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Plant Physiol, December 2001, Vol. 127, pp. 1394-1398
SCIENTIFIC CORRESPONDENCE
Assembly, Function, and Dynamics of the Photosynthetic Machinery
in Chlamydomonas reinhardtii
Jean-David
Rochaix
Departments of Molecular Biology and Plant Biology, University of
Geneva, 30, Quai Ernest Ansermet, 1211 Geneva, Switzerland
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INTRODUCTION |
The green unicellular alga
Chlamydomonas reinhardtii occupies a unique position among
photosynthetic organisms. Although its photosynthetic function is very
similar to that of vascular plants, it combines the advantages of
unicellular organisms, which include fast growth under controlled
environmental conditions with highly sophisticated genetics of the
nuclear, chloroplast, and mitochondrial compartments. The aim of this
article is to provide an overview of this powerful algal model system
and to show that C. reinhardtii is ideally suited for
studying the biogenesis of the photosynthetic apparatus, its
structure-function relationship, and its remarkable ability to adapt to
changing environmental conditions such as light quality and quantity
and nutrient limitation.
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BASIC GROWTH PROPERTIES |
C. reinhardtii cells are oval shaped, approximately 10 µm in length and 3 µm in width, with two flagella at their anterior end. The cells contain a single chloroplast occupying 40% of the cell
volume and several mitochondria. There are two mating types, mt+ and
mt , determined by two structurally distinct alleles of the mating
type locus. The haploid vegetative cells multiply through mitotic
divisions. However, upon nitrogen starvation the vegetative cells
differentiate into gametes, and cells of opposite mating type fuse to
give rise to a zygote, which will undergo meiosis under appropriate
light-dark conditions and produce four haploid daughter cells that can
resume vegetative growth. It is also possible to recover mitotically
dividing diploid cells after the mating reaction, a property that is
useful for determining whether a mutation is recessive or dominant and
for testing whether mutations with the same phenotype belong to the
same complementation group (see Harris, 1989 ).
In the presence of acetate in the growth medium, the photosynthetic
function of C. reinhardtii cells is dispensable. This feature has been exploited extensively for isolating and maintaining mutants deficient in photosynthetic function. Cells can thus be grown
under three different conditions: in minimal medium with light and
CO2 as the sole carbon source (phototrophic
growth), in acetate-containing medium with light (mixotrophic growth), or without light (heterotrophic growth). The growth of the cells can
easily be synchronized by light-dark cycles.
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THREE TRANSFORMABLE GENETIC SYSTEMS |
Like plants, C. reinhardtii contains three genetic
systems located in the nucleus, chloroplast, and mitochondria.
Mutations in the genomes of these three compartments can be easily
recognized by their unique segregation patterns during crosses. Whereas
nuclear mutations segregate according to the classical Mendelian rules, chloroplast and mitochondrial mutations are normally transmitted uniparentally from the mt+ and mt parents, respectively (see Harris,
1989).
The complexity of the nuclear genome has been estimated at 100 Mbp
(Harris, 1989). Currently, the genetic map includes 148 loci
distributed over 17 linkage groups. In addition, approximately 240 RFLP
and short tagged sequence markers have been mapped to all linkage
groups with an average spacing of 4 to 5 centiMorgan or 0.4 to
0.5 Mbp (Silflow, 1998). The nuclear transformation yield is
sufficiently high to allow for genomic complementation of nuclear
mutants (see Kindle, 1998). In addition, because nuclear transformation
of this alga occurs mainly through non-homologous recombination, the
transforming DNA integrates randomly into the nuclear genome. Thus,
transformation can be used as a mutagen for tagging genes.
The complete sequence of the chloroplast genome of C. reinhardtii has been recently completed (J. Maul, J. Lilly, and D. Stern, unpublished data). It consists of circular molecules, 204,210 bp
in length, and contains 34 genes involved in photosynthesis, 31 genes
involved in chloroplast transcription and translation, one protease
gene, 29 tRNA genes, and nine genes of unknown function. Chloroplast
transformation can be achieved routinely in C. reinhardtii by bombarding cells with DNA-coated tungsten particles (Boynton and
Gillham, 1993). In contrast to nuclear transformation, chloroplast transformation occurs exclusively through homologous recombination. Because foreign selectable marker genes are available, e.g.
aadA (Goldschmidt-Clermont, 1991) and aphA-6
(Bateman and Purton, 2000), conferring resistance to specific
antibiotics in the chloroplast, it is possible to inactivate specific
genes or to perform site-directed mutagenesis on any plastid gene of
interest (see below). This reverse genetics approach has been rather
successful, especially for elucidating the function of conserved open
reading frames, also called ycfs, present in the plastid
genomes of several plants, algae, and cyanobacteria (see Rochaix,
1997). Chloroplast transformation has also been extremely useful for
studying chloroplast gene expression, especially when it is combined
with classical genetic analysis. It has been possible to dissect
regulatory elements such as promoters and 5' and 3' untranslated
regions, and to use chimeric genes consisting of chloroplast regulatory
elements fused to reporter genes for identifying the target
sites of specific nucleus-encoded factors required for
chloroplast gene expression. This analysis has revealed that some of
these factors act on the 5' untranslated region of specific
mRNAs and that they are required for mRNA stability or translation (see
Goldschmidt-Clermont, 1998).
The 15.8-kbp linear mitochondrial genome of C. reinhardtii
encodes seven proteins involved in respiration, one protein resembling a reverse transcriptase, two ribosomal RNA genes that are fragmented and interspersed with other coding sequences, and three tRNA genes (see
Remacle and Matagne, 1998). The other tRNAs have to be imported from
the chloroplast or cytosol. Although mitochondrial transformation has
been reported for C. reinhardtii, the yield is rather low. However, the availability of several drug-resistant mitochondrial mutations offers promising new selectable markers for mitochondrial transformation (Remacle and Matagne, 1998).
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MOLECULAR CROSS TALK BETWEEN NUCLEUS AND CHLOROPLAST |
An area in which C. reinhardtii is
especially powerful as model system is the biosynthesis of the
photosynthetic apparatus that occurs through the concerted interactions
between the chloroplast and nuclear genomes. An extensive analysis of
nuclear mutants deficient in photosynthesis has revealed that besides
the mutations that directly affect the genes of the components of the
photosynthetic apparatus, the vast majority of the mutations are in
genes encoding factors that are required for several chloroplast
post-transcriptional steps, including RNA stability, RNA processing,
translation, and the assembly of photosynthetic complexes (see
Goldschmidt-Clermont, 1998). The number of these genes is surprisingly
high, and their products act in a gene-specific manner. Several of
these genes have recently been isolated through genomic complementation
of the mutants with genomic cosmid libraries or by gene tagging. The
phenotypes of some of these photosynthetic mutants resemble those of
mutants of Arabidopsis and maize (Zea mays),
indicating that a similar complex nuclear-chloroplast network may exist
in higher plants (Barkan and Goldschmidt-Clermont, 2000). The
sequencing of the Arabidopsis genome has indeed revealed that as many
as 3,000 nuclear genes encode chloroplast proteins (Abdallah et al., 2000). Many of these factors may be involved in chloroplast gene expression.
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GENETIC DISSECTION OF PHOTOSYNTHESIS |
The primary reactions of photosynthesis take place in the
thylakoid membranes within the chloroplast. An important advantage of
C. reinhardtii is that the functional state of its
photosynthetic system can be monitored in vivo with noninvasive
techniques such as chlorophyll fluorescence transients, absorption
spectrophotometry using detecting flashes, and photoacoustic techniques
(Joliot et al., 1998). The availability of a homogenous cell population grown under controlled environmental conditions is especially important
for this type of analysis. Because of the large number of mutants of
C. reinhardtii obtained both by random and site-directed mutagenesis, this alga has emerged as one of the best model systems for
this functional in vivo analysis. The alga is also suited for in vitro
studies because it can be grown in large amounts, making the
purification of the photosynthetic complexes relatively easy. An
additional important feature of C. reinhardtii is its ability to synthesize chlorophyll both in a light-dependent and light-independent manner. The cells are thus able to fully assemble the
photosynthetic apparatus in the dark in marked contrast to higher
plants. Many mutants deficient in photosynthesis are light sensitive
and need to be grown in the dark. It is thus possible to isolate
photosynthetic complexes from these mutants and to study their properties.
An example of the power of coupling genetics, chloroplast
transformation and in vivo and in vitro kinetic spectrophotometry in
C. reinhardtii is provided by the analysis of the
structure-function relationship of photosystem I (PSI). The PSI
complex acts as light driven oxidoreductase that transfers electrons
from plastocyanin or cytochrome c6 in the
thylakoid lumen to ferredoxin in the stroma (Fig.
1). The crystal structure of the complex
from a cyanobacterium has been determined (Jordan et al., 2001) and
revealed in particular the location of the redox components P700, the
primary electron donor, A0, a chlorophyll
a, A1, a phylloquinone, and the 4Fe-4S center FX that is liganded by PsaA and PsaB. The
structure of the complex is symmetrical in this region with two
potential electron transfer branches between P700 and
FX (Fig. 1). The in vivo analysis of the kinetics
of electron transfer from the quinone to FX
revealed two kinetic components (Joliot and Joliot, 1999). By mutating quasi symmetrical residues of PsaA and PsaB near the quinone, it was
found that a particular mutation in one branch affected the faster
component, whereas an analogous mutation in the other branch affected
the slower component, indicating that in striking contrast to
photosystem II (PSII), both branches are active in PSI (Guergova-Kuras
et al., 2001). It is not possible within this short review to mention
the numerous studies performed with C. reinhardtii on the
structure-function relationship of the other parts of PSI and on the
other complexes PSII, the cytochrome
b6f complex, the ATP
synthase, and Rubisco (for details, see Hippler et al., 1998).
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Figure 1.
Schematic view of the photosynthetic complexes
within the thylakoid membrane. The photosynthetic complexes PSII, PSI,
and the cytochrome b6f complex are
shown. PSII: D1 and D2, Main reaction center polypeptides;
QA and QB, primary and
secondary electron acceptors of PSII. PQ, Plastoquinone pool;
QO, binding site of the cytochrome
b6f complex for plastoquinol. LHC,
Light-harvesting complex; LHCIIP, phosphorylated form of LHCII. PC,
Plastocyanin; C6, cytochrome
c6. PSI: PsaA and PsaB, Reaction center
subunits with the ligands P700, a Chl dimer that acts as primary
electron donor, and the electron acceptors A0,
A1, and their homologs A0',
A1' in the other active branch, and the 4Fe-4S
center FX. FA,
FB, 4Fe-4S centers, Terminal electron acceptors
of PSI liganded by the PsaC subunit. Fd, Ferredoxin. PsaF, Docking
protein for PC (plastocyanin) and c6
(cytochrome c6).Ycf3 and Ycf4, PSI assembly
factors. Crd1, Di-Fe enzyme required for PSI accumulation under Cu
deficiency; Mco, hypothetical multi-Cu oxidase. Stt, Genetically
identified factors involved in state transition. In State I, the mobile
part of LHCII is associated with PSII, whereas in State II it is
phosphorylated and associated with PSI.
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DYNAMICS OF THE PHOTOSYNTHETIC APPARATUS |
Plants and algae have the remarkable ability to adapt and to
modulate the operation of the photosynthetic apparatus in response to
changes in light quality and quantity. Too much light can be harmful
and excess light energy can be dissipated as fluorescence or heat
(non-photochemical quenching [NPQ]). At least part of this
non-radiative energy dissipation occurs through reversible covalent
modifications of the thylakoid xanthophylls and involves the reductive
de-epoxidation of violaxanthin to zeaxanthin (xanthophyll cycle) that
is triggered by the pH gradient produced by photosynthetic electron
flow (see Muller et al., 2001). Among C. reinhardtii mutants
deficient in NPQ, npq1 was found to be defective in the xanthophyll cycle and provided direct genetic evidence for the importance of zeaxanthin in NPQ (Niyogi et al., 1997). This genetic analysis also revealed that the pigments of the xanthophyll cycle derived from  -carotene, and most likely lutein derived from
 -carotene are required both for NPQ and for protection against
oxidative damage in high light (Muller et al., 2001).
C. reinhardtii has proven to be uniquely suited for
analyzing state transition, a process that involves the reversible
distribution of excitation energy from PSII to PSI through a
reorganization of the antennae (State I to State II transition;
Wollman, 2001). In this way the two photosystems that are serially
linked by the photosynthetic electron transfer chain operate at the
same pace and the quantum yield is optimized. Key factors in this
process are the redox state of the plastoquinone pool, the cytochrome b6f complex, in particular the state
of occupancy of the quinol binding site QO, and
the LHCII kinase(s). In State I, the mobile part of LHCII is associated
with PSII. Preferential excitation energy flux to PSII reduces the
plastoquinone pool and leads to the activation of the LHCII kinase and
phosphorylation of LHCII that is laterally displaced from PSII in the
grana to PSI in the stroma lamellae of the thylakoid membranes (Vallon
et al., 1991; Delosme et al., 1996). Such a State I to State II
transition is associated with a significant fluorescence decrease in
C. reinhardtii because as much as 80% of LHCII is
displaced. In contrast, only 15% to 20% of LHCII is mobile in higher
plants. The large decrease in fluorescence during a State I to State II
transition has been used for screening mutants deficient in this
process by fluorescence video imaging (Fleischmann et al., 1999; Kruse
et al., 1999). Some of these mutants are deficient in LHC
phosphorylation, whereas others are still able to phosphorylate the
antenna. It should be noted that the distribution of excitation energy
to the two photosystems is 0.45 for PSII and 0.55 for PSI in State I
and 0.15 for PSII and 0.85 for PSI in State II. Thus, the cross
sections of the PSII and PSI antennae are nearly balanced in State I
and considerably uneven in state II in C. reinhardtii. It
has indeed been shown that linear electron transfer is active in State
I, whereas cyclic electron transfer operates in State II (Finazzi et
al., 1999). Interestingly, the state transition mutants have been used
for demonstrating that in C. reinhardtii state transition acts as a switch from linear electron transfer in State I to cyclic electron flow in State II (G. Finazzi and F. Rappaport, unpublished data). Mutants blocked in State I are unable to switch to cyclic electron flow under State II conditions. State
transition in C. reinhardtii serves not only as a light
adaptation mechanism, but also for rerouting photosynthetic electron
flow, thereby allowing the organism to adapt to changes in cellular
demand for ATP (Wollman, 2001).
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RESPONSE OF THE PHOTOSYNTHETIC SYSTEM TO NUTRIENT
LIMITATION |
A genetic analysis of the response to nutrient limitation in
C. reinhardtii has been especially rewarding. Upon depletion of sulfate or phosphate, the cells respond by arresting cell division, by decreasing photosynthetic electron flow, by inducing a highly efficient sulfate or phosphate uptake system, and by secreting arylsulfatase or phosphatases that are able to metabolize other sources
of sulfate or phosphate (see Grossman and Takahashi, 2001). SacI, a mutant unable to synthesize arylsulfatase upon
sulfur starvation, fails to diminish photosynthetic electron flow and dies in the light unless photosynthesis is blocked by
3-(3,4-dichlorophenyl)-1,1-dimethylurea, an inhibitor of PSII
(Wykoff et al., 1998). The SacI protein contains 12 transmembrane domains and resembles ion transporters.
Limitation in micronutrients such as Cu or Fe also induce specific
responses in C. reinhardtii. The best known example is the
replacement of plastocyanin by cytochrome
c6 under Cu starvation (Wood, 1978;
Merchant and Bogorad, 1987). Both proteins transfer electrons between
the cytochrome b6f
complex and PSI. Recent work has revealed a novel role of Cu in
photosynthesis through a search for mutants that are conditionally
deficient in photosynthetic activity under Cu deprivation (Moseley et
al., 2000). One of the mutants obtained, crd1, lacks PSI and
LHCI under Cu limitation, but not in the presence of nutritionally
adequate Cu. This phenotype is rather unusual, as the analysis of
numerous mutants deficient in PSI or LHC accumulation has shown that
either of these complexes can accumulate in the absence of the other.
The phenotype of the crd1 mutant reveals an unrecognized
role for Cu in the maintenance of PSI and LHCI. With its three 4Fe-4S
clusters, PSI is a major Fe sink in the chloroplast. Because the
chlorotic phenotype of the crd1 mutant in the absence of Cu
is recapitulated in Fe-deficient wild-type cells, it is likely that the
observed effect is mediated through interactions between Cu and Fe
metabolism. Crd1, which contains a dicarboxylate di-Fe binding site,
could possibly facilitate the mobilization of Fe in the chloroplast
when a multi-Cu oxidase is necessarily ineffective (Fig. 1; S. Merchant, unpublished data).
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PERSPECTIVES |
Since the isolation of the first chloroplast mutants of C. reinhardtii nearly 50 years ago, the genetic and molecular
analysis of this unicellular alga has greatly progressed. Among
eukaryotic photosynthetic organisms, C. reinhardtii has
emerged as one of the most powerful model systems for analyzing the
cooperative interplay between the nuclear and chloroplast genetic
systems in the biogenesis of the photosynthetic apparatus. Because
chloroplast transformation is easy to perform with C. reinhardtii, it has become the organism of choice for the
structure-function analysis of the components of the photosynthetic
apparatus. Thanks to the impressive advances in the determination of
the atomic structures of PSI, PSII, the cytochrome
b6f complex, LHC, and the ATP
synthase, it is possible, using chloroplast site-directed mutagenesis
and transformation, to selectively alter residues for addressing
specific questions about photosynthetic electron transfer processes.
Perhaps the most exciting area concerns the remarkable dynamics and
flexibility of the photosynthetic apparatus in response to changes in
light conditions and in nutrient limitation, which has only recently become accessible to experimental investigation. We still have a very
limited understanding of the molecular identity of the components of
the signal transduction pathways that are used in these processes. The
coming years should provide novel insights and many surprises.
ACKNOWLEDGMENTS
I thank D. Stern for communicating unpublished results and M. Goldschmidt-Clermont and S. Merchant for helpful comments.
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FOOTNOTES |
Received July 17, 2001; returned for revision July 30, 2001; accepted August 15, 2001.
*
E-mail jean-david.rochaix{at}molbio.unige.ch; fax
41-22-702-6868.
www.plantphysiol.org/cgi/doi/10.1104/pp.010628.
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LITERATURE CITED |
-
Abdallah F, Salamini F, Leister D
(2000)
Trends Plant Sci
5: 141-142[CrossRef][ISI][Medline]
-
Barkan A, Goldschmidt-Clermont M
(2000)
Biochimie
82: 559-572[Medline]
-
Bateman JM, Purton S
(2000)
Mol Gen Genet
263: 404-410[CrossRef][Medline]
-
Boynton JE, Gillham NW
(1993)
Methods Enzymol
217: 510-536[ISI][Medline]
-
Delosme R, Olive J, Wollman FA
(1996)
Biochim Biophys Acta
1273: 150-158[CrossRef]
-
Finazzi G, Furia A, Barbagallo RP, Forti G
(1999)
Biochim Biophys Acta
1413: 117-129[Medline]
-
Fleischmann MM, Ravanel S, Delosme R, Olive J, Zito F, Wollman FA, Rochaix JD
(1999)
J Biol Chem
274: 30987-30994[Abstract/Free Full Text]
-
Goldschmidt-Clermont M
(1991)
Nucleic Acids Res
19: 4083-4089[Abstract/Free Full Text]
-
Goldschmidt-Clermont M
(1998)
Int Rev Cytol
177: 115-180[ISI][Medline]
-
Grossman A, Takahashi H
(2001)
Annu Rev Plant Physiol Plant Mol Biol
52: 163-210[CrossRef][ISI][Medline]
-
Guergova-Kuras M, Boudreaux B, Joliot A, Joliot P, Redding K
(2001)
Proc Natl Acad Sci USA
98: 4437-4442[Abstract/Free Full Text]
-
Harris EH
(1989)
The Chlamydomonas Source Book: A Comprehensive Guide to Biology and Laboratory Use. Academic Press, Inc., San Diego
-
Hippler M, Redding K, Rochaix JD
(1998)
Biochim Biophys Acta
1367: 1-62[Medline]
-
Joliot P, Béal D, Delosme R
(1998)
In
JD Rochaix, M Goldschmidt-Clermont, S Merchant, eds, The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 443-449
-
Joliot P, Joliot A
(1999)
Biochemistry
38: 11130-11136[CrossRef][Medline]
-
Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N
(2001)
Nature
411: 909-917[CrossRef][Medline]
-
Kindle KL
(1998)
In
JD Rochaix, M Goldschmidt-Clermont, S Merchant, eds, The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 41-61
-
Kruse O, Nixon PJ, Schmid GH, Mullineaux CW
(1999)
Photosynth Res
61: 43-51[CrossRef]
-
Merchant S, Bogorad L
(1987)
EMBO J
6: 2531-2535[ISI][Medline]
-
Moseley J, Quinn J, Eriksson M, Merchant S
(2000)
EMBO J
19: 2139-2151[CrossRef][ISI][Medline].
-
Muller P, Li XP, Niyogi KK
(2001)
Plant Physiol
125: 1558-1566[Free Full Text]
-
Niyogi KK, Bjorkman O, Grossman AR
(1997)
Plant Cell
9: 1369-1380[Abstract]
-
Remacle C, Matagne RF
(1998)
In
JD Rochaix, M Goldschmidt-Clermont, S Merchant, eds, The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 661-674
-
Rochaix JD
(1997)
Trends Plant Sci
2: 419-425[CrossRef]
-
Silflow CD
(1998)
In
JD Rochaix, M Goldschmidt-Clermont, S Merchant, eds, The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 25-40
-
Vallon O, Bulte L, Dainese P, Olive J, Bassi R, Wollman FA
(1991)
Proc Natl Acad Sci USA
88: 8262-8266[Abstract/Free Full Text]
-
Wollman FA
(2001)
EMBO J
20: 3623-3630[CrossRef][ISI][Medline]
-
Wood PM
(1978)
Eur J Biochem
87: 9-19[ISI][Medline]
-
Wykoff DD, Davies JP, Melis A, Grossman AR
(1998)
Plant Physiol
117: 129-139[Abstract/Free Full Text]
© 2001 American Society of Plant Physiologists
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TOP
INTRODUCTION
BASIC GROWTH PROPERTIES