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State Transition Kinases and Redox Signal Transduction in Chloroplasts

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Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 41))

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Summary

Both linear (LEF) and cyclic electron flow (CEF) occur in the photosynthetic electron transfer chain and are essential to meet the cellular demands in energy and reducing power. Because photosynthetic organisms are constantly subjected to changes in light and nutrient availability, they need to continuously adapt the relative levels of LEF and CEF. A key parameter in this response is the redox state of the photosynthetic electron transport chain. While the molecular mechanisms underlying the regulation of the CEF/LEF ratio by the chloroplast redox state are still poorly understood, considerable progress has been achieved in elucidating how the redox state of the plastoquinone pool is sensed by the Stt7/STN7 protein kinase associated with the cytochrome b 6 f complex. This kinase induces both a short term and a long term response, both of which tend to restore the redox poise of the plastoquinone pool and thus to optimize the photosynthetic efficiency. The short term response, called “state transitions,” involves the phosphorylation of the light harvesting system of PSII and its reversible migration from photosystem II to photosystem I. The long term response involves a signaling information chain from the chloroplast to the nucleus which ultimately adjusts the stoichiometry between the two photosystems for re-equilibrating their redox state and that of the intervening cytochrome b 6 f complex. The Stt7/STN7 kinase together with the Stl1/STN8 kinase and their associated phosphatases form a central quartet which is part of an extended chloroplast signaling network that is important for the dynamic response of the photosynthetic apparatus, especially under adverse environmental conditions.

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Abbreviations

CEF:

Cyclic electron transfer

Cytb 6 f :

Cytochrome b 6 f complex

DCMU:

3-(3,4-Dichlorophenyl)-1,1-dimethylurea

LEF:

Linear electron flow

LHC:

Light harvesting system

Ndh:

NAD dehydrogenase

PQ:

Plastoquinone

PQH2 :

Plastoquinol

PSI:

Photosystem I

PSII:

Photosystem II

Ptox:

Plastid terminal oxidase

Qo Qp :

The quinone binding site on the electrochemically positive side of the membrane

References

  • Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphoryaltion: new links in the chain. Trends Plant Sci 8:15–19

    Article  CAS  PubMed  Google Scholar 

  • Allorent G, Tokutsu R, Roach T, Peers G, Cardol P, Girard-Bascou J, Seigneurin-Berny D, …, Finazzi G (2013) A dual strategy to cope with high light in Chlamydomonas reinhardtii. Plant Cell 25:545–557

    Google Scholar 

  • Alric J (2014) Redox and ATP control of photosynthetic cyclic electron flow in Chlamydomonas reinhardtii: (II) involvement of the PGR5-PGRL1 pathway under anaerobic conditions. Biochim Biophys Acta 1837:825–834

    Article  CAS  PubMed  Google Scholar 

  • Andersson B, Andersson J (1980) Lateral heterogeneity in the distribution of chlorophyll-protein complexes of the thylakoid membranes of spinach chloroplasts. Biochim Biophys Acta 593:427–440

    Article  CAS  PubMed  Google Scholar 

  • Bassi R, Giacometti GM, Simpson DJ (1988) Changes in the organization of stroma membranes induced by in vivo state 1 – state 2 transition. Biochim Biophys Acta 935:152–165

    Article  CAS  Google Scholar 

  • Bellafiore S, Barneche F, Peltier G, Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–895

    Article  CAS  PubMed  Google Scholar 

  • Bendall DS, Manasse RS (1995) Cyclic photophosphorylation and electron transport. Biochim Biophys Acta 1229:21–28

    Google Scholar 

  • Bennett J (1977) Phosphorylation of chloroplast membrane proteins. Nature 269:344–346

    Article  CAS  Google Scholar 

  • Bollenbach TJ, Schuster G, Stern DB (2004) Cooperation of endo- and exoribonucleases in chloroplast mRNA turnover. Prog Nucleic Acid Res Mol Biol 78:305–337

    Article  CAS  PubMed  Google 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 437:1179–1182

    Google Scholar 

  • Bonaventura C, Myers J (1969) Fluorescence and oxygen evolution from Chlorella pyrenoidosa. Biochim Biophys Acta 189:366–383

    Article  CAS  PubMed  Google Scholar 

  • Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC, Tripodi M, Bassi R, Caffarri S (2008) The occurrence of the PsbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem Photobiol 84:1359–1370

    Google Scholar 

  • Brautigam K, Dietzel L, Kleine T, Stroher E, Wormuth D, Dietz KJ, Radke 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 21:2715–2732

    Google Scholar 

  • Burrows PA, Sazanov LA, Svab Z, Maliga P, Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17:868–876

    Article  CAS  PubMed  PubMed Central  Google 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 106:15979–15984. Epub 12009 Sep 15971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Depège N, Bellafiore S, Rochaix JD (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575

    Article  PubMed  Google Scholar 

  • Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    Article  CAS  PubMed  Google 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 1413:117–129

    Article  CAS  PubMed  Google 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 3:280–285

    Article  CAS  PubMed  PubMed Central  Google 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 274:30987–30994

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Wei X, Li M, Pan X, Chang W, Liu Z (2013) Structure of the catalytic domain of a state transition kinase homolog from Micromonas algae. Protein Cell 4:607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan SS, Yamashita E, Ryan CM, Whitelegge JP, Cramer WA (2011) Conservation of lipid functions in cytochrome bc complexes. J Mol Biol 414:145–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan SS, Yamashitab E, Baniulisc D, Cramer WA (2013a) Quinone-dependent proton transfer pathways in the photosynthetic cytochrome b 6 f complex. Proc Natl Acad Sci USA 110:4297–4303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasan SS, Stofleth JT, Yamashita E, Cramer WA (2013b) Lipid-induced conformational changes within the cytochrome b6f complex of oxygenic photosynthesis. Biochemistry 52:2649–2654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M, Armbruster U, Leister D (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49:511–523

    Article  CAS  PubMed  Google Scholar 

  • Houille-Vernes L, Rappaport F, Wollman FA, Alric J, Johnson X (2011) Plastid terminal oxidase 2 (PTOX2) is the major oxidase involved in chlororespiration in Chlamydomonas. Proc Natl Acad Sci USA 108:20820–20825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010a) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213

    Article  CAS  PubMed  Google Scholar 

  • Iwai M, Yokono M, Inada N, Minagawa J (2010b) Live-cell imaging of photosystem II antenna dissociation during state transitions. Proc Natl Acad Sci USA 107:2337–2342

    Article  CAS  PubMed  Google Scholar 

  • Kargul J, Turkina MV, Nield J, Benson S, Vener AV, Barber J (2005) Light-harvesting complex II protein CP29 binds to photosystem I of Chlamydomonas reinhardtii under state 2 conditions. FEBS J 272:4797–4806

    Article  CAS  PubMed  Google Scholar 

  • Kyle DJ, Staehelin LA, Arntzen CJ (1983) Lateral mobility of the light-harvesting complex in chloroplast membranes controls excitation energy distribution in higher plants. Arch Biochem Biophys 222:527–541

    Article  CAS  PubMed  Google Scholar 

  • Lemeille S, Rochaix JD (2010) State transitions at the crossroad of thylakoid signalling pathways. Photosynth Res 106:33–46

    Article  CAS  PubMed  Google 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:e45

    Article  PubMed  Google Scholar 

  • Lemeille S, Turkina MV, Vener AV, Rochaix JD (2010) Stt7-dependent phosphorylation during state transitions in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 9:1281–1295

    Article  CAS  PubMed  PubMed Central  Google 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 13:2539–2551

    CAS  PubMed  PubMed Central  Google Scholar 

  • Link G (2003) Redox regulation of chloroplast transcription. Antioxid Redox Signal 5:79–87

    Article  CAS  PubMed  Google Scholar 

  • Livingston AK, Kanazawa A, Cruz JA, Kramer DM (2010) Regulation of cyclic electron flow in C(3) plants: differential effects of limiting photosynthesis at ribulose-1,5-bisphosphate carboxylase/oxygenase and glyceraldehyde-3-phosphate dehydrogenase. Plant Cell Environ 33:1779–1788

    Article  CAS  PubMed  Google Scholar 

  • Lucker B, Kramer DM (2013) Regulation of cyclic electron flow in Chlamydomonas reinhardtii under fluctuating carbon availability. Photosynth Res 117:449–459

    Article  CAS  PubMed  Google 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 408:613–615

    Article  CAS  PubMed  Google Scholar 

  • Munekage Y, Hoyo 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 110:361–371

    Article  CAS  PubMed  Google Scholar 

  • Murata N (1969) Control of excitation transfer in photosynthesis. I. Light-induced change of chlorophyll a fluorescence in Porphyridium cruentum. Biochim Biophys Acta 172:242–251

    Article  CAS  PubMed  Google Scholar 

  • Nunes-Nesi A, Sulpice R, Gibon Y, Fernie AR (2008) The enigmatic contribution of mitochondrial function in photosynthesis. J Exp Bot 59:1675–1684

    Article  CAS  PubMed  Google Scholar 

  • Page ML, Hamel PP, Gabilly ST, Zegzouti H, Perea JV, Alonso JM, Ecker JR, …, 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 279:32474–32482. Epub 32004 May 32424

    Google Scholar 

  • Peers G, Truong TB, Ostendorf E, Busch A, Elrad D, Grossman AR, Hippler M, Niyogi KK (2009) An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–521

    Google Scholar 

  • Pesaresi P, Hertle A, Pribil M, Kleine T, Wagner R, Strissel H, Ihnatowicz A, …, Leister D (2009) Arabidopsis STN7 kinase provides a link between short- and long-term photosynthetic acclimation. Plant Cell 21:2402–2423

    Google Scholar 

  • Pribil M, Pesaresi P, Hertle A, Barbato R, Leister D (2010) Role of plastid protein phosphatase TAP38 in LHCII dephosphorylation and thylakoid electron flow. PLoS Biol 8:e1000288

    Article  PubMed  PubMed Central  Google Scholar 

  • Puthiyaveetil S (2011) A mechanism for regulation of chloroplast LHC II kinase by plastoquinol and thioredoxin. FEBS Lett 585:1717–1721

    Article  CAS  PubMed  Google Scholar 

  • Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, …, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proc Natl Acad Sci U S A 105:10061–10066

    Google 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 150:889–903. Epub 2009 Apr 2017

    Google Scholar 

  • Rintamaki E, Martinsuo P, Pursiheimo S, Aro EM (2000) Cooperative regulation of light-harvesting complex II phosphorylation via the plastoquinol and ferredoxin-thioredoxin system in chloroplasts. Proc Natl Acad Sci USA 97:11644–11649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rochaix JD (2007) Role of thylakoid protein kinases in photosynthetic acclimation. FEBS Lett 581:2768–2775. Epub 2007 Apr 2725

    Article  CAS  PubMed  Google Scholar 

  • Rochaix JD (2013) Redox regulation of thylakoid protein kinases and photosynthetic gene expression. Antioxid Redox Signal 18:2184–2201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rochaix JD (2014) Regulation and dynamics of the light-harvesting system. Annu Rev Plant Biol 65:287–309

    Article  CAS  PubMed  Google Scholar 

  • Samol I, Shapiguzov A, Ingelsson B, Fucile G, Crevecoeur M, Vener AV, Rochaix JD, Goldschmidt-Clermont M (2012) Identification of a photosystem II phosphatase involved in light acclimation in Arabidopsis. Plant Cell 24:2596–2609

    Google Scholar 

  • Schuster G, Dewit M, Staehelin LA, Ohad I (1986) Transient inactivation of the thylakoid photosystem II light-harvesting protein kinase system and concomitant changes in intramembrane particle size during photoinhibition of Chlamydomonas reinhardtii. J Cell Biol 103:71–80

    Article  CAS  PubMed  Google Scholar 

  • Shapiguzov A, Ingelsson B, Samol I, Andres C, Kessler F, Rochaix JD, Vener AV, Goldschmidt-Clermont M (2010) The PPH1 phosphatase is specifically involved in LHCII dephosphorylation and state transitions in Arabidopsis. Proc Natl Acad Sci U S A 107:4782–4787

    Google Scholar 

  • Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95:9705–9709

    Article  CAS  PubMed  PubMed Central  Google 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 17:2580–2586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snyders S, Kohorn BD (1999) TAKs, thylakoid membrane protein kinases associated with energy transduction. J Biol Chem 274:9137–9140

    Article  CAS  PubMed  Google Scholar 

  • Stroebel D, Choquet Y, Popot JL, Picot D (2003) An atypical haem in the cytochrome b(6)f complex. Nature 426:413–418

    Article  CAS  PubMed  Google 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 103:477–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi H, Clowez S, Wollman FA, Vallon O, Rappaport F (2013) Cyclic electron flow is redox-controlled but independent of state transition. Nat Commun 4:1954

    PubMed  PubMed Central  Google Scholar 

  • Terashima M, Petroutsos D, Hudig M, Tolstygina I, Trompelt K, Gabelein P, Fufezan C, …, Hippler M (2012) Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc Natl Acad Sci U S A 109:17717–17722

    Google Scholar 

  • Tikkanen M, Grieco M, Kangasjärvi S, Aro EM (2007) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Biochim Biophys Acta 152:723–735

    Google 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 280:33679–33686

    Article  CAS  PubMed  Google 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 88:8262–8266

    Article  CAS  PubMed  PubMed Central  Google 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 94:1585–1590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Gau H, Slade WO, Juergens M, Li P, Hicks LM (2014) The global phosphoproteome of Chlamydomonas reinhardtii reveals complex organellar phosphorylation in the flagella and thylakoid membrane. Mol Cell Prot 13: 2337–2357. In press, published on 10 June 2014

    Google Scholar 

  • Widger WR, Cramer WA, Herrmann RG, Trebst A (1984) Sequence homology and structural similarity between cytochrome b of mitochondrial complex III and the chloroplast b6-f complex: position of the cytochrome b hemes in the membrane. Proc Natl Acad Sci USA 81:674–678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wientjes E, Drop B, Kouril R, Boekema EJ, Croce R (2013) During state 1 to state 2 transition in Arabidopsis thaliana, the photosystem II supercomplex gets phosphorylated but does not disassemble. J Biol Chem 288:32821–32826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willig A, Shapiguzov A, Goldschmidt-Clermont M, Rochaix JD (2011) The phosphorylation status of the chloroplast protein kinase STN7 of Arabidopsis affects its turnover. Plant Physiol 157:2102–2107

    Article  CAS  PubMed  PubMed Central  Google 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 18:2961–2969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

I thank Nicolas Roggli for preparing the figures. The work in the author’s laboratory was supported by grant 31003A_133089/1 from the Swiss National Foundation.

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Correspondence to Jean-David Rochaix .

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Rochaix, JD. (2016). State Transition Kinases and Redox Signal Transduction in Chloroplasts. In: Cramer, W., Kallas, T. (eds) Cytochrome Complexes: Evolution, Structures, Energy Transduction, and Signaling. Advances in Photosynthesis and Respiration, vol 41. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-7481-9_24

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