Download Biogenesis and Evolution of Photosynthetic (Thylakoid) Membranes

Bioscience Reports, Vol. 19, No. 5, 1999
MINI REVIEW
Biogenesis and Evolution of Photosynthetic (Thylakoid)
Membranes
Reinhold G. Herrmann
Work in molecular phylogeny during the past few years has documented that the biogenesis,
maintenance, adaptation, and controlled resorption of thylakoid (photosynthetic) membranes are by far more complex than the requirements for maintaining their function,
especially in plants (eukaryotic photoautotrophs). Plants, due to their genome compartmentation that originated in a cohabitation of cells (endosymbiotic events), have evolved
an exquisite set of regulatory mechanisms for their energy-transducing organelles. These
operate in concert with basically ancient regulatory circuits originating in the organelle
ancestors. It appears that the biogenesis of thylakoid membranes, as that of chloroplasts
in general, cannot be understood without knowledge of the history of the cells.
KEY WORDS: Chloroplast; thylakoid membrane; genome compartmentation; functional
molecular phylogeny; regulation.
INTRODUCTION
Thylakoid membranes capable of oxygenic photosynthesis contain an organized set
of intrinsic and peripheral supramolecular protein complexes, associated with the
membrane’s lipid bilayer [1], that function cooperatively to couple the photooxidation of water with electron transport and chemiosmosis. This biochemical process,
imperative for life on our globe, generates the high-energy metabolite ATP, the
reducing equivalent NADPH, both utilized for the photosynthetic dark (carbon fixation) reactions, and molecular oxygen. “Oxygenic” thylakoid membranes are found
in cyanobacteria and in the photosynthetic organelles (plastids) of plants. Plastids,
as mitochondria, contain DNA, the mechanisms to maintain this information and
to convert it into function. Their genetic machinery is part of the compartmentalized
genetic apparatus characteristic of eukaryotic cells. One of the outstanding characteristics of these specialized biomembranes is their enormous physiological and
structural versatility including changes in composition, i.e., to protect and adapt the
photosynthetic machinery to different environments, especially to light regimes.
Photosynthetic Organelles and Their Evolution
The family of photosynthetic organelles, chloroplasts, rhodoplasts, cyanoplasts
( = cyanelles), phaeoplasts etc., in algae, mosses and vascular plants is without doubt
1
Botanisches Institut der Ludwig-Maximilians-Universitat, Menzinger Str. 67, D-80 638 Munchen,
Germany.
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0144-8463/99/1000-0355$16.00/0 © 1999 Plenum Publishing Corporation
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the consequence of a cyanobacterial endosymbiosis which followed the a-proteobacterial endocytobiosis that led to the generation of mitochondria and hydrogenosomes. This implies that all modern photosynthesis originates in the eubacterial
domain of Life [2] and explains the fundamental feature of photosynthetic organelles
to house a residual genetic system. During the past decade the approach of molecular
phylogeny and ultrastructural information have permitted to construct an outline of
a natural genealogical system which includes all major groups of photoautotrophs
(plants). The chronometer molecules used to deduce plant genealogy were initially
rRNA sequences, then organelle DNAs from widely distant plants [e.g., 1, 3–5],
especially operon structures and genes involved in photosynthesis or in the flux of
genetic information in organelles, more recently nuclear genes involved in thylakoid
biology, and nowadays entire organismic coding potentials [1, 3–7]. The striking
similarity between corresponding cyanobacterial and chloroplast gene and operon
structures, nuclear genes encoding chloroplast proteins that plastid operons are missing, substantial sequence conservation, and, relevant in the context of this contribution, the almost identical design of the basic photosynthetic machinery in
thylakoids (but not of their antenna systems) in the various plant lineages, are all
consistent with the idea of a monophyletic ancestry of the organelle and host cell,
i.e., that all plastids ultimately trace back to a single, primary (eukaryotic/prokaryotic) endocytobiosis [3–5], approximately 2800 million years ago. However, photosynthetic organelles have also arisen through the incorporation of unicellular
autotrophic eukaryotes (microalgae) into heterotrophic or autotrophic host organisms. This implies that plant cells can be descendants of associations not only of
three, but also of four or even five cells (reviewed in 3, 4, 8]. With the exception of
Glaucocystophyta, red algae, and green algae and their derivatives, the photosynthetic organelles of the majority of proto- and thallophytic photosynthetic organisms, such as Euglenophyta, Dinophyta, Phaeophyta, Diatoms, Cryptophyta,
Xanthophyta etc., originated from several of such, so-called secondary (and tertiary)
endocytobioses, with different hosts and different endocytobionts. This resulted in
complex photosynthetic organelles, surrounded by 3-4 envelope membranes.
Cellular cohabitation is usually not considered to be a major driving force in
evolution. However, it generated one of the three domains of life [2], the eukarya.
Furthermore, endocytobioses that led to the plant kingdom not only occurred polyphyletically, they also permitted the development of advanced (true multicellular)
life, in combination with oxygenic photosynthesis also of terrestrial life [1, 3]. Multicellularity arose approximately 1.3 x 109 years ago, probably first with thallophytic
plants (red algae). The development of basic and advanced eukaryotism had profound effects on the biogenesis of organelles, in particular thylakoid membranes.
One of the crucial features which distinguishes eukaryotes from prokaryotes is
the evolution of an enormous spatiotemporal morphogenetic potential that the latter
have evolved. Especially the step to land, i.e., the transition from the aqueous to
a gaseous environment, more than 600 million years ago, exposed plants to new
physiological conditions and marks an interval of unparalleled biochemical innovation with crucial changes in genome and phenotype. Novel metabolic pathways,
such as lignin, flavonoid, wax and hormone synthesis, and biochemistry for structures have been principal responses to life on land. The general principles, e.g., the
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development of protection strategies, internalization of vital functions and organs,
the development of intricate fluid transportation systems, of cell and tissue systems
for stabilization, are comparable to those found in animal groups, but were invented
earlier than by those. The evolution of new pathways and of the novel structural
potential is poorly understood. Collectively, it resulted in significantly more highly
differentiated plants.
Evidence as it stands suggests that living plants are “relicts”, that is, that much
of the phylogenetic development should be deposited in their genomes, that both,
plant bodies and their ontogeny, are under the same or similar kind of developmental control in all main groups, and that much morphological diversity is reduceable
to the gradual acquisition of novel genes or gene combinations, and their integration
into existing regulatory networks. Also, much diversity can be interpreted in terms
of modification of basic structural and metabolic units. Classical examples are found
in the organelle “plastid” with its different modifications in higher plants, or in the
changes of the organ “leaf” into functionally very different photosynthetic-, floraland storage-type structures. In multicellular organisms chloroplasts diversified developmentally into related organelles with different functions, photosynthetic and nonphotosynthetic versions, such as leucoplasts or chromoplasts, each one comprised of
subclasses of the organelle. These include, for instance, bundle sheath and mesophyll
chloroplasts with structurally and functionally different thylakoid membranes [9].
The differentiation of all these diverse structures and cells that resulted in different
tissues and organs of a plant is brought about by specific, spatially and temporally
quite stringently regulated genetic programmes. Thus, establishing the biochemistry
for morphogenetic potential, as the step to multicellularity in general, required a
new quality of regulation, i.e., genetic information for regulation in space, which
relates to thylakoid membranes.
Plant Genomes and Their Evolution
Evidently, the initial associations of independent cells that generated the photosynthetic higher cell developed into a compartmentalized genetic system with a common metabolism and a common inheritance. This implies that biogenesis, function
and modification of photosynthetic membranes, as of the entire photosynthetic
organelles, are embedded into the outlined genetic context of the plant cell which
has changed during evolution and now includes remnants of the ancestral, eubacterial genomes that both chloroplasts and mitochondria have preserved. The approach
of molecular phylogeny has shown that the principal aspect in eukaryotic genome
evolution resides in an enormous capacity for restructuring genetic material [1, 3].
Although the causes for this fundamental feature of the eukaryotic cell and the
underlying mechanisms are not yet fully understood, the outlines that happened
have emerged during the past few years. This work has therefore led to a new understanding of the chloroplast and of crucial aspects of the photosynthetic membrane
and process in particular, as well as of the plant genome and plant cell in general,
which all appear in a new light, phylogenetically and functionally. It becomes more
and more evident that major aspects in design, biogenesis and regulation of thylakoids cannot be understood without the history of the plant cell (see below).
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Genome restructuration must have been relatively frequent, massive, and highly
complex. The most relevant observations for this are (i) the degree of functional gene
translocations, (ii) promiscuous DNA [10] and its distribution [3, 11], (iii) repeated,
convergent functional losses and transfers of genes in individual plant lineages [5],
(iv) comparison of coding potentials between cyanobacteria, a-proteobacteria and
eukaryotes, and (v) the different distributions of genes and DNA segments among
nucleus, plastids and mitochondria in the latter cell type. DNA rearrangements in
the plant cell included loss, intercompartmental transfer as well as gain of function,
which are equivalent in quality [3]. They have probably occurred between all genetic
compartments, although the transfer of genetic information occurred preferentially
from the organelles to the nucleus, and was accompanied by the establishment of
nuclear regulatory dominance [3, 12]. Gene translocations occurred gradually,
though with different kinetics after an endosymbiosis had occurred, and predominantly at the unicellar level. They are still ongoing, and not restricted to DNA and
its product “protein”. They can include multiple gene transfer/replacement [5], gene
transfer that resulted in product detour [6, 12], possibly gene transfer from an initial
endocytobiont in a “replaced” secondary endosymbiont, or the translocation of
RNA molecules or RNA/protein complexes across organelle envelopes [13, 14].
Clearly, this design diminishes the identity [10] and the independence of the cellular
genetic compartments. Its central functional and phylogenetic consequence is an
integrated genetic system, not semiautonomous organelles [1, 3]. From a functional
point of view, genome compartmentation adds a substantial degree of regulatory
complexity to the system (see below).
The elimination of redundant genes, probably to avoid competition between
the homologous basic metabolisms of the symbiotic partners, as well as the findings
that a significant fraction of the chloroplast enzymes that are nuclear-coded is of aproteobacterial (mitochondrial) origin and that most of the basic metabolism is of
eubacterial (endosymbiotic) origin [6] illustrate convincingly the intercompartmental
restructuration process. They are indicative of genetic integration and instructive
with regard to the cell status and the complexity of changes. Different from what
one would expect, the establishment of genetic nuclear regulatory dominance with
principal elements tracing back to the domain archaea, which is considered to be or
to have contributed to the ancestor of the eukaryotic host cell, has not found a
pendant in the metabolic dominance of that cell. The plant cell has retained much
more of the eubacterial (endosymbiont) biochemistry than is reflected in its organelle
DNAs, as can be judged from the finding that gene losses occurred to a surprising
extent from the host cell.
Available information indicates both a directionality of gene transfer [3] and a
time scale of the endosymbioses [5]. Today, genes for single- or simple-chain enzymes
of the organelle are all nuclear-coded and hence were efficiently and probably early
translocated from the organelles. On the other hand, the transfer of genes for complex organelle structures has occurred, and probably still occurs, in a gradual way.
The principal consequences are that such structures are of dual genetic origin [1],
and that the degree of translocation differs between organelles and plant lineages.
Chloroplasts contain various compounds of dual genetic origin, in addition to the
thylakoid membrane [1], the inner envelope membrane, and several components of
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Table 1. Structures of Dual Genetic Origin in Chloroplasts and
Plant Mitochondria
thylakoid membrane—respiratory membrane
[2, 3]
organelle stroma
ribulose bisphosphate carboxylase/oxygenase
70S ribosome— 70S/60S ribosome
acetyl-CoA carboxylase
Clp protease
eubacterial-type RNA polymerase
transcript processing machinery
[15]
[16]
[17]
[18]
inner envelope membrane
[e.g, 19]
the organelle stroma (Table 1) [15–19]. In all these structures it appears that basically
genes for regulatory components were translocated first, for thylakoid membranes
probably also peripheral compounds. The core components of the supramolecular
thylakoid complexes that usually harbour all subunits involved in redox and catalytic processes are generally organelle-coded [1]. The comparison of chloroplasts
and mitochondria illustrates that the genetic integration of mitochondria is more
advanced. In plant mitochondria, only the energy-transducing respiratory membrane
and the organelle ribosomes required for their synthesis are genetic hybrids, but less
so than their plastid equivalents (Table 1).
Unravelling the details of the outlined phylogenetic puzzle and its functional
consequences, using appropriate living and fossil plants as models, should help to
clarify origin and evolution of the plant biogenetic and spatiotemporal morphological potential. In particular, this includes the generation of an intracellular communication system between the genetic compartments, during the development of
multicellularity and morphological diversity also the establishment of intercellular
communication, and their integration into regulatory networks.
Functional Consequences of Gene Rearrangements
The operation of the compartmentalized, integrated genetic system in the plant
cell and the dual genetic origin of complex organelle structures, which both are
fundamental features of the eukaryotic genetic system (see above), required the
establishment of novel, intercompartmental regulatory circuitries. In terms of biogenesis, the dispersal of genes for complex chloroplast structures among organelle
and nucleus implies that the delivery of the components from two sources of protein
synthesis in the cytosol and plastid respectively, has to be coordinated. Further information is required to express the genetic programmes in multicellular organisms.
Regulation in this scenario is highly sophisticated since the regulatory schemes have
to coordinate the integrated genetic system in its entirety, i.e., in time, quantity,
in multicellular organisms also in space. The functional consequences of genome
compartmentation and of multicellularity for the biogenesis, maintenance, adaptation and resorption of the photosynthetic membrane are obvious at all levels of
regulation, with different mechanisms, over a wide range of time scales, and with
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nuclear regulatory dominance. Estimates indicate that in the order of 20% of the
nuclear coding potential is involved in the management of the energy-transducing
organelles. Several points of general interest emerged.
(i) Nuclear genes involved in thylakoid biogenesis. The majority of information
on expression of nuclear genes for constituent thylakoid proteins has been obtained
through the transgenic approach with modified promoter sequences, especially from
single copy genes, and appropriate reporter genes. Following transformation, the
pattern of a regulatory sequence is determined by analysing the spatiotemporal
expression pattern in situ or in vivo. Gel retardation assays, the use of gene machines
etc., in turn, have provided access to genes and polypeptides involved in the regulation of genes encoding thylakoid structure.
The success of a chloroplast gene that has been translocated to the nucleus
during evolution required the acquisition of an appropriate sequence context for
expression and for protein import, either during the translocation process or by
rearrangement after translocation. In line with phylogenetically individual transfer
events of originally organelle-encoded genes are the dispersal of genes in the nuclear
genome [20], and that the generally coordinated, often induced (light, hormones)
regulation or organ-specific expression of nuclear genes encoding thylakoid proteins
is not brought about by common cis-elements or common trans-acting factors as is
known from other collectively expressed groups of genes (e.g., heat shock genes) [3].
Even genes that code for different subunits of the same membrane complex usually
possess entirely different promoters (and transit peptides; see below), unlike homologous genes in different higher plants. Moreover, the inference that most genome
restructuration occurred at the unicellular level [5], and the temporal distance of
some 700 million years between the generation of plant cells and the appearance of
multicellular plant forms imply that much information for regulation in space had
to be generated after gene translocation. Comparative studies of promoters from
photosynthetic genes [e.g., 21, 22], including those from C3 and C4 plants [9], indicate that at least some information to ensure (transcriptional) regulation in space
must have been acquired during evolution. Important aspects of organelle biology,
notably the streamlining and integration of acquired promoter sequences into the
signal transduction chains, the principles of transcriptional changes as a means of
physiological adaptation of thylakoid membranes, and the link to the complex network of interacting signalling components and cascades remains to be explored. In
spite of substantial knowledge in detail, a coherent picture has not yet emerged.
(ii) Gene expression in plastids. The coding potential of chloroplast DNA is
generally organized in operons [22, 23]. However, genes for a given thylakoid polypeptide complex are generally not clustered, but dispersed throughout the chromosome and often cotranscribed with genes for other multisubunit assemblies. This has
important consequences for gene expression, especially with regard to posttranscriptional processes. Nevertheless, transcription in chloroplasts is substantially more
complex than previously anticipated [24] and unique, since it has now been proven
that the chloroplast of higher plants operates with more than one RNA polymerase.
These use different promoter types. The existence of a nuclear-coded, second plastidlocated RNA polymerase resembling phage-type and mitochondrial enzymes, in
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addition to the ancient, organelle-coded eubacterial multisubunit core enzyme, has
recently been demonstrated [e.g., 25], at least for higher plants [3]. This implies that
promoters in chloroplast chromosomes are complex due to multiple transcriptional
initiation sites. Some operons seem to be exclusively transcribed by either the plastidcoded or the nuclear-coded RNA-polymerase, the majority of them is transcribed
by both, with different basic cis elements for each polymerase type [26, 27].
Strikingly, the nuclear-coded enzyme appears to be the result of an internal
duplication of the gene for the corresponding mitochondrial enzyme [25]. The
appearance of this additional RNA polymerase in plastids that became the sole kind
of enzyme in mitochondria [25, but see 28] has caused promoter changes in the
respective organelle chromosomes. These changes are more or less terminal in mitochondria and probably at an intermediate stage in plastids [3]. The interaction of
the two plastid RNA polymerases in tissue- and development-specific expression of
plastid genes is not understood nor are the phylogenetic origin of the nuclear-coded
enzyme, its appearance, and the reasons why a second enzyme has been established.
Recent findings of our laboratory on the off-white rpo-deficient plastome mutants
cannot be reconciled with simple assumptions such as that the plastid-encoded core
polymerase were involved in the expression of photosynthetic genes, while the
enzyme of nuclear origin in that of the housekeeping genes of the organelle.
Although previous opinion that the major level of regulation in chloroplasts is
not transcriptional but posttranscriptional [e.g., 24] has to be revised, modification
of RNA molecules and translational control represent key levels of regulation in
thylakoid biogenesis. The known polycistronic transcripts of plastid chromosomes
often give rise to complex sets of overlapping RNA species, usually through a series
of processing steps. Posttranscriptional RNA changes are complex. The multiple
mechanisms known are interwoven into a regulatory network. Nearly a dozen enzymatic machineries have been deduced to modify plastid RNA, such as activities
involved in group I and group II intron splicing, 5' and 3' terminal shortage by
endo- and exonucleolytic activities, 3' poly(A) addition to mRNA fragments, 3' CCA
addition to tRNAs or nucleotide substitutions and nucleotide modifications. C-toU conversions and the reverse process, designated RNA editing, are often essential
for the decoding and/or for the structural and functional fidelity of the respective
protein, or change the expression patterns and/or RNA stability [29]. The edited
sites in plastid transcripts are generally found in reading frames, but can also be
present in nontranslated RNA segments. Editing can restore initiation, termination,
or conformationally crucial codons, and hence represents an important means for
nuclear regulatory control, as the other posttranslational modifications. With the
exception of some components involved in the 3' processing of plastid encoded
mRNAs and RNA stability [30], the enzymes and factors involved in posttranscriptional processing and transcript stability are not known. Although the majority of
regulatory components involved is encoded in nuclear genes, it is relevant to mention
that the modification machinery is of dual genetic origin (Table 1, [18]) and that
the extensive transcript processing in chloroplasts and some of its mechanisms are
phylogenetically derived, and not original traits. They are not or to a much lesser
extent found in prokaryotes or in thallophytes, and hence appear to be phylogenetic
innovations [e.g., 31]. Some evidence suggests also that editing may have been
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acquired from the nuclear and mitochondrial compartments. If correct, this would
be an interesting analogy to the nuclear-coded, second plastid RNA polymerase,
and imply that the nucleus, which itself relies on RNA processing in gene expression,
converts analogous complexity to the regulation of gene expression to the organelle.
(iii) Genome rearrangements had substantial consequences for later biogenetic
processes as well, besides the demand that a functional intracellular gene transfer to
the nucleus requires the return of the respective protein into the organelle [32].
Import of proteins, their transport to and assembly at various locations within the
chloroplast depend on specific targeting and sorting signals, translocation machineries and protein folding/unfolding catalysts (chaperones) [e.g., 33–36]. Plastid-encoded proteins possess generally intrinsic thylakoid-targeting and assembly signals.
One of the rare exceptions is cytochrome f which is made as an apoprotein precursor
molecule with a transitory, N-terminal signal peptide-like extension. Nuclear-coded
plastid proteins require import sequences that first direct translocation across the
envelope membranes, and subsequently target proteins to their suborganelle destination, including into or across thylakoids. Highly specific, soluble and membranebound receptor systems decode the targeting signals and initiate translocation
through protein conducting channels [e.g., 33].
For chloroplasts, targeting signals show expectedly no obvious sequence homology (see above), but fall into two principal classes, stroma- and stroma-thylaloidtargeting presequences. The latter operate successively with two distinct translocation and processing systems located in the envelope/stroma and thylakoids. In
contrast to the import of cytosolically made precursor proteins which appear to
use a common general import machinery [33], work on protein targeting to and
translocation across the thylakoid membrane rests on at least four targeting systems,
the Sec-, SRP-like, ApH- and spontaneous pathways, that function non-competitively with specific subclasses of membrane proteins [e.g., 34, 35]. Although this complexity is only partly understood functionally and phylogenetically, it is noteworthy
in the context of the topic of this article that at least three of these pathways possess
ancestry in translocation systems that operate in bacteria. The discovery of these
multiple routes has therefore contributed significantly to our understanding of
assembly processes of the photosynthetic machinery and, importantly, has provided
new insights into evolutionary relationships, differences and novelties between proand eukaryotic structures and between membrane-targeting systems of different
organelles. Initially, the ApH route was thought to be a phylogenetic gain, since it
was found only with nuclear-coded, extrinsic (lumenal) thylakoid components, such
as the 23 and 16 kDa polypeptides of the oxygen-evolving system, that cyanobacteria
are lacking [1, 3]. This turned out not to be correct. The Rieske FeS protein of the
cytochome b6f complex is a first example for an ancient as well as for an integral
protein using the ApH route [36]. Different from all other compounds known to use
this route, it operates with an uncleaved thylakoid targeting signal, and integration
of its FeS centre appears to be required for transport, reminiscent of an only recently
found specific group of bacterial proteins which share a cofactor-mediated folded
state during membrane translocation [see 35]. It also lacks the twin arginine motif
characteristic of all other ApH-dependent transit peptides, and, again different from
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all other components known to use this route, interacts for various chaperones,
successively with cpn60, Rubisco activase, and with the stromal Hsp100 (ClpC),
competitively with Sec route components [36].
An exception to this appears to be the integration process of polypeptides using
the spontaneous mechanism which depends on bitopic transit peptides [37]. It turned
out recently that this pathway constitutes a general route for the integration of
bitopic proteins of nuclear (but not plastid) origin. The mechanism may not exist
with the equivalent components of prokaryotes and secondary plastids (in which
they are plastid-encoded), where existing. This has been shown, for instance, from
the study of the related ATP synthase subunits CFo-I and -II (b, b') [37], which
originated in a gene duplication at the prokaryotic stage, but, in the chlorophyll a/
b lineage of plants, are favourably encoded in different cellular compartments. This,
obviously, would imply that gene translocation can change late biogenetic processes
[see [3]). Furthermore, this work has also shown that at least some of the second
domains of bipartite transit peptides were not inherited from the prokaryotic progenitor of chloroplasts.
ACKNOWLEDGEMENTS
This work was supported by the Deutsche Forschungsgemeinschaft (SFB 184),
and the Fonds der Chemischen Industrie.
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