1932

Abstract

The light reactions in photosynthesis drive both linear and cyclic electron transport around photosystem I (PSI). Linear electron transport generates both ATP and NADPH, whereas PSI cyclic electron transport produces ATP without producing NADPH. PSI cyclic electron transport is thought to be essential for balancing the ATP/NADPH production ratio and for protecting both photosystems from damage caused by stromal overreduction. Two distinct pathways of cyclic electron transport have been proposed in angiosperms: a major pathway that depends on the PROTON GRADIENT REGULATION 5 (PGR5) and PGR5-LIKE PHOTOSYNTHETIC PHENOTYPE 1 (PGRL1) proteins, which are the target site of antimycin A, and a minor pathway mediated by the chloroplast NADH dehydrogenase–like (NDH) complex. Recently, the regulation of PSI cyclic electron transport has been recognized as essential for photosynthesis and plant growth. In this review, we summarize the possible functions and importance of the two pathways of PSI cyclic electron transport.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-043015-112002
2016-04-29
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/arplant/67/1/annurev-arplant-043015-112002.html?itemId=/content/journals/10.1146/annurev-arplant-043015-112002&mimeType=html&fmt=ahah

Literature Cited

  1. Alboresi A, Gerotto C, Giacometti GM, Bassi R, Morosinotto T. 1.  2010. Physcomitrella patens mutants affected on heat dissipation clarify the evolution of photoprotection mechanisms upon land colonization. PNAS 107:11128–33 [Google Scholar]
  2. Allahverdiyeva Y, Suorsa M, Tikkanen M, Aro EM. 2.  2015. Photoprotection of photosystems in fluctuating light intensities. J. Exp. Bot. 66:2427–36 [Google Scholar]
  3. Allen JF. 3.  2003. Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci. 8:15–19 [Google Scholar]
  4. Amthor JS. 4.  2010. From sunlight to phytomass: on the potential efficiency of converting solar radiation to phyto-energy. New Phytol. 188:939–59 [Google Scholar]
  5. Arnon DI, Allen MB, Whatley FR. 5.  1954. Photosynthesis by isolated chloroplasts. Nature 174:394–96 [Google Scholar]
  6. Arnon DI, Allen MB, Whatley FR. 6.  1954. Photosynthesis by isolated chloroplasts. II. Photosynthetic phosphorylation, the conversion of light into phosphate bound energy. J. Am. Chem. Soc. 76:6324–29 [Google Scholar]
  7. Asada K. 7.  1999. The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:601–39 [Google Scholar]
  8. Asada K. 8.  2000. The water-water cycle as alternative photon and electron sinks. Philos. Trans. R. Soc. Lond. B 355:1419–31 [Google Scholar]
  9. Asada K, Heber U, Schreiber U. 9.  1993. Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as detected in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant Cell Physiol. 34:39–50 [Google Scholar]
  10. Avenson TJ, Cruz JA, Kanazawa A, Kramer DM. 10.  2005. Regulating the proton budget of higher plant photosynthesis. PNAS 102:9709–13 [Google Scholar]
  11. Avenson TJ, Cruz JA, Kramer DM. 11.  2004. Modulation of energy-dependent quenching of excitons in antennae of higher plants. PNAS 101:5530–35 [Google Scholar]
  12. Bailey S, Walters RG, Jansson S, Horton P. 12.  2001. Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794–801 [Google Scholar]
  13. Bailleul B, Cardol P, Breyton C, Finazzi G. 13.  2010. Electrochromism: a useful probe to study algal photosynthesis. Photosynth. Res. 106:179–89 [Google Scholar]
  14. Baker NR, Harbinson J, Kramer DM. 14.  2007. Determining the limitations and regulation of photosynthetic energy transduction in leaves. Plant Cell Environ. 30:1107–25 [Google Scholar]
  15. Barth C, Krause GH. 15.  2002. Study of tobacco transformants to assess the role of chloroplastic NAD(P)H dehydrogenase in photoprotection of photosystems I and II. Planta 216:273–79 [Google Scholar]
  16. Battchikova N, Eisenhut M, Aro EM. 16.  2011. Cyanobacterial NDH-1 complexes: novel insights and remaining puzzles. Biochim. Biophys. Acta 1807:935–44 [Google Scholar]
  17. Bellafiore S, Barneche F, Peltier G, Rochaix JD. 17.  2005. State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433:892–95 [Google Scholar]
  18. Bendall DS. 18.  1982. Photosynthetic cytochromes of oxygenic organisms.. Biochim. Biophys. Acta 683:119–57 [Google Scholar]
  19. Bendall DS, Manasse RS. 19.  1995. Cyclic photophosphorylation and electron transport. Biochim. Biophys. Acta 1229:23–38 [Google Scholar]
  20. Bonente G, Passarini F, Cazzaniga S, Mancone C, Buia MC. 20.  et al. 2008. The occurrence of the PsbS gene product in Chlamydomonas reinhardtii and in other photosynthetic organisms and its correlation with energy quenching. Photochem. Photobiol. 84:1359–70 [Google Scholar]
  21. Bukhov NG, Wiese C, Neimanis S, Heber U. 21.  1999. Heat sensitivity of chloroplasts and leaves: leakage of protons from thylakoids and reversible activation of cyclic electron transport. Photosynth. Res. 59:81–93 [Google Scholar]
  22. Burrows PA, Sazanov A, Svab Z, Maliga P, Nixon PJ. 22.  1998. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes.. EMBO J. 17:868–76 [Google Scholar]
  23. Carol P, Stevenson D, Bisanz C, Breitenbach J, Sandmann G. 23.  et al. 1999. Mutations in the Arabidopsis gene IMMUTANS cause a variegated phenotype by inactivating a chloroplast terminal oxidase associated with phytoene desaturation.. Plant Cell 11:57–68 [Google Scholar]
  24. Chang CC, Lin HC, Lin IP, Chow TY, Chen HH. 24.  et al. 2006. The chloroplast genome of Phalaenopsis aphrodite (Orchidaceae): comparative analysis of evolutionary rate with that of grasses and its phylogenetic implications. Mol. Biol. Evol. 23:279–91 [Google Scholar]
  25. Clarke JE, Johnson GN. 25.  2001. In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212:808–16 [Google Scholar]
  26. DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D. 26.  et al. 2008. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–85 [Google Scholar]
  27. Darie CC, De Pascalis L, Mutschler B, Haehnel W. 27.  2006. Studies of the Ndh complex and photosystem II from mesophyll and bundle sheath chloroplasts of the C4-type plant Zea mays. J. Plant Physiol. 163:800–8 [Google Scholar]
  28. Dunham KR, Selman BR. 28.  1981. Regulation of spinach chloroplast coupling factor 1 ATPase activity. J. Biol. Chem. 256:212–18 [Google Scholar]
  29. Endo T, Kawase D, Sato F. 29.  2005. Stromal over-reduction by high-light stress as measured by decreases in P700 oxidation by far-red light and its physiological relevance. Plant Cell Physiol. 46:775–81 [Google Scholar]
  30. Endo T, Shikanai T, Takabayashi A, Asada K, Sato F. 30.  1999. The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett. 457:5–8 [Google Scholar]
  31. Falkowski PG, Fujita Y, Ley A, Mauzerall D. 31.  1986. Evidence for cyclic electron flow around photosystem II in Chlorella pyrenoidosa. Plant Physiol. 81:310–12 [Google Scholar]
  32. Fan X, Zhang J, Li W, Peng L. 32.  2015. The NdhV subunit is required to stabilize the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant J. 82:221–31 [Google Scholar]
  33. Finazzi G, Rappaport F, Furia A, Fleischmann M, Rochaix JD. 33.  et al. 2002. Involvement of state transitions in the switch between linear and cyclic electron flow in Chlamydomonas reinhardtii. EMBO Rep. 3:280–85 [Google Scholar]
  34. Fisher N, Kramer DM. 34.  2014. Non-photochemical reduction of thylakoid photosynthetic redox carriers in vitro: relevance to cyclic electron flow around photosystem I?. Biochim. Biophys. Acta 1837:1944–54 [Google Scholar]
  35. Foyer CH, Furbank R, Harbinson J, Horton P. 35.  1990. The mechanisms contributing to photosynthetic control of electron-transport by carbon assimilation in leaves. Photosynth. Res. 25:83–100 [Google Scholar]
  36. Foyer CH, Neukermans J, Queval G, Noctor G, Harbinson J. 36.  2012. Photosynthetic control of electron transport and the regulation of gene expression. J. Exp. Bot. 63:1637–61 [Google Scholar]
  37. Furbank RT, Hatch MD. 37.  1987. Mechanism of C4 photosynthesis. The size and composition of the inorganic carbon pool in the bundle sheath cells. Plant Physiol. 85:958–64 [Google Scholar]
  38. Genty B, Harbinson J, Baker NR. 38.  1990. Relative quantum efficiencies of the 2 photosystems of leaves in photorespiratory and nonphotorespiratory conditions. Plant Physiol. Biochem. 28:1–10 [Google Scholar]
  39. Golding AJ, Finazzi G, Johnson GN. 39.  2004. Reduction of the thylakoid electron transport chain by stromal reductants: evidence for activation of cyclic electron transport upon dark adaptation or under drought. Planta 220:356–63 [Google Scholar]
  40. 40. Govindjee 2004. Chlorophyll a fluorescence: a bit of basics and history. Chlorophyll a Fluorescence: A Signature of Photosynthesis GC Papageorgiou, Govindjee 1–42 Dordrecht, Neth: Kluwer [Google Scholar]
  41. Harbinson J, Foyer CH. 41.  1991. Relationships between the efficiencies of PS I and II and stromal redox state in CO2-free air: evidence for cyclic electron flow in vivo. Plant Physiol. 97:41–49 [Google Scholar]
  42. Havaux M. 42.  1996. Short-term responses of photosystem I to heat stress. Photosynth. Res. 47:85–97 [Google Scholar]
  43. Hertle AP, Blunder T, Wunder T, Pesaresi P, Pribil M. 43.  et al. 2013. PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol. Cell 49:511–23 [Google Scholar]
  44. Hisabori T, Sunamura E, Kim Y, Konno H. 44.  2013. The chloroplast ATP synthase features the characteristic redox regulation machinery. Antioxid. Redox Signal. 19:1846–54 [Google Scholar]
  45. Horváth EM, Peter SO, Joet T, Rumeau D, Cournac L. 45.  et al. 2000. Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiol. 123:1337–49 [Google Scholar]
  46. Ifuku K, Endo T, Shikanai T, Aro EM. 46.  2011. Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant Cell Physiol. 52:1560–68 [Google Scholar]
  47. Ishikawa N, Endo T, Sato F. 47.  2008. Electron transport activities of Arabidopsis thaliana mutants with impaired chloroplastic NAD(P)H dehydrogenase. J. Plant Res. 121:521–26 [Google Scholar]
  48. Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y. 48.  et al. 2010. Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–13 [Google Scholar]
  49. Joët T, Cournac L, Horvath EM, Medgyesy P, Peltier G. 49.  2001. Increased sensitivity of photosynthesis to antimycin A induced by inactivation of the chloroplast ndhB gene. Evidence for a participation of the NADH-dehydrogenase complex to cyclic electron flow around photosystem I. Plant Physiol. 125:1919–29 [Google Scholar]
  50. Joët T, Cournac L, Peltier G, Havaux M. 50.  2002. Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiol. 128:760–69 [Google Scholar]
  51. Johnson EA, McCarty RE. 51.  2002. The carboxyl terminus of the ε subunit of the chloroplast ATP synthase is exposed during illumination. Biochemistry 41:2446–51 [Google Scholar]
  52. Johnson X, Steinbeck J, Dent RM, Takahashi H, Richaud P. 52.  et al. 2014. Proton gradient regulation 5-mediated cyclic electron flow under ATP- or redox-limited conditions: a study of ΔATPase pgr5 and ΔrbcL pgr5 mutants in the green alga Chlamydomonas reinhardtii. Plant Physiol. 165:438–52 [Google Scholar]
  53. Joliot P, Joliot A. 53.  2002. Cyclic electron transfer in plant leaf. PNAS 99:10209–14 [Google Scholar]
  54. Joliot P, Joliot A. 54.  2005. Quantification of cyclic and linear flows in plants. PNAS 102:4913–18 [Google Scholar]
  55. Josse EM, Simkin AJ, Gaffe J, Labore AM, Kuntz M. 55.  et al. 2000. A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol. 123:1427–36 [Google Scholar]
  56. Junge W, Witt HT. 56.  1968. On the ion transport system in photosynthesis: investigations on a molecular level. Z. Naturforsch. B 23:244–54 [Google Scholar]
  57. Kallas T. 57.  2012. Cytochrome b6f complex at the heart of energy transduction and redox signaling. Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation JJ Eaton-Rye, BC Tripathy, TD Sharkey 501–60 Dordrecht, Neth: Springer [Google Scholar]
  58. Kiss AZ, Ruban AV, Horton P. 58.  2008. The PsbS protein controls the organisation of the photosystem II antenna in higher plant thylakoid membranes. J. Biol. Chem 15:3972–78 [Google Scholar]
  59. Kofer W, Koop HU, Wanner G, Steinmüller K. 59.  1998. Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycol-mediated plastome transformation. Mol. Gen. Genet. 258:166–73 [Google Scholar]
  60. Kono M, Noguchi K, Terashima I. 60.  2014. Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant Cell Physiol. 55:990–1004 [Google Scholar]
  61. Kou J, Takahashi S, Oguchi R, Fan DY, Badger M, Chow WS. 61.  2013. Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO2-enriched air and other varied conditions. Funct. Plant Biol. 40:1018–28 [Google Scholar]
  62. Kramer DM, Avenson TJ, Edwards GE. 62.  2004. Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci. 9:349–57 [Google Scholar]
  63. Kramer DM, Evans JR. 63.  2011. The importance of energy balance in improving photosynthetic productivity. Plant Physiol. 155:70–78 [Google Scholar]
  64. Kubicki A, Funk E, Westhoff P, Steinmuller K. 64.  1996. Differential expression of plastome-encoded ndh genes in mesophyll and bundle-sheath chloroplasts of the C4 plant Sorghum bicolor indicates that the complex I-homologous NAD(P)H-plastoquinone oxidoreductase is involved in cyclic electron transport. Planta 199:276–81 [Google Scholar]
  65. Kukuczka B, Magneschi L, Petroutsos D, Steinbeck J, Bald T. 65.  et al. 2014. Proton Gradient Regulation5-Like1-mediated cyclic electron flow is crucial for acclimation to anoxia and complementary to nonphotochemical quenching in stress adaptation. Plant Physiol. 165:1604–17 [Google Scholar]
  66. Kurisu G, Zhang H, Smith JL, Cramer WA. 66.  2003. Structure of the cytochrome b6f complex of oxygenic photosynthesis: tuning the cavity. Science 302:1009–14 [Google Scholar]
  67. Leister D, Shikanai T. 67.  2013. Complexities and protein complexes in the antimycin A-sensitive pathway of cyclic electron flow in plants. Front. Plant Sci. 4:161 [Google Scholar]
  68. Li XG, Duan W, Meng QW, Zou Q, Zhao SJ. 68.  2004. The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. Plant Cell Physiol. 45103–8
  69. Li XP, Gilmore AM, Caffarri S, Bassi R, Golan T. 69.  et al. 2004. Regulation of photosynthetic light harvesting involves intrathylakoid lumen pH sensing by the PsbS protein. J. Biol. Chem. 279:22866–74 [Google Scholar]
  70. Li XP, Müller-Moulé P, Gilmore AM, Niyogi KK. 70.  2002. PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. PNAS 99:15222–27 [Google Scholar]
  71. Long SP, Zhu XG, Naidu SL, Ort DR. 71.  2006. Can improvement in photosynthesis increase crop yields?. Plant Cell Environ 29:315–30 [Google Scholar]
  72. Long TA, Okegawa Y, Shikanai T, Schmidt GW, Covert SF. 72.  2008. Conserved role of PROTON GRADIENT REGULATOR 5 (PGR5) in the regulation of PSI cyclic electron transport. Planta 228:907–18 [Google Scholar]
  73. Martín M, Casano LM, Zapata JM, Guéra A, del Campo EM. 73.  et al. 2004. Role of thylakoid Ndh complex and peroxidase in the protection against photo-oxidative stress: fluorescence and enzyme activities in wild-type and ndhF-deficient tobacco. Physiol. Plant. 122:1–10 [Google Scholar]
  74. Matsubayashi T, Wakasugi T, Shinozaki K, Yamaguchi-Shinozaki K, Zaita N. 74.  et al. 1987. Six chloroplast genes (ndhA–F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Mol. Gen. Genet. 210:385–93 [Google Scholar]
  75. Miyake C. 75.  2010. Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol. 51:1951–63 [Google Scholar]
  76. Miyake C, Miyata M, Shinzaki Y, Tomizawa K. 76.  2005. CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves—relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. Plant Cell Physiol. 46:629–37 [Google Scholar]
  77. Miyake C, Okamura M. 77.  2003. Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts. Plant Cell Physiol. 44:457–62 [Google Scholar]
  78. Miyake C, Shinzaki Y, Miyata M, Tomizawa K. 78.  2004. Enhancement of cyclic electron flow around PSI at high light and its contribution to the induction of non-photochemical quenching (NPQ) of Chl fluorescence in intact leaves of tobacco plants. Plant Cell Physiol. 45:1426–33 [Google Scholar]
  79. Müller P, Li XP, Niyogi KK. 79.  2001. Non-photochemical quenching. A response to excess light energy. Plant Physiol. 125:1558–66 [Google Scholar]
  80. Munekage YN, Eymery F, Rumeau D, Cuine S, Oguri M. 80.  et al. 2010. Elevated expression of PGR5 and NDH-H in bundle sheath chloroplasts in C4Flaveria species. Plant Cell Physiol. 51:664–68 [Google Scholar]
  81. Munekage YN, Genty B, Peltier G. 81.  2008. Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant Cell Physiol. 49:1688–98 [Google Scholar]
  82. Munekage YN, Hashimoto M, Miyake C, Tomizawa K, Endo T. 82.  et al. 2004. Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–82 [Google Scholar]
  83. Munekage YN, Hojo M, Meurer J, Endo T, Tasaka M. 83.  et al. 2002. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–71 [Google Scholar]
  84. Munné-Bosch S, Shikanai T, Asada K. 84.  2005. Enhanced ferredoxin dependent cyclic electron flow around photosystem I and α-tocopherol quinone accumulation in water-stressed ndhB-inactivated tobacco mutants. Planta 222:502–11 [Google Scholar]
  85. Nagy G, Unnep R, Zsiros O, Ryutaro Tokutsu R, Takizawa K. 85.  et al. 2014. Chloroplast remodeling during state transitions in Chlamydomonas reinhardtii as revealed by noninvasive techniques in vivo. PNAS 111:5042–47 [Google Scholar]
  86. Nakamura N, Iwano M, Havaux M, Yokota A, Munekage YN. 86.  2013. Promotion of cyclic electron transport around photosystem I during the evolution of NADP-malic enzyme-type C4 photosynthesis in the genus Flaveria. New Phytol. 199:832–42 [Google Scholar]
  87. Nandha B, Finazzi G, Joliot P, Hald S, Johnson GN. 87.  2007. The role of PGR5 in the redox poising of photosynthetic electron transport. Biochim. Biophys. Acta 1767:1252–59 [Google Scholar]
  88. Nishikawa Y, Yamamoto H, Okegawa Y, Wada S, Sato N. 88.  et al. 2012. PGR5-dependent cyclic electron transport around PSI contributes to the redox homeostasis in chloroplasts rather than CO2 fixation and biomass production in rice. Plant Cell Physiol. 53:2117–26 [Google Scholar]
  89. Niyogi KK. 89.  1999. Photoprotection revisited: genetic and molecular approaches. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:333–59 [Google Scholar]
  90. Niyogi KK, Grossman AR, Bjorkman O. 90.  1998. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 10:1121–34 [Google Scholar]
  91. Niyogi KK, Truong TB. 91.  2013. Evolution of flexible non-photochemical quenching mechanisms that regulate light harvesting in oxygenic photosynthesis. Curr. Opin. Plant Biol. 16:307–14 [Google Scholar]
  92. Noctor G, Foyer CH. 92.  2000. Homeostasis of adenylate status during photosynthesis in a fluctuating environment. J. Exp. Bot. 51:347–56 [Google Scholar]
  93. Ogawa T, Mi H. 93.  2007. Cyanobacterial NADPH dehydrogenase complexes. Photosynth. Res. 93:69–77 [Google Scholar]
  94. Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T. 94.  et al. 1986. Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature 322:572–74 [Google Scholar]
  95. Okegawa Y, Kagawa Y, Kobayashi Y, Shikanai T. 95.  2008. Characterization of factors affecting the activity of photosystem I cyclic electron transport in chloroplasts. Plant Cell Physiol. 49:825–34 [Google Scholar]
  96. Okegawa Y, Kobayashi Y, Shikanai T. 96.  2010. Physiological links among alternative electron transport pathways that reduce and oxidize plastoquinone in Arabidopsis. Plant J. 63:458–68 [Google Scholar]
  97. Okegawa Y, Long TA, Iwano M, Takayama S, Kobayashi Y. 97.  et al. 2007. Balanced PGR5 level is required for chloroplast development and optimum operation of cyclic electron transport around photosystem I. Plant Cell Physiol. 48:1462–71 [Google Scholar]
  98. Okegawa Y, Tsuyama M, Kobayashi Y, Shikanai T. 98.  2005. The pgr1 mutation in the Rieske subunit of the cytochrome b6f complex does not affect PGR5-dependent cyclic electron transport around photosystem I. J. Biol. Chem. 280:28332–36 [Google Scholar]
  99. Peers G, Truong TB, Ostendorf E, Busch A, Elrad D. 99.  et al. 2009. An ancient light-harvesting protein is critical for the regulation of algal photosynthesis. Nature 462:518–21 [Google Scholar]
  100. Peltier G, Aro EM, Shikanai T. 100.  2016. NDH-1 and NDH-2 plastoquinone reductases in oxygenic photosynthesis. Annu. Rev. Plant. Biol. 67:55–80 [Google Scholar]
  101. Peltier G, Cournac L. 101.  2002. Chlororespiration. Annu. Rev. Plant Biol. 53:523–50 [Google Scholar]
  102. Peltier G, Tolleter D, Billon E, Cournac L. 102.  2010. Auxiliary electron transport pathways in chloroplasts of micro algae. Photosynth. Res. 106:19–31 [Google Scholar]
  103. Peng L, Fukao Y, Fujiwara M, Shikanai T. 103.  2012. Multistep assembly of chloroplast NADH dehydrogenase-like subcomplex A requires several nucleus-encoded proteins, including CRR41 and CRR42, in Arabidopsis. Plant Cell 24:202–14 [Google Scholar]
  104. Peng L, Fukao Y, Fujiwara M, Takami T, Shikanai T. 104.  2009. Efficient operation of NAD(P)H dehydrogenase requires supercomplex formation with photosystem I via minor LHCI in Arabidopsis. Plant Cell 21:3623–40 [Google Scholar]
  105. Peng L, Shikanai T. 105.  2011. Supercomplex formation with photosystem I is required for the stabilization of the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Physiol. 155:1629–39 [Google Scholar]
  106. Peng L, Yamamoto H, Shikanai T. 106.  2011. Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. Biochim. Biophys. Acta 1807:945–53 [Google Scholar]
  107. Petersen J, Förster K, Turina P, Gräber P. 107.  2012. Comparison of the H+/ATP ratios of the H+-ATP synthases from yeast and from chloroplast. PNAS 109:11150–55 [Google Scholar]
  108. Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS. 108.  et al. 2009. PGRL1 participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J. Biol. Chem. 284:32770–81 [Google Scholar]
  109. Prasil O, Kolber Z, Berry JA, Falkowski PG. 109.  1996. Cyclic electron flow around photosystem II in vivo.. Photosynth. Res. 48:395–410 [Google Scholar]
  110. Price GD, Yu JW, von Caemmerer S, Evans JR, Chow WS. 110.  et al. 1995. Chloroplast cytochrome b6/f and ATP synthase complexes in tobacco: transformation with antisense RNA against nuclear-encoded transcripts for the Rieske FeS and ATP polypeptides. Aust. J. Plant Physiol. 22:285–97 [Google Scholar]
  111. Rochaix JD. 111.  2011. Regulation of photosynthetic electron transport. Biochim. Biophys. Acta 1807:375–83 [Google Scholar]
  112. Rochaix JD. 112.  2014. Regulation and dynamics of the light-harvesting system. Annu. Rev. Plant Biol. 65:287–309 [Google Scholar]
  113. Scheibe R. 113.  2004. Malate valves to balance cellular energy supply. Physiol. Plant. 120:21–26 [Google Scholar]
  114. Seelert H, Dencher NA, Muller DJ. 114.  2003. Fourteen protomers compose the oligomer III of the proton-rotor in spinach chloroplast ATP synthase. J. Mol. Biol. 333:337–44 [Google Scholar]
  115. Seelert H, Poetsch A, Dencher NA, Engel A, Stahlberg H, Müller DJ. 115.  2000. Structural biology: proton-powered turbine of a plant motor. Nature 405:418–19 [Google Scholar]
  116. Shikanai T. 116.  2007. Cyclic electron transport around photosystem I: genetic approaches. Annu. Rev. Plant. Biol. 58:199–217 [Google Scholar]
  117. Shikanai T. 117.  2014. Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Curr. Opin. Biotechnol. 26:25–30 [Google Scholar]
  118. Shikanai T, Aro EM. 118.  2016. Evolution of photosynthetic NDH-1: structure and physiological function. Advances in Photosynthesis and Respiration Govindjee, TD Sharkey New York: Springer. In press [Google Scholar]
  119. Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A. 119.  1998. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. PNAS 95:9705–9 [Google Scholar]
  120. Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayashida N. 120.  et al. 1986. The complete nucleotide sequence of tobacco chloroplast genome: its gene organization and expression. EMBO J. 5:2043–49 [Google Scholar]
  121. Sonoike K. 121.  2011. Photoinhibition of photosystem I. Physiol. Plant. 142:56–64 [Google Scholar]
  122. Sonoike K, Terashima I, Iwaki M, Itoh S. 122.  1995. Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett. 362:235–38 [Google Scholar]
  123. Steigmiller S, Turina P, Gräber P. 123.  2008. The thermodynamic H+/ATP ratios of the H+-ATP synthases from chloroplasts and Escherichia coli. PNAS 105:3745–50 [Google Scholar]
  124. Stroebel D, Choquet Y, Popot JL, Picot D. 124.  2003. An atypical haem in the cytochrome b6f complex. Nature 426:413–18 [Google Scholar]
  125. Sugimoto K, Okegawa Y, Tohri A, Long TA, Sarah FS. 125.  et al. 2013. A single amino acid alteration in PGR5 confers resistance to antimycin A in cyclic electron transport around PSI. Plant Cell Physiol. 54:1525–34 [Google Scholar]
  126. Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M. 126.  et al. 2012. PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–48 [Google Scholar]
  127. Tagawa K, Tsujimoto HY, Arnon DI. 127.  1963. Role of chloroplast ferredoxin in the energy conversion process of photosynthesis. PNAS 49:567–72 [Google Scholar]
  128. Takabayashi A, Endo T, Shikanai T, Sato F. 128.  2002. Post-illumination reduction of the plastoquinone pool in chloroplast transformants in which chloroplastic NAD(P)H dehydrogenase was inactivated. Biosci. Biotechnol. Biochem. 66:2107–11 [Google Scholar]
  129. Takabayashi A, Kishine M, Asada K, Endo T, Sato F. 129.  2005. Differential use of two cyclic electron flows around photosystem I for driving CO2-concentration mechanism in C4 photosynthesis. PNAS 102:16898–903 [Google Scholar]
  130. Takahashi H, Clowez S, Wollman FA, Vallon O, Rappaport F. 130.  2013. Cyclic electron flow is redox-controlled but independent of state transition. Nat. Commun. 4:1954 [Google Scholar]
  131. Takahashi S, Badger MR. 131.  2011. Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci. 16:53–60 [Google Scholar]
  132. Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR. 132.  2009. How does cyclic electron flow alleviate photoinhibition in Arabidopsis?. Plant Physiol. 149:1560–67 [Google Scholar]
  133. Terashima M, Petroutsos D, Hüdig M, Tolstygina I, Trompelt K. 133.  et al. 2012. Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. PNAS 109:17717–22 [Google Scholar]
  134. Tikkanen M, Grieco M, Kangasjärvi S, Aro EM. 134.  2010. Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol. 152:723–35 [Google Scholar]
  135. Tikkanen M, Mekala NR, Aro EM. 135.  2014. Photosystem II photoinhibition-repair cycle protects photosystem I from irreversible damage. Biochim. Biophys. Acta 1837:210–15 [Google Scholar]
  136. Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I. 136.  et al. 2011. Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619–30 [Google Scholar]
  137. Ueda M, Kuniyoshi T, Yamamoto Y, Sugimoto K, Ishizaki K. 137.  et al. 2012. Composition and physiological function of the chloroplast NADH dehydrogenase-like complex in Marchantia polymorpha. Plant J. 72:683–93 [Google Scholar]
  138. Vollmar M, Schlieper D, Winn M, Büchner C, Groth G. 138.  2009. Structure of the c14 rotor ring of the proton translocating chloroplast ATP synthase. J. Biol. Chem. 284:18228–35 [Google Scholar]
  139. Wakasugi T, Tsudzuki J, Ito S, Nakashima K, Tsudzuki T, Sugiura M. 139.  1994. Loss of all ndh genes as determined by sequencing the entire chloroplast genome of the black pine Pinus thunbergii. PNAS 91:9794–98 [Google Scholar]
  140. Wang C, Yamamoto H, Shikanai T. 140.  2015. Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochim. Biophys. Acta 1847:931–38 [Google Scholar]
  141. Wang D, Portis AR Jr. 141.  2007. A novel nucleus-encoded chloroplast protein, PIFI, is involved in NAD(P)H dehydrogenase complex-mediated chlororespiratory electron transport in Arabidopsis. Plant Physiol. 144:1742–52 [Google Scholar]
  142. Wang P, Duan W, Takabayashi A, Endo T, Shikanai T. 142.  et al. 2006. Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiol. 141:465–74 [Google Scholar]
  143. Wang Y, He X, Ma W, Zhao X, Li B. 143.  et al. 2014. Wheat PROTON GRADIENT REGULATION 5 is involved in tolerance to photoinhibition. J. Integr. Agric. 13:1206–15 [Google Scholar]
  144. Wu D, Wright DA, Wetzel C, Voytas DF, Rodermel S. 144.  1999. The IMMUTANS variegation locus of Arabidopsis defines a mitochondrial alternative oxidase homolog that functions during early chloroplast biogenesis. Plant Cell 11:43–56 [Google Scholar]
  145. Xia D, Yu CA, Kim H, Xia JZ, Kachurin AM. 145.  et al. 1997. Crystal structure of the cytochrome bc1 complex from bovine heart mitochondria. Science 277:60–66 [Google Scholar]
  146. Yamamoto H, Peng L, Fukao Y, Shikanai T. 146.  2011. An Src homology 3 domain-like fold protein forms a ferredoxin-binding site for the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Cell 23:1480–93 [Google Scholar]
  147. Yamamoto H, Shikanai T. 147.  2013. In planta mutagenesis of Src homology 3 domain-like fold of NdhS, a ferredoxin-binding subunit of the chloroplast NADH dehydrogenase-like complex in Arabidopsis. A conserved Arg-193 plays a critical role in ferredoxin binding. J. Biol. Chem. 288:36328–37 [Google Scholar]
  148. Yamori W. 148.  2013. Improving photosynthesis to increase food and fuel production by biotechnological strategies in crops. J. Plant Biochem. Physiol. 1:113 [Google Scholar]
  149. Yamori W, Kondo E, Sugiura D, Terashima I, Suzuki Y. 149.  et al. 2016. Enhanced leaf photosynthesis as a target to increase grain yield: insights from transgenic rice lines with variable Rieske FeS protein content in the cytochrome b6/f complex. Plant Cell Environ. 39:80–87 [Google Scholar]
  150. Yamori W, Makino A, Shikanai T. 150.  2016. A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci. Rep. 6:20147 [Google Scholar]
  151. Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A. 151.  2011. Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. Plant J. 68:966–76 [Google Scholar]
  152. Yamori W, Shikanai T, Makino A. 152.  2015. Photosystem I cyclic electron flow via chloroplast NADH dehydrogenase-like complex performs a physiological role for photosynthesis at low light. Sci. Rep. 5:13908 [Google Scholar]
  153. Yamori W, Takahashi S, Makino A, Price GD, Badger MR. 153.  et al. 2011. The roles of ATP synthase and the cytochrome b6/f complexes in limiting chloroplast electron transport and determining photosynthetic capacity. Plant Physiol. 155:956–62 [Google Scholar]
  154. Yeremenko N, Jeanjean R, Prommeenate P, Krasikov V, Nixon PJ. 154.  et al. 2005. Open reading frame ssr2016 is required for antimycin A-sensitive photosystem I-driven cyclic electron flow in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 46:1433–36 [Google Scholar]
  155. Yoshida K, Matsuoka Y, Hara S, Konno H, Hisabori T. 155.  2014. Distinct redox behaviors of chloroplast thiol enzymes and their relationships with photosynthetic electron transport in Arabidopsis thaliana. Plant Cell Physiol. 55:1415–25 [Google Scholar]
  156. Zapata JM, Guera A, Esteban-Carrasco A, Martin M, Sabater B. 156.  2005. Chloroplasts regulate leaf senescence: delayed senescence in transgenic ndhF-defective tobacco. Cell Death Differ. 12:1277–84 [Google Scholar]
  157. Zhang R, Sharkey TD. 157.  2009. Photosynthetic electron transport and proton flux under moderate heat stress. Photosynth. Res. 100:29–43 [Google Scholar]
  158. Zhu SH, Green BR. 158.  2010. Photoprotection in the diatom Thalassiosira pseudonana: role of LI818-like proteins in response to high light stress. Biochim. Biophys. Acta 1797:1449–57 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043015-112002
Loading
/content/journals/10.1146/annurev-arplant-043015-112002
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error