope, respectively; others are targeted
via the endoplasmic reticulum (Kessler and Schnell,
2009). The proteins are directed to the complex by their
chloroplast targeting peptide by heat shock protein 90
(HSP90) and TOC159. Mutant analyses of the different
components of this complex demonstrate that chloroplast biogenesis is dramatically impaired if the major
component of the outer complex, TOC159, is knocked
out, though they survive if minor components such as
Toc33 or Toc34 are missing (Kessler and Schnell, 2009;
Inoue et al., 2010; Shi and Theg, 2010). The complex
mechanism of protein import into the chloroplast via
the TOC/TIC complex is reviewed elsewhere (Kessler
and Schnell, 2009).
Imported proteins, either into the chloroplast or into
the thylakoids of the chloroplasts, need to be processed by removal of their N-terminal targeting signal.
For the TOC/TIC complex a stromal processing peptidase as well as heat shock proteins have been described (Cline and Dabney-Smith, 2008).
Within the chloroplast, there is also a targeting
system to integrate proteins into the thylakoid
membranes and/or lumen. Integration of proteins
into the membrane can either be spontaneous or via
the chloroplast signal recognition particle pathway that
has been described for light-harvesting chlorophyllbinding proteins (Falk and Sinning, 2010). Part of this
mechanistic pathway is the ALBINO3 protein, which
by loss of function—as the name already suggests—
leads to a white seedling phenotype. Transport of
proteins into the thylakoid lumen is either ATP dependent via the chloroplast Sec pathway or DpH dependent using the chloroplast twin arginin translocation
mechanism. For both pathways, mutants have been
described as being either seedling lethal or affecting
thylakoid formation (Cline and Dabney-Smith, 2008). A
thylakoidal processing peptidase, PISP1, is required for
removing the thylakoid-targeting sequence from thylacoidal proteins and has been shown to be involved in
processing PsbO and PsbP proteins. Loss of the protein
to be seedling lethal if no exogenous carbon source is
provided (Shipman-Roston et al., 2010).
Chloroplast Gene Transcription and Translation
Chloroplast gene transcription, RNA maturation,
protein translation, and modification have a great impact on chloroplast biogenesis and development. This
includes both nuclear-encoded polymerase and plastidencoded polymerase machinery. Plastidic RNA polymerase sigma (sig) factors are required as transcription
factors for chloroplast genes with the loss of sig2 and
sig6 delaying chloroplast biogenesis (Ishizaki et al.,
2005; Chi et al., 2010) and nuclear-encoded RNA
polymerases, such as rpoT, has been shown to affect
chloroplast biogenesis (Azevedo et al., 2008).
Interestingly, a protein that is required for plastid
transcription, pTAC12/HEMERA, has been shown to
be dual targeted to the chloroplast and nucleus. In the
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Pogson and Albrecht
Figure 3. Model of environmental, cellular, and
temporal factors that influence chloroplast biogenesis and development in seedlings. Environmental factors involved are, among others, light,
the cellular factors include the communication
between the organelles, and the embryo development is one of the temporal factors that influences chloroplast biogenesis in germinating
seedlings.
latter it regulates phytochrome-mediated transcription, as it is required for the regulation of PIF1 and
PIF3 protein accumulation. Loss of this protein results
in an albino phenotype that can only be rescued when
both the chloroplast and the nuclear-targeting signals
are accessible (Chen et al., 2010).
While the chloroplast genome only encodes about
100 genes, mutations that affect transcription and
RNA processing, such as RNA editing, lead to impairment of photosynthetic function (Delannoy et al.,
2009). Recently, a large class of nuclear-encoded proteins known as PPRs (pentatricopeptide repeats) have
been demonstrated to be critical for RNA processing,
splicing, editing, stability, maturation, and translation
in the chloroplast. In most cases the phenotypes of PPR
mutations are seedling lethal and typically each PPR
protein has a specific role, be it RNA editing or transcript stability, for a particular chloroplast-encoded
gene (Chateigner-Boutin et al., 2008; Pfalz et al., 2009;
Chi et al., 2010).
Maturated and/or edited chloroplast mRNA is then
translated into proteins by the ribosomal complex.
Complete loss of essential proteins of the plastid ribosomal complex results in an embryo-lethal phenotype.
Phenotypes associated with a reduced functionality
due to leaky point mutations in proteins of the ribosomal complex can be described as virescent, or somewhat green, as is the case for sco1 or the rice (Oryza
sativa) mutant virescent2 (Osvir2; Albrecht et al., 2006;
Sugimoto et al., 2007). Such mutations either result in a
reduced protein translation, as has been shown for sco1
mutant that impairs the binding of chloroplast elongation factor G to the ribosomal complex, or a reduced
content of the ribosomal complex, as described for the
loss of the DNA- and RNA-binding protein Whirly1 in
maize (Zea mays; Prikryl et al., 2008).
Protein Folding and Degradation
Translated proteins need to be folded and further
processed or even degraded if nonfunctional. Chloroplast protein folding is mediated by chaperones, such
as HSP70 and Cpn60, with the hsp70-1 mutation leading to variegated cotyledons (Latijnhouwers et al.,
2010). Also, protein disulfide isomerases have been
shown to be required for protein folding, with, for
example, sco2/cyo1 lesions in a protein disulfide isomerase, resulting in a cotyledon-restricted pale-green
phenotype (Shimada et al., 2007; Albrecht et al., 2008).
The rates of protein translation and degradation are
important for chloroplast development with mutations in the family of FtsH proteases, such as var2,
impairing PSII D1 protein degradation causing a
white-patched phenotype in true leaves, but not cotyledons. This phenotype can be overcome by decelerating protein biosynthesis by second site mutations in
genes involved in protein translation (Miura et al.,
2007; Zhang et al., 2010). The multisubunit ClpPR
proteinase complex has a central role in degrading
proteins and is required for chloroplast protein homoestasis. Loss of ClpP proteins are either embryo or
seedling lethal (Kim et al., 2009b).
Thylakoid Formation and Pigment Biosynthesis
The thylakoids are formed mainly by mono- and
digalactosyldiacylglycerol that are either produced
within the chloroplasts or at the endoplasmatic reticulum. The biosynthetic pathway of the lipids as well as
proteins involved in their integration and formation of
thalkoids has been described elsewhere (Benning,
2009). Many mutations have been reported to affect
thylakoid formation, although a direct involvement of
the corresponding protein in thylakoid formation
could not be attributed to their protein function, rather
than that they are essential in particular thylakoid
protein complexes.
During thylakoid formation the photosynthetic
complexes are formed, which requires a coordinated
import of pigment-binding proteins such as chlorophyll a/b-binding proteins (CAB/light-harvesting
chlorophyll-binding) and the biosynthesis of the pigments. Thus, carotenoid and chlorophyll biosynthesis
is tightly regulated during chloroplast development as
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Chloroplast Biogenesis
they are essential for the assembly of photosynthetic
complexes and photoprotection (Cazzonelli and Pogson,
2010). Therefore, it is not surprising that screens for
chloroplast development mutants have identified
steps in these pathways, such as chloroplast biogenesis4
(clb4) and clb6, which are lesions in enzymes in
the chloroplast 2-C-methyl-D-erythritol 4-P pathway
(Gutiérrez-Nava Mde et al., 2004; Guevara-Garciá
et al., 2005). The chlorophyll precursors, tetrapyrroles,
have been implicated in coordination of chloroplast
biogenesis (Zhang et al., 2006) as well as the ratio of
different carotenoids in photosynthetic tissues that is
regulated by nuclear gene transcription and a histone
methyl transferase, SDG8 (Cazzonelli et al., 2009).
Retrograde Signaling
The fact that most of the proteins needed for chloroplast function are encoded in the nucleus necessitates a tight regulation between the chloroplast
functional status and nuclear gene transcription. Thus,
signaling from the chloroplast is involved in regulating
nuclear gene transcription, a process called retrograde
signaling. Many factors have been suggested to be
involved in the retrograde signaling control, ranging
from reactive oxygen species to metabolites and proteins that regulate or transduce the signals (Pogson
et al., 2008; Pfannschmidt, 2010). Of particular interest
in the context of this article are signals related to
biogenic control, that is, those that affect nuclear
transcription during plastid development (Pogson
et al., 2008). The PSII-associated proteins, EXECUTER1
and EXECUTER2, mediate singlet oxygen signaling
pathways (Kim et al., 2009a). Interestingly, the double
mutant ex1ex2 exhibit white cotyledon regions that
contain undifferentiated plastids that resemble proplastids. This chloroplast biogenesis defect can be
overcome by growth of the seedlings on abscisic
acid-containing media (Kim et al., 2009a).
A series of mutants that affect nuclear transcription
in response to inhibitors of pigment biosynthesis and/
or plastid transcription and translation are the genomes
uncoupled (gun) mutants (Pfannschmidt, 2010). This
series of mutants demonstrate a role for tetrapyrrole
biosynthesis and the PPR protein, GUN1, in retrograde
signaling, but the nature of the signaling cascade is still
debated and although the gun1 mutation affects the
signaling from chloroplast to nucleus, chloroplast biogenesis proceeds normally in the absence of inhibitors.
This and other findings raise the question as to how
much the different retrograde signaling mutants directly affect signaling or result in a perturbation of
plastidic processes and metabolic signatures that alters
nuclear transcription (Pfannschmidt, 2010).
Chloroplast Division
A typical higher plant cell contains between 100
and 300 chloroplasts, which necessitates organelle
division that has been shown to be largely indepen-
dent of cell division. Chloroplast division is mediated
by tubulin-like proteins known as FtsZ and dynaminlike proteins, such as ARC5 (accumulation and replication of chloroplasts) that form concentric rings
within and outside the chloroplast envelope, respectively (Yang et al., 2008). Recent findings include a
role for chaperones, cpn60, and PARC60 in coordinating and regulating division (Glynn et al., 2009;
Suzuki et al., 2009). Affected chloroplast division,
though, does not have any substantive effect on chloroplast development.
NONPLASTIDIC FACTORS REQUIRED FOR
CHLOROPLAST BIOGENESIS AND DEVELOPMENT
Thus far, we have discussed processes and proteins
within the plastid that influence chloroplast biogenesis
and development. However, it is important to note that
environmental, cellular, and temporal factors also contribute to chloroplast biogenesis and development (Fig. 3).
One major environmental factor determining the
biogenesis of chloroplast is light, which is acting via
photomorphogenic pathways to control gene transcription, chlorophyll biosynthesis, and protein degradation; as has been shown in the constitutive
photomorphogenic (cop)/de-etiolated/fusca mutants (Wei
et al., 2008). The cop mutants derepress photomorphogenesis in the dark, enabling the onset of chloroplast
biogenesis in etiolated seedlings and are components
of the so-called cytosolic COP signalosome, which is
involved in ubiquitin-dependent protein degradation
(Wei et al., 2008). COP1 is chryptochrome regulated, a
blue-light sensor that deactivates the signalosome,
thereby inhibiting further ubiquitination and degradation of proteins involved in light signaling such as
the transcription factorHY5 (Long Hypocotyl5; Wei
et al., 2008). Interestingly, loss of four PIF proteins
(PIF1, PIF3, PIF4, and PIF5) results in chloroplast biogenesis in dark-grown seedlings due to up-regulation
of genes for chloroplast function comparable to the cop
mutants (Shin et al., 2009).
Not only environmental factors influence chloroplast development but also components within the cell
such as peroxisomes and the cytoskeleton (Albrecht
et al., 2010). The SCO3 protein is required for chloroplast biogenesis and signaling with sco3 mutation
impairing chloroplast and etioplast differentiation in
seedlings. Unexpectedly, the SCO3 protein is not located to the chloroplast or nucleus but to the periphery
of peroxisomes and is associated with the microtubule
cytoskeleton (Albrecht et al., 2010). Perturbations to
the actin cytoskeleton coupled with a lack of change
in nuclear and plastidic transcription in sco3 suggest
that transport and/or import of specific, but as-yetunknown, proteins or metabolites might require
interactions between chloroplasts, cytoskeleton, and
peroxisomes during biogenesis in seedlings.
Temporal factors also have an impact on chloroplast
biogenesis in seedlings. Embryo maturation influences
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Pogson and Albrecht
chloroplast development, that is, even though proplastids are present in the seed prior to germination
and are largely undifferentiated, the way in which
they are formed during embryogenesis affects chloroplast biogenesis. Mutants affected in chloroplast
biogenesis in the embryonic leaves (cotyledons) of
germinating seedlings, such as sco and ex1ex2, are not
affected in chloroplast development during embryogenesis in the developing silique (Albrecht et al., 2008;
Kim et al., 2009a). Indeed, it could be shown that these
mutants exhibit normal green cotyledons if the mature
green embryo was extracted from green seed and
germinated precociously. On the other hand, if siliques
of the ex1ex2 double mutant were covered with aluminum foil, so that the embryo matured in the dark
instead of continuous light prior to seed desiccation
and dormancy, then seedlings derived from this darkmatured embryo do not exhibit impaired chloroplast
biogenesis (Kim et al., 2009a). Thus, some as-yetunknown process(es) during embryogenesis influences the differentiation of proplastids to chloroplasts
in germinating seedlings.
SUMMARY AND FUTURE PROSPECTS
The process of chloroplast biogenesis and development requires a network of environmental, cellular,
and temporal factors. The environmental factors are
influencing gene transcription and protein degradation processes largely regulated via light signaling or
oxidative stress. Cellular factors can be divided into
those within the chloroplast and those outside of the
plastid. To date most studies have identified chloroplast-localized proteins involved in import, chloroplast
transcription/RNA maturation/protein translation,
assembly, and signaling. Temporal factors have to be
taken into account and insights into the effects of embryogenesis on photomorphogenesis reveal new fields
to analyze the regulation of chloroplast biogenesis.
Key questions that remain include: (1) what is the
interaction between chloroplast development and
photomorphogenesis; (2) how do interactions with
different organelles influence the biogenesis of the
chloroplast; (3) what are the components in retrograde
signaling that mediate chloroplast development; and
(4) what are the check points in chloroplast biogenesis
and development?
Supplemental Data
The following materials are available in the online version of this article.
Supplemental Table S1. List of mutants and genes affected and involved
in chloroplast biogenesis.
ACKNOWLEDGMENTS
We thank Christoffer Johnsson for critically reading this manuscript.
Received December 1, 2010; accepted February 3, 2011; published February
17, 2011.
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