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EMBO reports 4, 8, 752–756 (2003)
doi:10.1038/sj.embor.embor906
AOP Published online: 18 July 2003
From light to life: an interdisciplinary journey into photosynthetic activity
Workshop on Molecular Genetics and Biophysical Aspects of
Photosynthesis
Giovanni Finazzi1, Fabrice Rappaport1 & Michel Goldschmidt-Clermont2
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1 Institut de Biologie Physico-Chimique, 13 Rue
Pierre et Marie Curie, 75005 Paris,
France
2 Departments of Plant
Biology and Molecular Biology, University of Geneva, Sciences II,
30 Quai E. Ansermet, 1211 Geneva 4,
Switzerland
To whom correspondence should be addressed
Michel Goldschmidt-Clermont Tel: +41 22 379 6188; Fax: +41 22 379 6868;
michel.goldschmidt-clermont@molbio.unige.ch
Received 22 April 2003; Accepted 26 June 2003; Published online 18 July 2003.
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Introduction
One intention of the organizers of the EMBO workshop on Molecular
Genetics and Biophysical Aspects of Photosynthesis was to bring together
scientists with different backgrounds and experimental approaches. Indeed, the
meeting proved that photosynthesis is a privileged field of interdisciplinary
research, in which each of the many methods used in its investigation (whether
biophysical, biochemical or biological) provides measurements on a timescale
appropriate to the vastly different turnover rates for the process it
investigates. As pointed out in one of the opening lectures by L. Mets
(Chicago, IL, USA), these can vary in range from fractions of picoseconds for
the energy transfer between the chlorophylls in the light-harvesting antennae
to days or years for growth and development. Genetic analysis stood out at the
meeting because, in synergy with other approaches, it contributes to our
understanding across a vast range of these timescales. Indeed, the analysis of
mutant phenotypes was a recurrent theme throughout the meeting (a typical
example is shown in Fig. 1).
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| On the snowy slopes of Les Diablerets, some skiers seemed to be
outlining the Z-scheme of photosynthetic electron flow: up the PSII chair lift
to Les Mazots, down the b6f trail and up the PSI chair lift to the
summit at Meilleret. Others were depicting cyclic flow by repeatedly riding the
PSI lift to Meilleret and returning to its base via the b6f trail.
But the flow of skiers did not generate a proton gradient, and if any energy
was captured it was in the form of renewed enthusiasm to attend the sessions of
the EMBO workshop entitled: 'Molecular Genetics and Biophysical Aspects of
Photosynthesis', which was organized by J.-D. Rochaix, W. Rutherford and F.-A.
Wollman and took place from 26 to 29 January 2003.
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Figure 1
Chlorophyll fluorescence imaging of photosynthetic mutants.
(A) Digital imaging of the fluorescence emitted by wild-type seedlings
(WT; left) and a mutant plant that lacks the cytochrome b6f complex
( b6f; right). (B) Kinetics of fluorescence emission
measured at the points indicated in (A) by the red and black squares.
The mutant was provided by D. Stern (Ithaca, NY, USA).
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Assembly and maintenance of the photosynthetic
machinery
Making and maintaining the plastid requires the import of thousands
of nucleus-encoded polypeptides (Fig. 2). S. Baginsky
(Zürich, Switzerland) warned that in his extensive proteomic survey of
plastid proteins,  40% were not predicted by the commonly used algorithms
to be imported into the plastid. This implies that the plastid proteome may be
significantly larger than previously estimated.
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Figure 2
Plastid biogenesis. Many nucleus-encoded polypeptides are imported
into the plastid through the translocons of the outer and inner chloroplast
envelope membranes (Toc and Tic, respectively). Some of these polypeptides
assemble with others that are encoded by plastid DNA to form photosynthetic
complexes or metabolic enzymes. Many of the nucleus-encoded polypeptides also
participate in various steps of plastid gene expression. The nucleocytosolic
and plastidic compartments also exchange metabolites and regulatory signals.
(Image drawn by Nicolas Roggli, University of Geneva, Switzerland.)
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Protein translocation into the chloroplast is known to be mediated
by the Toc and Tic complexes in its outer and inner envelope membranes,
respectively. Toc159 and Toc34 are GTP-binding proteins that also bind
precursor polypeptides; Toc75 forms the membrane pore and Toc64 is involved in
the docking of precursors to the membrane. J. Soll (Munich, Germany) reported
that Toc75 and Toc159 are sufficient to allow GTP-dependent polypeptide import
when they are reconstituted into liposomes. He suggested that the energy from
GTP hydrolysis might allow Toc159 to drive the import of the polypeptide
precursor through the Toc75 pore. F. Kessler (Neuchâtel, Switzerland)
showed that the Toc159 protein is localized in the outer envelope, as expected,
but is also present at similar levels in the cytosol, as a soluble protein.
Furthermore, a Toc159 mutant polypeptide that does not bind or hydrolyse GTP
localized only to the cytosol in Arabidopsis, and failed to integrate
into the envelope in vitro. Thus, a GTP-hydrolysis/GDP-exchange cycle
may regulate the insertion of Toc159 into the chloroplast envelope.
Over the course of evolution, specialized photosynthetic membranes,
the thylakoids, appeared at the same time as the emergence of oxygenic
photosynthesis. J. Soll showed that treatment with inhibitors of vesicular
membrane fusion leads to the accumulation of vesicles in the chloroplasts of
land plants. This suggests that plastids have evolved a vesicular mode of
thylakoid membrane biogenesis. As endosymbiotic descendants of a prokaryote,
plastids may have acquired this pathway from their original eukaryotic host.
The cargo of these vesicles might include some of the proteins that are
directed to the thylakoid membrane or to its lumen, as well as lipids, pigments
and pigment precursors.
The vast majority of chloroplast proteins are encoded by nuclear
genes, including the factors involved in chloroplast gene expression. In plants
and algae, mutational analyses have revealed that the products of a
surprisingly large class of nuclear genes are required for the
post-transcriptional steps of plastid gene expression, including: RNA
processing, RNA splicing, RNA turnover, translation, protein assembly and
degradation (M. Goldschmidt-Clermont, Geneva, Switzerland; W. Gruissem,
Zürich, Switzerland; P. Westhoff, Düsseldorf, Germany).
In the green alga Chlamydomonas reinhardtii, the translation
of cytf (a subunit of the cytochrome b6f complex; Fig. 3), is repressed by the low levels of unassembled cytf
that accumulate when other subunits of the complex are missing (Choquet et al., 2001). This is in contrast with the
fate of other subunits, which are rapidly degraded when unassembled. Y. Choquet
(Paris, France) presented evidence that similar negative-feedback loops may
also regulate the translation of specific subunits from all the other
photosynthetic complexes. This homeostatic regulation may be important because
it maintains constant pools of these subunits, which might be important for the
assembly of the others.
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Figure 3
The thylakoid membranes and their domains, and the dynamics of the
photosynthetic electron-flow machinery. In the thylakoid membranes (lower
panel), photosynthetic activity results from the balance between light
absorption and utilization. Several dynamic processes regulate the absorption
of light: thermal dissipation in the photosystem II (PSII) outer antenna
light-harvesting complex II (LHCII) is modulated by the xanthophyll cycle.
Phosphorylation induces the reversible migration of this subcomplex from PSII
to PSI (a state transition), which adjusts the relative absorption properties
of the two photosystems and allows for the optimization of their relative
activities. This dynamic regulation of photosynthesis also involves electron
transport. Alternative electron carriers can be recruited depending on nutrient
availability. The copper-containing plastocyanin (PC) enzyme can be replaced by
cytochrome c6 (Cyt c6) under conditions of
Cu2+ deficiency. In addition, supramolecular structures, granal
stacks, the uneven distribution of complexes, and protein–protein
interactions result in compartmentalization of the photosynthetic complexes and
electron carriers. This is likely to modulate the efficiency of linear (blue)
and cyclic (red) electron flow, and thus that of ATP synthesis, through the
generation of a H+ gradient. Fd, ferredoxin; FNR,
Fd:NADP+ reductase; PQ, plastoquinone. (Image drawn by Nicolas
Roggli, University of Geneva, Switzerland.)
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The photosystems (PSI and PSII) are complexes of proteins and
pigments that convert light into redox potential through a photochemical
reaction. This process occurs in a specialized structure, the reaction centre.
The photosystems contain proteins that absorb light (the inner antennae), and
are surrounded by many light-harvesting complexes (LHCs), which form the outer
antennae. The assembly of these complex structures is a dynamic process, as
described for PSII by E.-M. Aro (Turku, Finland). By using protein
pulse-labelling followed by two-dimensional electrophoresis to analyse
chloroplast mutants of tobacco, she showed that the small PSII subunit PsbL is
essential for the stable association of the CP43 subunit with PSII monomers,
whereas PsbJ is required for the formation of the PSII–LHCII
supercomplexes.
H. Scheller (Frederiksberg, Denmark) is using Arabidopsis to
investigate the role of individual PSI subunits. Of particular interest are
those that are found in plants and algae but not in cyanobacteria (PSI-G, -H,
-N and -O), as the X-ray structure of PSI that is available at present was
obtained from a cyanobacterium (see below). Electron fluxes through the
photosystems are regulated by state transitions, a process in which LHCII
migrates between PSII and PSI in response to phosphorylation (Fig. 3). Plants lacking PSI-O, -H or -L show reduced state
transitions. The binding of PSI-O to the complex depends on both PSI-H and
PSI-L. Crosslinking studies show that the three proteins are closely associated
and that PSI-L can interact with the LHCII protein Lhcb1. Thus, these subunits
may provide a docking site for phosphorylated LHCII on PSI, explaining their
role in state transitions.
The harvesting of light for photochemistry is a dangerous business,
and PSII pays a heavy toll in photodamage. As reviewed by I. Ohad (Jerusalem,
Israel), damage occurs at all light intensities, and the primary victim is the
PSII D1 subunit, which is rapidly degraded and replaced through an active
repair cycle. An early step in the repair cycle is the cleavage of D1 on the
lumenal side of the thylakoid membrane by an endoprotease, DegP2, to give a
23-kDa intermediate. Z. Adam (Rehovot, Israel) showed that this fragment is
further degraded by FtsH, a membrane protease that faces the stroma, in a
process that can be reconstituted in vitro using recombinant proteins.
The genes that encode this protease belong to large families, with some members
being expressed differently in response to light or other forms of stress.
Members of the FtsH family in Arabidopsis may have partly
redundant functions, as suggested by the lack of an obvious phenotype in an
FtsH1 mutant and the variegation in the leaves of Arabidopsis
FtsH2 and FtsH5 mutants. By contrast, their orthologues in other
species may be less redundant; P. Nixon (London, UK), reported that disruption
of one of the FtsH genes in Synechocystis 6803 leads to increased
light sensitivity and severely impaired repair of PSII in high-intensity
light.
Apart from its role in photosynthesis, light also regulates many
aspects of plant development and gene expression. Phytochromes are
light-receptor protein kinases that are regulated by red and far-red light.
Phytochrome-like proteins have also been found previously in prokaryotes, and
A. Vermeglio (Cadarache, France) described a novel type that is found in
Rhodopseudomonas palustris and in a symbiotic Brahdyrhizobium
strain. The BphP gene encodes a phytochrome that has the familiar
chromophore-binding domain and a PAS (Per/ARNT/Sim) domain, which is otherwise
found only in eukaryotic phytochromes, but lacks a histidine-kinase domain. In
this case, the light signal is transduced by the inhibitory
protein–protein interaction of BphP with PpsR, which is itself a negative
transcriptional regulator of photosynthetic genes in aerobic conditions.
Plants adapt not only to changes in light conditions, but also to
many other aspects of their environment, and in particular to nutrient
limitation. To systematically explore this type of adaptation, A. Grossman
(Stanford, CA, USA) used microarrays of Chlamydomonas complementary
DNAs. He showed that acclimatization to sulphur deprivation involves increases
in the levels of many transcripts, for example those encoding proteins involved
in sulphur scavenging and assimilation, and cell-wall proteins with
particularly low sulphur contents, as well as decreases in other transcripts,
such as those for PSII proteins. In sulphur acclimation 1 (sac1),
a regulatory mutant that dies under conditions of sulphur stress, the levels of
many (although not all) of these transcripts do not change. Thus, the Sac1
regulator governs part of the response, but is not the master regulator.
Under low copper conditions, Chlamydomonas cells respond by
activating backup genes to replace copper-containing proteins through several
different pathways. For example, plastocyanin is replaced by an iron-containing
cytochrome as an electron carrier from the b6f complex to PSI (Fig. 3). In addition, S. Merchant (Los Angeles, CA, USA) showed
that for iron assimilation, the Crd2 pathway is activated to bypass a
copper-containing ferroxidase. Mutations in the genes for these surrogates lead
to copper-conditional phenotypes. Merchant's group also identified a pair of
homologous genes, Crd1 and Cth1, that are reciprocally expressed
under copper limitation versus repletion and encode oxygen-dependent di-iron
enzymes. The reduced chlorophyll protein accumulation in crd1 mutants in
conditions of copper limitation was explained by the finding that Crd1 is
involved in chlorophyll biosynthesis, consistent with an earlier proposal that
its homologue in Rubrivivax gelatinosus, AcsF, is the elusive cyclic
oxidative cyclase (C. Astier, Gif-sur-Yvette, France). It is puzzling that the
crd1 mutation specifically affects PSI and its antenna LHCI.
Iron limitation causes a dynamic adaptation of the protein
composition of the thylakoid membrane. Using two-dimensional gel
electrophoresis and mass-spectrometry, M. Hippler (Jena, Germany) was able to
unravel part of the mechanism for the protein degradation that is involved in
this process: degradation of the LHCI protein Lhca3 involves a specific
amino-terminal cleavage.
Light harvesting
Light excitation is transferred from the antenna proteins to the
reaction centres, where a strongly reducing species of the centre is formed
and, consequently, an electron is transferred between a primary electron donor
and an acceptor. Without detailed knowledge of the structure of the
photosystems and their antenna partners, the evaluation of the energy-transfer
parameters has usually been based on theoretical models that comprise an
energy-transfer ('hopping') rate between two chlorophylls in the antenna and
the intrinsic photochemical rate of the reaction centre. During the past
decade, however, the atomic structures of the main photosynthetic complexes
have become available, and femtosecond laser-spectroscopy has permitted the
estimation of the rates of individual energy-transfer steps. These two
breakthroughs have greatly enhanced our knowledge of light harvesting in
photosynthetic organisms. On the basis of these approaches, R. van Grondelle
(Amsterdam, The Netherlands) proposed a model for PSI in which the average time
taken for a single energy-transfer step is 150 fs and trapping requires
8 ps.
R. Bassi (Marseille, France) investigated the ability of LHCII to
dissipate excess light energy (photoprotection). Non-radiative dissipation in
LHCII is modulated by changes in the carotenoid composition of the different
LHC proteins that form this complex, with xanthophylls having a major role.
Bassi showed that different binding sites have different affinities for
carotenoids, and that stress conditions (mainly light and cold) affect their
nature and number in the LHC proteins. Thus, carotenoid binding regulates the
efficiency of light harvesting by allosteric modification of antenna protein
conformation.
The peripheral (LH2) and core (LH1) antennae of photosynthetic
bacteria are highly symmetrical structures compared with their plant
counterparts, PSII/LHCII and PSI/LHCI. This is probably due, at least in part,
to the sizes of their elementary building blocks, which in bacteria are small
proteins that assemble into larger ring systems. No such symmetry is found for
PSI, whose outer antenna (which is composed of LHCI dimers) is located on one
side of the core. In PSII, an intermediate situation is found, as LHCII trimers
display a perfect C3 symmetry. R. Cogdell (Glasgow, UK) discussed the question
of the true oligomeric state of the bacterial LH antennae, pointing out that
the integrity of the LH rings may be disrupted in vivo. He proposed that
members of the PufX protein family could allow the passage of the
membrane-soluble quinone through the LH rings that surround the reaction
centre.
Reaction centres
The photochemical and photo-induced electron-transfer reactions that
occur in the reaction centres (for a review, see Nicholls
& Ferguson, 2002) have long been studied using both spectroscopic
techniques and site-directed mutagenesis. This knowledge has now been advanced
by the recent determination of the X-ray structures of PSI and PSII. P. Fromme
(Temple, Arizona, USA) presented the structure of the PSI complex from the
cyanobacterium Synechococcus elongatus at 2.5-Å resolution,
clearly identifying the positions of the individual subunits and cofactors. She
focused on the two phylloquinones, molecules that have been reported to be
equally reduced on exposure to light, but are then reoxidized by the nearest
[4Fe4S] cluster at rates that differ by almost one order of magnitude. She
proposed that their different local environments could explain this difference.
Indeed, two of the four structural lipids identified bind in close vicinity to
the phylloquinones and are very different: one is a phosphatidyl glycerol and
the other a monogalactosyl diacyl glycerol.
As a complementary approach to three-dimensional crystallography, P.
Sétif (Saclay, France) showed that the interaction between PSI and a
soluble electron carrier, ferredoxin (Fd), can be studied by site-directed
mutagenesis. As well as confirming the electrostatic nature of their
interaction, extensive mutagenesis of charged residues on both partners allowed
Sétif to draw a detailed map of the Fd docking site on PSI.
A remarkable recent achievement is the determination by X-ray
crystallography of the three-dimensional structure of PSII from the
thermophilic cyanobacterium S. elongatus at 3.8-Å resolution.
Fromme discussed how the recent refinement of the side-chain assignments made
it possible to identify His 190 of the D1 polypeptide. Functional studies
suggested a role of His 190 in the deprotonation that accompanies the oxidation
of YZ, a D1 tyrosine residue that is part of the electron-transfer
chain. However, the crystallographic data are incompatible with this role, as
the distance between these two residues is not consistent with the
hydrogen-bond network that had been proposed to facilitate proton release from
YZ. The finding is consistent, however, with the previously reported
absence of any electronic coupling between the tyrosine radical and any
nitrogen atom (for a review, see Diner, 2001). The
electron-density map allowed Fromme to propose a structural model for the
tetra-manganese cluster involved in water oxidation. In the most likely
arrangement, three manganese atoms would be strongly coupled to one another and
the fourth weakly coupled to the other three.
Another useful technique for studying the reaction centres is
high-field electron paramagnetic resonance (HFEPR). This provides invaluable
information about the distances between redox cofactors, their orientation and
the interactions between a free radical and its protein environment under
'native' conditions. Using this strategy to study PSII, S. Un (Saclay, France)
was able to measure the angular orientations of the different radicals that are
transiently generated during PSII activity. This information complements the
crystallographic structure, which, even at its current resolution, provides
only the overall protein topology of the complex and the positions of the
electron transfer cofactors. HFEPR can also be used in a classical
spectroscopic approach to characterize the interactions between the redox
cofactors and the nearby residues. These interactions, such as hydrogen bonds,
have an important role in determining the redox properties of the
electron-transfer components.
Supramolecular features of the photosynthetic
apparatus
Structural and functional studies of the antenna rings that surround
the reaction centers of photosynthetic bacteria (discussed above) have led to
the concept of the supramolecular organization of the electron-transport
chain.
In plants and algae, the peculiar arrangement of the thylakoid
membranes might result in the compartmentalization of photosynthetic complexes.
The thylakoids comprise stacks of vesicles (the grana) that are connected by
unstacked regions (the stromal lamellae), with an uneven distribution of
complexes between the two regions (Fig. 3). New insights
into this structure and the mechanism of grana formation in native thylakoid
membranes were presented by Z. Reich (Rehovot, Israel), who used scanning-force
microscopy to obtain images of native, hydrated specimens at up to 3-nm lateral
resolution and 0.3-nm vertical resolution. The images revealed detailed
features of the thylakoid surfaces, including the distribution of individual
proteins across the stroma, grana margin, and grana-end membrane domains. Using
immunogold labelling, Reich was able to identify two of the photosynthetic
complexes (PSI and the ATP synthase) in the membranes, and to visualize their
high density at the grana margins.
The consequences of compartmentalizing photosynthetic activity have
been analysed by P. Joliot (Paris, France). He showed that cyclic electron flow
around the PSI complex (Fig. 3) operates at a rate that
is close to the maximum turnover of photosynthetic flow during the first
seconds of illumination of dark-adapted leaves. This high efficiency implies
that the cyclic and linear transfer processes (between the PSI and PSII
complexes) do not compete with one another, and therefore that they are
structurally isolated. According to Joliot's model, the cyclic pathway would
operate within a supercomplex that is present in stromal lamellae and includes
stoichiometric amounts of PSI, the cytochrome b6f complex,
plastocyanin and ferredoxin. Consistent with this possibility are results from
the analysis of an engineered Arabidopsis line (generated in the
laboratory of H.V. Scheller). In this line, the gene producing the PSI subunit
PsaF, which is required to dock plastocyanin to PSI, is silenced by antisense
RNA, and this results in an inhibition of cyclic electron flow.
Another example of limited diffusion in photosynthetic membranes
that greatly influences the overall photosynthetic activity is provided by the
state transitions that occur in Chlamydomonas, in which the fraction of
LHCII that migrates between PSII and PSI is greater (up to 80%) than in other
photosynthetic organisms (15–20%). G. Finazzi (Paris, France) showed
that state transitions in this alga result not only in changes in the
absorption properties of the two photosystems, but also in a reversible switch
between linear and cyclic electron flow. This is probably due to the
significant protein rearrangement that occurs in thylakoid membranes in
response to the movement of LHCII, and the consequent modifications in the
diffusion properties of the hydrophobic electron carriers.
Metabolism
Photosynthesis drives not only CO2 fixation, but also
several other biochemical activities in the plastid, such as nitrogen
assimilation and the biosynthesis of amino acids, fatty acids, starch and
secondary metabolites. All of these processes are intimately related, as
underlined by M. Stitt (Golm, Germany). He pointed out that the interplay
between different metabolic pathways is not achieved solely through the
regulation of the so-called 'rate-limiting' enzymes. Indeed, a 'global target
analysis' of the main metabolic species ('metabolomics') has revealed several
strategies that modulate metabolic responses. For example, interactions between
the nitrogen and secondary metabolism pathways seem to occur at the level of
specific metabolic precursors, such as glutamine, the levels of which correlate
negatively with levels of the nitrate reductase transcript. A more general
response is also induced by changes in sugar accumulation. These effects of the
metabolites on gene expression are complementary to the effects of nitrate:
they induce the genes for nitrate transporters and nitrate reductase, and
stimulate the post-translational activation of nitrate reductase itself.
Exchange of metabolites between the plastid and the surrounding
cytosol is mediated by a large number of transporters. U.-I. Flügge
(Cologne, Germany) reviewed the nature and physiological properties of
transporters that are located in the inner envelope membrane, and showed
examples of the compensation ability of the different pathways that are
implicated in solute transport across the chloroplast membranes. For example,
the Arabidopsis tpt-1 mutant is defective in the chloroplast triose
phosphate/phosphate translocator (TPT). Nonetheless, the lack of triose
phosphate for use in the synthesis of cytosolic sucrose is almost fully
compensated for both by continuously accelerated starch turnover and by the
export of neutral sugars from the stroma throughout the day. Crosses of
tpt-1 with mutants that are unable to mobilize starch (sex1) or
to synthesize starch (adg1-1) revealed that growth and photosynthesis of
the double mutants was severely impaired only when starch biosynthesis, but not
its mobilization, was affected.
N. Rolland (Grenoble, France) pointed out that, in spite of their
well-known physiological characterization, most of the proteins involved in ion
and metabolite transport across the chloroplast envelope have not been
identified. For this reason, he has developed a new proteomic approach that is
specifically designed to identify the most hydrophobic polypeptides of the
envelope. The use of organic solvents during the first steps of extraction
allows an enrichment for highly lipophilic proteins, and more than 100 proteins
have been identified, including most of the previously known envelope
transporters and more than 50 novel candidates.
Concluding remarks
Photosynthesis can be studied from many different angles. In Les
Diablerets, biophysicists and biochemists showed mountainous profiles with high
peaks, and physiologists shared their admiration for the stress resistance of
pine trees covered with snow. Participants had a chance to share their ideas
and challenge one another about the different perspectives of the field. Given
the success of this interdisciplinary meeting, maybe the next one will extend
the landscape even further to include a view of the ocean, with studies of the
ecological and global aspects of photosynthesis.
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Acknowledgements
We are grateful to the organizers for a lively meeting in a format
that promoted interactions among participants, to EMBO for sponsoring the
meeting and to the Swiss Committee for Molecular Biology. We thank J.-D.
Rochaix for his helpful comments on the manuscript. We apologize to the many
participants whose results we could not present due to lack of space.
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References
Choquet, Y., Wostrikoff, K., Rimbault, B., Zito, F., Girard-Bascou, J., Drapier, D. & Wollman, F.A. ( 2001) Assembly-controlled regulation of chloroplast gene translation. Biochem. Soc. Trans., 29, 421–426. | PubMed | ChemPort |
Diner, B.A. ( 2001) Amino acid residues involved in the coordination and assembly of the manganese cluster of photosystem II. Proton-coupled electron transport of the redox-active tyrosines and its relationship to water oxidation. Biochim. Biophys. Acta, 1503, 147–163. | Article | PubMed | ChemPort |
Nicholls, D.G. & Ferguson, S.J. ( 2002) Bioenergetics, 3rd edn. Academic, New York, USA.
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