State transitions at the crossroad of thylakoid signalling pathways
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Abstract
In order to maintain optimal photosynthetic activity under a changing light environment, plants and algae need to balance the absorbed light excitation energy between photosystem I and photosystem II through processes called state transitions. Variable light conditions lead to changes in the redox state of the plastoquinone pool which are sensed by a protein kinase closely associated with the cytochrome b 6 f complex. Preferential excitation of photosystem II leads to the activation of the kinase which phosphorylates the light-harvesting system (LHCII), a process which is subsequently followed by the release of LHCII from photosystem II and its migration to photosystem I. The process is reversible as dephosphorylation of LHCII on preferential excitation of photosystem I is followed by the return of LHCII to photosystem II. State transitions involve a considerable remodelling of the thylakoid membranes, and in the case of Chlamydomonas, they allow the cells to switch between linear and cyclic electron flow. In this alga, a major function of state transitions is to adjust the ATP level to cellular demands. Recent studies have identified the thylakoid protein kinase Stt7/STN7 as a key component of the signalling pathways of state transitions and long-term acclimation of the photosynthetic apparatus. In this article, we present a review on recent developments in the area of state transitions.
Keywords
Photosynthesis State transitions LHCII kinase Arabidopsis ChlamydomonasNotes
Acknowledgements
We thank Michel Goldschmidt-Clermont for his helpful comments. Research in the authors’ laboratory was supported by a grant from the Swiss National Foundation (3100AO-117712) to J.D.R.
Supplementary material
References
- Adam Z, Clarke AK (2002) Cutting edge of chloroplast proteolysis. Trends Plant Sci 7:451–456CrossRefPubMedGoogle Scholar
- Albertsson PA (2001) A quantitative model of the domain structure of the photosynthetic membrane. Trends Plant Sci 6:349–354CrossRefPubMedGoogle Scholar
- Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335CrossRefPubMedGoogle Scholar
- Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19CrossRefPubMedGoogle Scholar
- Allen JF, Pfannschmidt T (2000) Balancing the two photosystems: photosynthetic electron transfer governs transcription of reaction centre genes in chloroplasts. Philos Trans R Soc Lond B Biol Sci 355:1351–1359CrossRefPubMedGoogle Scholar
- Allen JF, Bennett J, Steinback KE, Arntzen CJ (1981) Chloroplast protein phosphorylation couples plastoquinone redox state to distribution of excitation energy between photosystems. Nature 291:25–29CrossRefGoogle Scholar
- Andersson B, Andersson J (1980) Lateral heterogeneity in the distribution of chlorophyll–protein complexes of the thylakoid membranes of spinach chloroplasts. Biochem Biophys Acta 593:427–440CrossRefPubMedGoogle Scholar
- Barber J (1982) The control of membrane organization by electrostatic forces. Biosci Rep 2:1–13CrossRefPubMedGoogle Scholar
- Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895CrossRefPubMedGoogle Scholar
- Bennett J (1977) Phosphorylation of chloroplast membrane proteins. Nature 269:344–346CrossRefGoogle Scholar
- Bennett J (1979) Chloroplast phosphoproteins. Phosphorylation of polypeptides of the light-harvesting chlorophyll protein complex. Eur J Biochem 99:133–137CrossRefPubMedGoogle Scholar
- Bennett J (1980) Chloroplast phosphoproteins. Evidence for a thylakoid-bound phosphoprotein phosphatase. Eur J Biochem 104:85–89CrossRefPubMedGoogle Scholar
- Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635CrossRefPubMedGoogle Scholar
- Bollenbach TJ, Schuster G, Stern DB (2004) Cooperation of endo- and exoribonucleases in chloroplast mRNA turnover. Prog Nucleic Acid Res Mol Biol 78:305–337CrossRefPubMedGoogle Scholar
- Bonardi V, Pesaresi P, Becker T, Schleiff E, Wagner R, Pfannschmidt T, Jahns P, Leister D (2005) Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases. Nature 437:1179–1182CrossRefPubMedGoogle Scholar
- Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383CrossRefPubMedGoogle Scholar
- Brautigam K, Dietzel L, Kleine T, Stroher E, Wormuth D, Dietz KJ, Radke D, Wirtz M, Hell R, Dormann P, Nunes-Nesi A, Schauer N, Fernie AR, Oliver SN, Geigenberger P, Leister D, Pfannschmidt T (2009) Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis. Plant Cell 21:2715–2732CrossRefPubMedGoogle Scholar
- Breyton C (2000) Conformational changes in the cytochrome b6f complex induced by inhibitor binding. J Biol Chem 275:13195–13201CrossRefPubMedGoogle Scholar
- Bulté L, Gans P, Rebeille F, Wollman FA (1990) ATP control on state transitions in Chlamydomonas. Biochim Biophys Acta 1020:72–80CrossRefGoogle Scholar
- Cardol P, Gloire G, Havaux M, Remacle C, Matagne R, Franck F (2003) Photosynthesis and state transitions in mitochondrial mutants of Chlamydomonas reinhardtii affected in respiration. Plant Physiol 133:2010–2021CrossRefPubMedGoogle Scholar
- Cardol P, Alrich J, Girard-Bascou J, Franck F, Wollman FA, Finazzi G (2009) Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc Natl Acad Sci USA 106:15979–15984CrossRefPubMedGoogle Scholar
- Chuartzman SG, Nevo R, Shimoni E, Charuvi D, Kiss V, Ohad I, Brumfeld V, Reich Z (2008) Thylakoid membrane remodeling during state transitions in Arabidopsis. Plant Cell 20:1029–1039CrossRefPubMedGoogle Scholar
- Cleland RE, Bendall DS (1992) Photosystem I cyclic electron transport: measurement of ferredoxin-plastoquinone reductase activity. Photosynth Res 34:409–418CrossRefGoogle Scholar
- Coughlan SJ, Hind G (1986) Purification and characterization of a membrane-bound protein kinase from spinach thylakoids. J Biol Chem 261:11378–11385PubMedGoogle Scholar
- Coughlan S, Hind G (1987) Phosphorylation of thylakoid proteins by a purified kinase. J Biol Chem 262:8402–8408PubMedGoogle Scholar
- DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schunemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285CrossRefPubMedGoogle Scholar
- de Lacroix de Lavalette A, Finazzi G, Zito F (2008) b6f-Associated chlorophyll: structural and dynamic contribution to the different cytochrome functions. Biochemistry 47:5259–5265CrossRefPubMedGoogle Scholar
- Delosme R, Olive J, Wollman FA (1996) Changes in light energy distribution upon state transitions: an in vivo photoacoustic study of the wild type and photosynthesis mutants from Chlamydomonas reinhardtii. Biochim Biophys Acta 1273:150–158CrossRefGoogle Scholar
- Depège N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575CrossRefPubMedGoogle Scholar
- Dietzel L, Bräutigam K, Pfannschmidt T (2008) Photosynthetic acclimation: state transitions and adjustment of photosystem stoichiometry–functional relationships between short-term and long-term light quality acclimation in plants. FEBS J 275:1080–1088CrossRefPubMedGoogle Scholar
- Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129CrossRefPubMedGoogle Scholar
- Finazzi G, Zito F, Barbagallo RP, Wollman FA (2001) Contrasted effects of inhibitors of cytochrome b6f complex on state transitions in Chlamydomonas reinhardtii: the role of Qo site occupancy in LHCII kinase activation. J Biol Chem 276:9770–97743CrossRefPubMedGoogle Scholar
- Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix JD, Zito F, Forti G (2002) Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep 3:280–285CrossRefPubMedGoogle Scholar
- Fleischmann MM, Ravanel S, Delosme R, Olive J, Zito F, Wollman FA, Rochaix JD (1999) Isolation and characterization of photoautotrophic mutants of Chlamydomonas reinhardtii deficient in state transition. J Biol Chem 274:30987–30994CrossRefPubMedGoogle Scholar
- Frenkel M, Bellafiore S, Rochaix JD, Jansson S (2007) Hierarchy amongst photosynthetic acclimation responses for plant fitness. Physiol Plantarum 129:455–459CrossRefGoogle Scholar
- Fristedt R, Willig A, Granath P, Crèvecoeur M, Rochaix JD, Vener A (2009) Phosphorylation of photosystem II controls functional macroscopic folding of plant photosynthetic membranes. Plant Cell 21:3950–3964CrossRefPubMedGoogle Scholar
- Fulgosi H, Vener AV, Altschmied L, Herrmann RG, Andersson B (1998) A novel multi-functional chloroplast protein: identification of a 40 kDa immunophilin-like protein located in the thylakoid lumen. EMBO J 17:1577–1587CrossRefPubMedGoogle Scholar
- Gal A, Hauska G, Herrmann RG, Ohad I (1990) Interaction between light-harvesting chlorophyll-a/b protein (LHCII)kinase and cytochrome b 6 f complex. In vitro control of kinase activity. J Biol Chem 265:17749–19742Google Scholar
- Hamel P, Olive J, Pierre Y, Wollman FA, de Vitry C (2000) A new subunit of cytochrome b6f complex undergoes reversible phosphorylation upon state transition. J Biol Chem 275:17072–17079CrossRefPubMedGoogle Scholar
- Hammer MF, Markwell J, Sarath G (1997) Purification of a protein phosphatase from chloroplast stroma capable of dephosphorylating the light-harvesting complex-II. Plant Physiol 113:227–233CrossRefPubMedGoogle Scholar
- Helm M, Luck C, Prestele J, Hierl G, Huesgen PF, Frohlich T, Arnold GJ, Adamska I, Gorg A, Lottspeich F, Gietl C (2007) Dual specificities of the glyoxysomal/peroxisomal processing protease Deg15 in higher plants. Proc Natl Acad Sci USA 104:11501–11506CrossRefPubMedGoogle Scholar
- Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43:8281–8289CrossRefPubMedGoogle Scholar
- Horton P, Black MT (1980) Activation of adenosine 5′ triphosphate-induced quenching of chlorophyll fluorescence by reduced plastoquinone. FEBS Lett 119:141–145CrossRefGoogle Scholar
- Hou CH, Rintamäki E, Aro EM (2003) Ascorbate-mediated LHCII protein phosphorylation—LHCII kinase regulation in light and in darkness. Biochemistry 42:5828–5836CrossRefPubMedGoogle Scholar
- Huesgen PF, Schuhmann H, Adamska I (2009) Deg/HtrA proteases as components of a network for photosystem II quality control in chloroplasts and cyanobacteria. Res Microbiol 160:726–732CrossRefPubMedGoogle Scholar
- Iwai M, Takahashi Y, Minagawa J (2008) Molecular remodeling of photosystem II during state transitions in Chlamydomonas reinhardtii. Plant Cell 20:2177–2189CrossRefPubMedGoogle Scholar
- Joliot P, Joliot A (2006) Cyclic electron flow in C3 plants. Biochim Biophys Acta 1757:362–368CrossRefPubMedGoogle Scholar
- Kieleczawa J, Coughlan SJ, Hind G (1992) Isolation and characterization of an alkaline phosphatase from pea thylakoids. Plant Physiol 99:1029–1036CrossRefPubMedGoogle Scholar
- Kouril R, Zygadlo A, Arteni AA, DeWit CD, Delkker JP, Jensen PE, Scheller HV, Boekema EJ (2005) Structural characterization of a complex of photosystem I and light-harvesting complex II of Arabidopsis thaliana. Biochemistry 44:10935–10940CrossRefPubMedGoogle Scholar
- Kruse O, Nixon PJ, Schmid GH, Mullineaux CW (1999) Isolation of state transition mutants of Chlamydomonas reinhardtii by fluorescence video imaging. Photosynth Res 61:43–51CrossRefGoogle Scholar
- Lemeille S, Willig A, Depège-Fargeix N, Delessert C, Bassi R, Rochaix JD (2009) Analysis of the chloroplast protein kinase Stt7 during state transitions. PLoS Biol 7:e45CrossRefPubMedGoogle Scholar
- Lemeille S, Turkina M, Vener AV, Rochaix JD (2010) Stt7-dependent phosphorylation during state transitions in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics. doi: 10.1074/mcp.M000020-MCP201 PubMedGoogle Scholar
- Lennartz K, Plucken H, Seidler A, Westhoff P, Bechtold N, Meierhoff K (2001) HCF164 encodes a thioredoxin-like protein involved in the biogenesis of the cytochrome b(6)f complex in Arabidopsis. Plant Cell 13:2539–2551CrossRefPubMedGoogle Scholar
- Link G (2003) Redox regulation of chloroplast transcription. Antioxid Redox Signal 5:79–87CrossRefPubMedGoogle Scholar
- Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408:613–615CrossRefPubMedGoogle Scholar
- Melis A, Murakami A, Nemson JA, Aizawa K, Ohki K, Fujita Y (1996) Chromatic regulation in Chlamydomonas reinhardtii alters photosystem stoichiometry and improves the quantum efficiency of photosynthesis. Photosynth Res 47:253–265CrossRefGoogle Scholar
- Moss DA, Bendall DS (1984) Cyclic electron transport in chloroplasts: the Q-cycle and the site of action of anthocyanin. Biochim Biophys Acta 767:389–395CrossRefGoogle Scholar
- Motohashi K, Hisabori T (2006) HCF164 receives reducing equivalents from stromal thioredoxin across the thylakoid membrane and mediates reduction of target proteins in the thylakoid lumen. J Biol Chem 281:35039–35047CrossRefPubMedGoogle Scholar
- Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371CrossRefPubMedGoogle Scholar
- Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251CrossRefPubMedGoogle Scholar
- Page ML, Hamel PP, Gabilly ST, Zegzouti H, Perea JV, Alonso JM, Ecker JR, Theg SM, Christensen SK, Merchant S (2004) A homolog of prokaryotic thiol disulfide transporter CcdA is required for the assembly of the cytochrome b6f complex in Arabidopsis chloroplasts. J Biol Chem 279:32474–32482CrossRefPubMedGoogle Scholar
- Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, Bonardi V, Scharfenberg M, Schneider A, Pfannschmidt T, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423CrossRefPubMedGoogle Scholar
- Pfannschmidt T (2003) Chloroplast redox signals: how photosynthesis controls its own genes. Trends Plant Sci 8:33–41CrossRefPubMedGoogle Scholar
- Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation an thylakoid electron flow. PLoS Biol 8:e 1000288CrossRefGoogle Scholar
- Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc Natl Acad Sci USA 105:10061–10066CrossRefPubMedGoogle Scholar
- Reiland S, Messerli G, Baerenfaller K, Gerrits B, Endler A, Grossmann J, Gruissem W, Baginsky S (2009) Large-scale Arabidopsis phosphoproteome profiling reveals novel chloroplast kinase substrates and phosphorylation networks. Plant Physiol 150:889–903CrossRefPubMedGoogle Scholar
- Rintamaki E, Salonen M, Suoranta UM, Carlberg I, Andersson B, Aro EM (1997) Phosphorylation of light-harvesting complex II and photosystem II core proteins shows different irradiance-dependent regulation in vivo. Application of phosphothreonine antibodies to analysis of thylakoid phosphoproteins. J Biol Chem 272:30476–30482CrossRefPubMedGoogle Scholar
- Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775CrossRefPubMedGoogle Scholar
- Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phophatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci USA. doi: 10.1073/pnas.0913810107 PubMedGoogle Scholar
- Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217CrossRefPubMedGoogle Scholar
- Shimoni E, Rav-Hon O, Ohad I, Brumfeld V, Reich Z (2005) Three-dimensional organization of higher-plant chloroplast thylakoid membranes revealed by electron tomography. Plant Cell 17:2580–2586CrossRefPubMedGoogle Scholar
- Silverstein T, Cheng L, Allen JF (1993) Chloroplast thylakoid protein phosphatase reactions are redox-independent and kinetically heterogeneous. FEBS Lett 334:101–105CrossRefPubMedGoogle Scholar
- Snyders S, Kohorn BD (1999) TAKs, thylakoid membrane protein kinases associated with energy transduction. J Biol Chem 274:9137–9140CrossRefPubMedGoogle Scholar
- Snyders S, Kohorn BD (2001) Disruption of thylakoid-associated kinase 1 leads to alteration of light harvesting in Arabidopsis. J Biol Chem 276:32169–32176CrossRefPubMedGoogle Scholar
- Sokolenko A, Fulgosi H, Gal A, Altschmied L, Ohad I, Herrmann RG (1995) The 64 kDa polypeptide of spinach may not be the LHCII kinase, but a lumen-located polyphenol oxidase. FEBS Lett 371:176–180CrossRefPubMedGoogle Scholar
- Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418CrossRefPubMedGoogle Scholar
- Takahashi H, Iwai M, Takahashi Y, Minagawa J (2006) Identification of the mobile light-harvesting complex II polypeptides for state transitions in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 103:477–482CrossRefPubMedGoogle Scholar
- Tikkanen M, Piippo M, Suorsa M, Sirpio S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y, Aro EM (2006) State transitions revisited—a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62:779–79371CrossRefPubMedGoogle Scholar
- Tikkanen M, Nurmi M, Suorsa M, Danielsson R, Mamedov F, Styring S, Aro EM (2008) Phosphorylation-dependent regulation of excitation energy distribution between the two photosystems in higher plants. Biochim Biophys Acta 1777:425–432CrossRefPubMedGoogle Scholar
- Tokutsu R, Iwai M, Minagawa J (2009) CP29, a monomeric light-harvesting complex II protein, is essential for state transitions in Chlamydomonas reinhardtii. J Biol Chem 284:7777–7782CrossRefPubMedGoogle Scholar
- Turkina MV, Kargul J, Blanco-Rivero A, Villarejo A, Barber J, Vener AV (2006) Environmentally modulated phosphoproteome of photosynthetic membranes in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 5:1412–1425 [Epub 2006 May 2]CrossRefPubMedGoogle Scholar
- Vainonen JP, Hansson M, Vener AV (2005) STN8 protein kinase in Arabidopsis thaliana is specific in phosphorylation of photosystem II core proteins. J Biol Chem 280:33679–33686CrossRefPubMedGoogle Scholar
- Vallon O, Bulte L, Dainese P, Olive J, Bassi R, Wollman FA (1991) Lateral redistribution of cytochrome b6/f complexes along thylakoid membranes upon state transitions. Proc Natl Acad Sci USA 88:8262–8266CrossRefPubMedGoogle Scholar
- Vener AV, van Kan PJ, Rich PR, Ohad II, Andersson B (1997) Plastoquinol at the quinol oxidation site of reduced cytochrome bf mediates signal transduction between light and protein phosphorylation: thylakoid protein kinase deactivation by a single-turnover flash. Proc Natl Acad Sci USA 94:1585–1590CrossRefPubMedGoogle Scholar
- Vener AV, Rokka A, Fulgosi H, Andersson B, Herrmann RG (1999) A cyclophilin-regulated PP2A-like protein phosphatase in thylakoid membranes of plant chloroplasts. Biochemistry 38:14955–14965 [erratum appears in Biochemistry (2000) 39:2130]CrossRefPubMedGoogle Scholar
- Wagner R, Dietzel L, Bräutigam K, Fischer W, Pfannschmidt T (2008) The long-term response to fluctuating light quality is an important and distinct light acclimation mechanism that supports survival of Arabidopsis thaliana under low light conditions. Planta 228:573–587CrossRefPubMedGoogle Scholar
- Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20:3623–3630CrossRefPubMedGoogle Scholar
- Wollman FA, Delepelaire P (1984) Correlations between fluorescence and phosphorylation changes in thylakoid membranes of Chlamydomonas reinhardtii in vivo: a kinetic analysis. J Cell Biol 98:1–7CrossRefPubMedGoogle Scholar
- Wollman FA, Lemaire C (1988) Studies on kinase-controlled state transitions in photosystem II and b6f mutants from Chlamydomonas reinhardtii which lack quinone-binding proteins. Biochim Biophys Acta 933:85–94CrossRefGoogle Scholar
- Zhang S, Scheller HV (2004) Light-harvesting complex II binds to several small subunits of photosystem I. J Biol Chem 279:3180–3187CrossRefPubMedGoogle Scholar
- Zhang Z, Huang L, Shulmeister VM, Chi YI, Kim KK, Hung LW, Crofts AR, Berry EA, Kim SH (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392:677–684CrossRefPubMedGoogle Scholar
- Zito F, Finazzi G, Delosme R, Nitschke W, Picot D, Wollman FA (1999) The Qo site of cytochrome b6f complexes controls the activation of the LHCII kinase. EMBO J 18:2961–2966CrossRefPubMedGoogle Scholar
- Zito F, Vinh J, Popot JL, Finazzi G (2002) Chimeric fusions of subunit IV and PetL in the b6f complex of Chlamydomonas reinhardtii: structural implications and consequences on state transitions. J Biol Chem 277:12446–12455CrossRefPubMedGoogle Scholar