Journal of Plant Research

, Volume 129, Issue 3, pp 379–395 | Cite as

Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress

  • Wataru YamoriEmail author
JPR Symposium Responses of the Photosynthetic Systems to Spatio-temporal Variations in Light Environments: Scaling and Eco-devo Approaches


Plants in natural environments must cope with diverse, highly dynamic, and unpredictable conditions. They have mechanisms to enhance the capture of light energy when light intensity is low, but they can also slow down photosynthetic electron transport to prevent the production of reactive oxygen species and consequent damage to the photosynthetic machinery under excess light. Plants need a highly responsive regulatory system to balance the photosynthetic light reactions with downstream metabolism. Various mechanisms of regulation of photosynthetic electron transport under stress have been proposed, however the data have been obtained mainly under environmentally stable and controlled conditions. Thus, our understanding of dynamic modulation of photosynthesis under dramatically fluctuating natural environments remains limited. In this review, first I describe the magnitude of environmental fluctuations under natural conditions. Next, I examine the effects of fluctuations in light intensity, CO2 concentration, leaf temperature, and relative humidity on dynamic photosynthesis. Finally, I summarize photoprotective strategies that allow plants to maintain the photosynthesis under stressful fluctuating environments. The present work clearly showed that fluctuation in various environmental factors resulted in reductions in photosynthetic rate in a stepwise manner at every environmental fluctuation, leading to the conclusion that fluctuating environments would have a large impact on photosynthesis.


Alternative pathway Electron transport Fluctuating environment Photoinhibition Photoprotection Photosynthesis 



This work was supported by the Japan Science and Technology Agency, PRESTO (to W.Y.).


  1. Ainsworth EA, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270. doi: 10.1111/j.1365-3040.2007.01641.x PubMedCrossRefGoogle Scholar
  2. Ainsworth EA, Davey PA, Bernacchi CJ et al (2002) A meta-analysis of elevated [CO2] effects on soybean (Glycine max) physiology, growth and yield. Glob Chang Biol 8:695–709. doi: 10.1046/j.1365-2486.2002.00498.x CrossRefGoogle Scholar
  3. Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19. doi: 10.1016/S1360-1385(02)00006-7 PubMedCrossRefGoogle Scholar
  4. Allen MT, Pearcy RW (2000) Stomatal versus biochemical limitations to dynamic photosynthetic performance in four tropical rainforest shrub species. Oecologia 122:479–486. doi: 10.1007/s004420050969 CrossRefGoogle Scholar
  5. André MJ (2011) Modelling 18O2 and 16O2 unidirectional fluxes in plants: II. Analysis of Rubisco evolution. Biosystems 103:252–264. doi: 10.1016/j.biosystems.2010.10.003 PubMedCrossRefGoogle Scholar
  6. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399. doi: 10.1146/annurev.arplant.55.031903.141701 CrossRefGoogle Scholar
  7. Arena C, Vitale L, De Santo AV (2008) Paraheliotropism in Robinia pseudoacacia L.: an efficient strategy to optimise photosynthetic performance under natural environmental conditions. Plant Biol 10:194–201. doi: 10.1111/j.1438-8677.2008.00032.x PubMedCrossRefGoogle Scholar
  8. Aro EM, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134. doi: 10.1016/0005-2728(93)90134-2 PubMedCrossRefGoogle Scholar
  9. Aro E-M, Suorsa M, Rokka A et al (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56:347–356. doi: 10.1093/jxb/eri041 PubMedCrossRefGoogle Scholar
  10. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639. doi: 10.1146/annurev.arplant.50.1.601 PubMedCrossRefGoogle Scholar
  11. Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396. doi: 10.1104/pp.106.082040 PubMedPubMedCentralCrossRefGoogle Scholar
  12. Baena-Gonzalez E, Aro EM (2002) Biogenesis, assembly and turnover of photosystem II units. Philos Trans R Soc Lond B Biol Sci 357:1451–1459. doi: 10.1098/rstb.2002.1141 PubMedPubMedCentralCrossRefGoogle Scholar
  13. Bai KD, Liao DB, Jiang DB, Cao KF (2008) Photosynthetic induction in leaves of co-occurring Fagus lucida and Castanopsis lamontii saplings grown in contrasting light environments. Trees 22:449–462. doi: 10.1007/s00468-007-0205-4 CrossRefGoogle Scholar
  14. Bauwe H, Hagemann M, Fernie AR (2010) Photorespiration: players, partners and origin. Trends Plant Sci 15:330–336. doi: 10.1016/j.tplants.2010.03.006 PubMedCrossRefGoogle Scholar
  15. Bernacchi CJ, Bagley JE, Serbin SP et al (2013) Modelling C3 photosynthesis from the chloroplast to the ecosystem. Plant Cell Environ 36:1641–1657. doi: 10.1111/pce.12118 PubMedCrossRefGoogle Scholar
  16. Bielenberg DG, Miller JD, Berg VS (2003) Paraheliotropism in two Phaseolus species: combined effects of photon flux density and pulvinus temperature, and consequences for leaf gas exchange. Environ Exp Bot 49:95–105. doi: 10.1016/S0098-8472(02)00062-X CrossRefGoogle Scholar
  17. Blot N, Mella-Flores D, Six C et al (2011) Light history influences the response of the marine cyanobacterium Synechococcus sp. WH7803 to oxidative stress. Plant Physiol 156:1934–1954. doi: 10.1104/pp.111.174714 PubMedPubMedCentralCrossRefGoogle Scholar
  18. Brugnoli E, Bjorkman O (1992) Chloroplast movements in leaves: influence on chlorophyll fluorescence and measurements of light-induced absorbance changes related to pH and zeaxanthin formation. Photosynth Res 32:23–35. doi: 10.1007/BF00028795 PubMedCrossRefGoogle Scholar
  19. Buchanan BB (1980) Role of light in the regulation of chloroplast enzymes. Annu Rev Plant Physiol 31:341–374. doi: 10.1146/annurev.pp.31.060180.002013 CrossRefGoogle Scholar
  20. Buchanan BB (1991) Regulation of CO2 assimilation in oxygenic photosynthesis: the ferredoxin/thioredoxin system. Perspective on its discovery, present status, and future development. Arch Biochem Biophys 288:1–9. doi: 10.1016/0003-9861(91)90157-E PubMedCrossRefGoogle Scholar
  21. Bunce JA (1997) Does transpiration control stomatal responses to water vapour pressure deficit? Plant Cell Environ 20:131–135CrossRefGoogle Scholar
  22. 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. doi: 10.1093/emboj/17.4.868 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Cardon ZG, Berry J (1992) Effects of O2 and CO2 concentration on the steady-state fluorescence yield of single guard cell pairs in intact leaf discs of Tradescantia albiflora. Plant Physiol 99:1238–1244. doi: 10.1104/pp.99.3.1238 PubMedPubMedCentralCrossRefGoogle Scholar
  24. Cardon ZG, Berry JA, Woodward IE (1994) Dependence of the extent and direction of average stomatal responses in Zea mays L. and Phaseolus vulgaris L. on the frequency of fluctuations in environmental stimuli. Plant Physiol 105:1007–1013. doi: 10.1104/pp.105.3.1007 PubMedPubMedCentralGoogle Scholar
  25. Cardon ZG, Berry JA, Woodward IE (1995) Fluctuating [CO2] drives species specific changes in water use efficiency. J Biogeogr 22:203–208. doi: 10.2307/2845911 CrossRefGoogle Scholar
  26. Carol P, Kuntz M (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trend Plant Sci 6:31–36. doi: 10.1016/S1360-1385(00)01811-2 CrossRefGoogle Scholar
  27. Chang CC, Slesak I, Jordá L et al (2009) Arabidopsis chloroplastic glutathione peroxidases play a role in cross talk between photooxidative stress and immune responses. Plant Physiol 150:670–683. doi: 10.1104/pp.109.135566 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. doi: 10.1093/aob/mcn125 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Chazdon RL, Pearcy RW (1986) Photosynthetic responses to light variation in rainforest species. II. Carbon gain and photosynthetic efficiency during lightflecks. Oecologia 69:524–531. doi: 10.1007/BF00410358 CrossRefGoogle Scholar
  30. Chen JW, Zhang Q, Li XS, Cao KF (2011) Steady and dynamic photosynthetic responses of seedlings from contrasting successional groups under low-light growth conditions. Physiol Plant 141:84–95. doi: 10.1111/j.1399-3054.2010.01414.x PubMedCrossRefGoogle Scholar
  31. Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212:808–816. doi: 10.1007/s004250000432 PubMedCrossRefGoogle Scholar
  32. Conklin PL, Williams EH, Last RL (1996) Environmental stress sensitivity of an ascorbic acid-deficient Arabidopsis mutant. Proc Natl Acad Sci USA 93:9970–9974PubMedPubMedCentralCrossRefGoogle Scholar
  33. Corlett JE, Jones HG, Massacci A, Masojidek J (1994) Water deficit, leaf rolling and susceptibility to photoinhibition in field grown sorghum. Physiol Plant 92:423–430. doi: 10.1111/j.1399-3054.1994.tb08831.x CrossRefGoogle Scholar
  34. Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture—not by affecting ATP synthesis. Trends Plant Sci 5:187–188. doi: 10.1016/S1360-1385(00)01625-3 CrossRefGoogle Scholar
  35. Crafts-Brandner SJ, Salvucci ME (2000) Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proc Natl Acad Sci USA 97:13430–13435. doi: 10.1073/pnas.230451497 PubMedPubMedCentralCrossRefGoogle Scholar
  36. DalCorso G, Pesaresi P, Masiero S et al (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285. doi: 10.1016/j.cell.2007.12.028 PubMedCrossRefGoogle Scholar
  37. Davison PA, Hunter CN, Horton P (2002) Overexpression of β-carotene hydroxylase enhances stress tolerance in Arabidopsis. Nature 418:203–206. doi: 10.1038/nature00861 PubMedCrossRefGoogle Scholar
  38. DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738. doi: 10.1146/annurev.arplant.56.032604.144301 PubMedCrossRefGoogle Scholar
  39. Demmig-Adams B, Adams WW III (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626. doi: 10.1146/annurev.pp.43.060192.003123 CrossRefGoogle Scholar
  40. Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515. doi: 10.1146/annurev.genet.42.110807.091452 PubMedCrossRefGoogle Scholar
  41. Evans JR, Jakobsen I, Ogren E (1993) Photosynthetic light-response curves 2. Gradients of light absorption and photosynthetic capacity. Planta 189:191–200. doi: 10.1007/BF00195076 CrossRefGoogle Scholar
  42. Fan DY, Nie Q, Hope AB, Hillier W, Pogson BJ, Chow WS (2007) Quantification of cyclic electron flow around photosystem I in spinach leaves during photosynthetic induction. Photosynth Res 94:347–357. doi: 10.1007/s11120-006-9127-z PubMedCrossRefGoogle Scholar
  43. Fan D, Ye Z, Wang S, Chow WS (2016) Multiple roles of oxygen in the photoinactivation and dynamic repair of photosystem II in spinach leaves. Photosynth Res 127:307–319. doi: 10.1007/s11120-015-0185-y PubMedCrossRefGoogle Scholar
  44. Farquhar GD, Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149:78–90. doi: 10.1007/BF00386231 PubMedCrossRefGoogle Scholar
  45. Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189. doi: 10.1093/aob/mcf027 PubMedPubMedCentralCrossRefGoogle Scholar
  46. Forseth IN, Ehleringer JR (1982) Ecophysiology of two solar-tracking desert winter annuals. II. Leaf movements, water relations and microclimate. Oecologia 54:41–49. doi: 10.1007/BF00541105 CrossRefGoogle Scholar
  47. Foyer CH, Trebst A, Noctor G (2006) Signaling and integration of defense functions of tocopherol, ascorbate and glutathione. In: Demmig-Adams B, Adams WW III, Mattoo AK (eds) Photoprotection, photoinhibition, gene regulation and environment. Springer, Dordrecht, pp 241–268. doi: 10.1007/1-4020-3579-9_16 CrossRefGoogle Scholar
  48. Gamon JA, Pearcy RW (1989) Leaf movement, stress avoidance and photosynthesis in Vitis californica. Oecologia 79:475–481. doi: 10.1007/BF00378664 CrossRefGoogle Scholar
  49. Gamon JA, Pearcy RW (1990) Photoinhibition in Vitis californica: interactive effects of sunlight, temperature and water status. Plant Cell Environ 13:267–275. doi: 10.1111/j.1365-3040.1990.tb01311.x CrossRefGoogle Scholar
  50. Golding AJ, Finazzi G, Johnson GN (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 220:356–363. doi: 10.1007/s00425-004-1345-z PubMedCrossRefGoogle Scholar
  51. Grieco M, Tikkanen M, Paakkarinen V, Kangasjarvi S, Aro EM (2012) Steady-state phosphorylation of light-harvesting complex II proteins preserves photosystem I under fluctuating white light. Plant Physiol 160:1896–1910. doi: 10.1104/pp.112.206466 PubMedPubMedCentralCrossRefGoogle Scholar
  52. Groenendijk M, Dolman AJ, van der Molen MK et al (2011) Assessing parameter variability in a photosynthesis model within and between plant functional types using global Fluxnet eddy covariance data. Agric For Meteorol 151:22–38. doi: 10.1016/j.agrformet.2010.08.013 CrossRefGoogle Scholar
  53. Han Q, Yamaguchi E, Odaka N, Kakubari Y (1999) Photosynthetic induction responses to variable light under field conditions in three species grown in the gap and understory of a Fagus crenata forest. Tree Physiol 19:625–634. doi: 10.1093/treephys/19.10.625 PubMedCrossRefGoogle Scholar
  54. Hanson DT, Swanson S, Graham LE, Sharkey TD (1999) Evolutionary significance of isoprene emission from mosses. Am J Bot 86:634–639. doi: 10.2307/2656571 PubMedCrossRefGoogle Scholar
  55. Havaux M, Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of photosystem-II activity. Photosynth Res 40:75–92. doi: 10.1007/BF00019047 PubMedCrossRefGoogle Scholar
  56. Havaux M, Niyogi KK (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767. doi: 10.1073/pnas.96.15.8762 PubMedPubMedCentralCrossRefGoogle Scholar
  57. Hertle AP, Blunder T, Wunder T et al (2013) PGRL1 is the elusive ferredoxin-plastoquinone reductase in photosynthetic cyclic electron flow. Mol Cell 49:511–523. doi: 10.1016/j.molcel.2012.11.030 PubMedCrossRefGoogle Scholar
  58. Hideg É, Deák Z, Hakala-Yatkin M et al (2011) Pure forms of the singlet oxygen sensors TEMP and TEMPD do not inhibit photosystem II. Biochim Biophys Acta 1807:1658–1661. doi: 10.1016/j.bbabio.2011.09.009 PubMedCrossRefGoogle Scholar
  59. Holt NE, Fleming GR, Niyogi KK (2004) Toward an understanding of the mechanism of non-photochemical quenching in green plants. Biochemistry 43:8281–8289. doi: 10.1021/bi0494020 PubMedCrossRefGoogle Scholar
  60. Horváth EM, Peter SO, Joet T 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 123:1337–1350. doi: 10.1104/pp.123.4.1337 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotechnol Biochem 72:1143–1154. doi: 10.1271/bbb.80062 PubMedCrossRefGoogle Scholar
  62. Jiang CD, Gao HY, Zou Q, Jiang GM, Li LH (2006) Leaf orientation, photorespiration and xanthophyll cycle protect young soybean leaves against high irradiance in the field. Environ Exp Bot 55:87–96. doi: 10.1016/j.envexpbot.2004.10.003 CrossRefGoogle Scholar
  63. Josse EM, Simkin AJ, Gaffé J, Labouré AM, Kuntz M, Carol P (2000) A plastid terminal oxidase associated with carotenoid desaturation during chromoplast differentiation. Plant Physiol 123:1427–1436. doi: 10.1104/pp.123.4.1427 PubMedPubMedCentralCrossRefGoogle Scholar
  64. Kagawa T, Wada M (2004) Velocity of chloroplast avoidance movement is fluence rate dependent. Photochem Photobiol Sci 3:592–595. doi: 10.1039/B316285K PubMedCrossRefGoogle Scholar
  65. Kaiser E, Morales A, Harbinson J, Kromdijk J, Heuvelink E, Marcelis LFM (2015) Dynamic photosynthesis in different environmental conditions. J Exp Bot 66:2415–2426. doi: 10.1093/jxb/eru406 PubMedCrossRefGoogle Scholar
  66. Kanwischer M, Porfirova S, Bergmüller E, Dörmann P (2005) Alterations in tocopherol cyclase activity in transgenic and mutant plants of Arabidopsis affect tocopherol content, tocopherol composition, and oxidative stress. Plant Physiol 137:713–723. doi: 10.1104/pp.104.054908 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Kasahara M, Kagawa T, Oikawa K et al (2002) Chloroplast avoidance movement reduces photodamage in plants. Nature 420:829–832. doi: 10.1038/nature01213 PubMedCrossRefGoogle Scholar
  68. Kirschbaum MUF, Pearcy RW (1988) Gas exchange analysis of the fast phase of photosynthetic induction in Alocasia macrorrhiza. Plant Physiol 87:818–821. doi: 10.1104/pp.87.4.818 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Kofer W, Koop HU, Wanner G, Steinmüller K (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 258:166–173. doi: 10.1007/s004380050719 PubMedCrossRefGoogle Scholar
  70. Kono M, Noguchi K, Terashima I (2014) Roles of 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. doi: 10.1093/pcp/pcu033 PubMedCrossRefGoogle Scholar
  71. Kornyeyev D, Logan BA, Allen RD, Holaday AS (2003a) Effect of chloroplastic overexpression of ascorbate peroxidase on photosynthesis and photoprotection in cotton leaves subjected to low temperature photoinhibition. Plant Sci 165:1033–1041. doi: 10.1016/S0168-9452(03)00294-2 CrossRefGoogle Scholar
  72. Kornyeyev D, Logan BA, Payton PR, Allen RD, Holaday AS (2003b) Elevated chloroplastic glutathione reductase activities decrease chilling-induced photoinhibition by increasing rates of photochemistry, but not thermal energy dissipation, in transgenic cotton. Funct Plant Biol 30:101–110. doi: 10.1071/FP02144 CrossRefGoogle Scholar
  73. Kornyeyev D, Logan BA, Holaday AS (2010) Excitation pressure as a measure of the sensitivity of photosystem II to photoinactivation. Funct Plant Biol 37:943–951. doi: 10.1071/fp09276 CrossRefGoogle Scholar
  74. Kozaki A, Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384:557–560. doi: 10.1038/384557a0 CrossRefGoogle Scholar
  75. Kramer DM, Avenson TJ, Edwards GE (2004) Dynamic flexibility in the light reactions of photosynthesis governed by both electron and proton transfer reactions. Trends Plant Sci 9:349–357. doi: 10.1016/j.tplants.2004.05.001 PubMedCrossRefGoogle Scholar
  76. Kudoh H, Sonoike K (2002) Irreversible damage to photosystem I by chilling in the light: cause of the degradation of chlorophyll after returning to normal growth temperature. Planta 215:541–548. doi: 10.1007/s00425-002-0790-9 PubMedCrossRefGoogle Scholar
  77. Kuntz M (2004) Plastid terminal oxidase and its biological significance. Planta 218:896–899. doi: 10.1007/s00425-004-1217-6 PubMedCrossRefGoogle Scholar
  78. Kuvykin IV, Ptushenko VV, Vershubskii AV, Tikhonov AN (2011) Regulation of electron transport in C3 plant chloroplasts in situ and in silico. Short-term effects of atmospheric CO2 and O2. Biochim Biophys Acta 1807:336–347. doi: 10.1016/j.bbabio.2010.12.012 PubMedCrossRefGoogle Scholar
  79. Laisk A, Eichelmann H, Oja V, Peterson RB (2005) Control of cytochrome b6f at low and high light intensity and cyclic electron transport in leaves. Biochim Biophys Acta 1708:79–90. doi: 10.1016/j.bbabio.2005.01.007 PubMedCrossRefGoogle Scholar
  80. Laisk A, Eichelmann H, Oja V, Talts E, Scheibe R (2007) Rates and roles of cyclic and alternative electron flow in potato leaves. Plant Cell Physiol 48:1575–1588. doi: 10.1093/pcp/pcm129 PubMedCrossRefGoogle Scholar
  81. Lawson T, Oxborough K, Morison JIL, Baker NR (2002) Responses of photosynthetic electron transport in stomatal guard cells and mesophyll cells in intact leaves to light, CO2, and humidity. Plant Physiol 128:52–62. doi: 10.1104/pp.010317 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Leakey ADB, Scholes JD, Press MC (2004) Physiological and ecological significance of sunflecks for dipterocarp seedlings. J Exp Bot 56:469–482. doi: 10.1093/jxb/eri055 PubMedCrossRefGoogle Scholar
  83. Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395. doi: 10.1038/35000131 PubMedCrossRefGoogle Scholar
  84. Li XP, Muller-Moule P, Gilmore AM, Niyogi KK (2002) PsbS-dependent enhancement of feedback de-excitation protects photosystem II from photoinhibition. Proc Natl Acad Sci USA 99:15222–15227. doi: 10.1073/pnas.232447699 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Long SP, Zhu XG, Naidu SL, Ort DR (2006) Can improvement in photosynthesis increase crop yields? Plant Cell Environ 29:315–330PubMedCrossRefGoogle Scholar
  86. Lu N, Nukaya T, Kamimura T et al (2015) Control of vapor pressure deficit (VPD) in greenhouse enhanced tomato growth and productivity during the winter season. Sci Hortic 197:17–23. doi: 10.1016/j.scienta.2015.11.001 CrossRefGoogle Scholar
  87. Ludlow MM, Bjorkman O (1984) Paraheliotropic leaf movement in Siratro as a protective mechanism against drought-induce damage to primary photosynthetic reactions: damage by excessive light and heat. Planta 161:505–518. doi: 10.1007/BF00407082 PubMedCrossRefGoogle Scholar
  88. Makino A, Miyake C, Yokota A (2002) Physiological functions of the water-water cycle (Mehler reaction) and the cyclic electron flow around PSI in rice leaves. Plant Cell Physiol 43:1017–1026. doi: 10.1093/pcp/pcf124 PubMedCrossRefGoogle Scholar
  89. McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Huner NPA (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967. doi: 10.1016/j.bbabio.2010.10.024 PubMedCrossRefGoogle Scholar
  90. Medlyn BE, Barton CVM, Broadmeadow MSJ et al (2001) Stomatal conductance of forest species after long-term exposure to elevated CO2 concentration: a synthesis. New Phytol 149:247–264. doi: 10.1046/j.1469-8137.2001.00028.x CrossRefGoogle Scholar
  91. Mehler AH (1951) Studies on reactions of illuminated chloroplasts. I. Mechanisms of the reduction of oxygen and other Hill reagents. Arch Biochem Biophys 33:65–77. doi: 10.1016/0003-9861(51)90082-3 PubMedCrossRefGoogle Scholar
  92. Miyake C (2010) Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: molecular mechanisms and physiological functions. Plant Cell Physiol 51:1951–1963. doi: 10.1093/pcp/pcq173 PubMedCrossRefGoogle Scholar
  93. Miyake C, Okamura M (2003) Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts. Plant Cell Physiol 44:457–462. doi: 10.1093/pcp/pcg053 PubMedCrossRefGoogle Scholar
  94. Miyake C, Miyata M, Shinzaki Y, Tomizawa K (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 46:629–637. doi: 10.1093/pcp/pci067 PubMedCrossRefGoogle Scholar
  95. Morison JIL (1998) Stomatal response to increased CO2 concentration. J Exp Bot 49:443–453. doi: 10.1093/jxb/49.Special_Issue.443 CrossRefGoogle Scholar
  96. Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566. doi: 10.1104/pp.125.4.1558 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Munekage Y, Hojo M, Meurer J et al (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371. doi: 10.1016/S0092-8674(02)00867-X PubMedCrossRefGoogle Scholar
  98. Munekage Y, Hashimoto M, Miyake C et al (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582. doi: 10.1038/nature02598 PubMedCrossRefGoogle Scholar
  99. Murchie EH, Chen YZ, Hubbart S, Peng SB, Horton P (1999) Interactions between senescence and leaf orientation determine in situ patterns of photosynthesis and photoinhibition in field-grown rice. Plant Physiol 119:553–563. doi: 10.1104/pp.119.2.553 PubMedPubMedCentralCrossRefGoogle Scholar
  100. Naumburg E, Ellsworth DS (2002) Short-term light and leaf photosynthetic dynamics affect estimates of daily understory photosynthesis in four tree species. Tree Physiol 22:393–401. doi: 10.1093/treephys/22.6.393 PubMedCrossRefGoogle Scholar
  101. Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Wollman FA (2015) The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Ann Rev Plant Biol 66:49–74. doi: 10.1146/annurev-arplant-043014-114744 CrossRefGoogle Scholar
  102. Nishiyama Y, Allakhverdiev SI, Murata N (2006) A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochim Biophys Acta 1757:742–749. doi: 10.1016/j.bbabio.2006.05.013 PubMedCrossRefGoogle Scholar
  103. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359. doi: 10.1146/annurev.arplant.50.1.333 PubMedCrossRefGoogle Scholar
  104. Niyogi KK (2000) Safety valves for photosynthesis. Curr Opin Plant Biol 3:455–460. doi: 10.1016/S1369-5266(00)00113-8 PubMedCrossRefGoogle Scholar
  105. Niyogi KK, Li XP, Rosenberg V, Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56:375–382. doi: 10.1093/jxb/eri056 PubMedCrossRefGoogle Scholar
  106. Noctor G, Dutilleul C, De Paepe R, Foyer CH (2004) Use of mitochondrial electron transport mutants to evaluate the effects of redox state on photosynthesis, stress tolerance and the integration of carbon/nitrogen metabolism. J Exp Bot 55:49–57. doi: 10.1093/jxb/erh021 PubMedCrossRefGoogle Scholar
  107. Noguchi K, Yoshida K (2008) Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 8:87–99. doi: 10.1016/j.mito.2007.09.003 PubMedCrossRefGoogle Scholar
  108. Ogren WL (1984) Photorespiration: pathways, regulation, and modification. Ann Rev Plant Physiol 35:415–442. doi: 10.1146/annurev.pp.35.060184.002215 CrossRefGoogle Scholar
  109. Ögren E, Evans JR (1993) Photosynthetic light response curves. 1. The influence of CO2 partial pressure and leaf inversion. Planta 189:182–190. doi: 10.1007/BF00195075 CrossRefGoogle Scholar
  110. Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opp Plant Biol 5:193–197. doi: 10.1016/S1369-5266(02)00259-5 CrossRefGoogle Scholar
  111. Osmond CB (1981) Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim Biophys Acta 639:77–98. doi: 10.1016/0304-4173(81)90006-9 CrossRefGoogle Scholar
  112. Pastenes C, Pimentel P, Lillo J (2005) Leaf movements and photoinhibition in relation to water stress in field-grown beans. J Exp Bot 56:425–433. doi: 10.1093/jxb/eri061 PubMedCrossRefGoogle Scholar
  113. Peak D, Mott KA (2011) A new, vapour-phase mechanism for stomatal responses to humidity and temperature. Plant Cell Environ 34:162–178. doi: 10.1111/j.1365-3040.2010.02234.x PubMedCrossRefGoogle Scholar
  114. Pearcy RW (1988) Photosynthetic utilization of lightflecks by understory plants. Aust J Plant Physiol 15:223–238. doi: 10.1071/PP9880223 CrossRefGoogle Scholar
  115. Pearcy RW (1990) Sunflecks and photosynthesis in plant canopies. Annu Rev Plant Physiol Plant Mol Biol 41:421–453. doi: 10.1146/annurev.pp.41.060190.002225 CrossRefGoogle Scholar
  116. Pearcy RW, Way DA (2012) Two decades of sunfleck research: looking back to move forward. Tree Physiol 32:1059–1061. doi: 10.1093/treephys/tps084 PubMedCrossRefGoogle Scholar
  117. Peltier G, Cournac L (2002) Chlororespiration. Annu Rev Plant Biol 53:523–550. doi: 10.1146/annurev.arplant.53.100301.135242 PubMedCrossRefGoogle Scholar
  118. Peng L, Yamamoto H, Shikanai T (2011) Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. Biochim Biophys Acta 1807:945–953. doi: 10.1016/j.bbabio.2010.10.015 PubMedCrossRefGoogle Scholar
  119. Pfitsch WA, Pearcy RW (1989) Steady-state and dynamic photosynthetic response of Adenocaulon bicolor (Asteraceae) in its redwood forest habitat. Oecologia 80:471–476. doi: 10.1007/BF00380068 CrossRefGoogle Scholar
  120. Portis AR Jr (2003) Rubisco activase: Rubisco’s catalytic chaperone. Photosynth Res 75:11–27. doi: 10.1023/A:1022458108678 PubMedCrossRefGoogle Scholar
  121. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44. doi: 10.1146/annurev.pp.35.060184.000311 CrossRefGoogle Scholar
  122. Prasil O, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around photosystem II in vivo. Photosynth Res 48:395–410. doi: 10.1007/BF00029472 PubMedCrossRefGoogle Scholar
  123. Raghavendra AS, Padmasree K (2003) Beneficial interactions of mitochondrial metabolism with photosynthetic carbon assimilation. Trends Plant Sci 8:546–553. doi: 10.1016/j.tplants.2003.09.015 PubMedCrossRefGoogle Scholar
  124. Rawson HM, Begg JE, Woodward RG (1977) The effect of atmospheric humidity on photosynthesis, transpiration and water use efficiency of leaves of several plant species. Planta 134:5–10. doi: 10.1007/BF00390086 PubMedCrossRefGoogle Scholar
  125. Rijkers T, de Vries PJ, Pons TL, Bongers F (2000) Photosynthetic induction in saplings of three shade-tolerant tree species: comparing understorey and gap habitats in a French Guiana rain forest. Oecologia 125:331–340. doi: 10.1007/s004420000459 CrossRefGoogle Scholar
  126. Ruuska SA, Badger MR, Andrews TJ, von Caemmerer S (2000) Photosynthetic electron sinks in transgenic tobacco with reduced amounts of Rubisco: little evidence for significant Mehler reaction. J Exp Bot 51:357–368. doi: 10.1093/jexbot/51.suppl_1.357 PubMedCrossRefGoogle Scholar
  127. Sage RF, Sage TL, Kocacinar F (2012) Photorespiration and the evolution of C4 photosynthesis. Ann Rev Plant Biol 63:19–47. doi: 10.1146/annurev-arplant-042811-105511 CrossRefGoogle Scholar
  128. Salvucci ME, Crafts-Brandner SJ (2004) Relationship between the heat tolerance of photosynthesis and the thermal stability of Rubisco activase in plants from contrasting thermal environments. Plant Physiol 134:1460–1470. doi: 10.1104/pp.103.038323 PubMedPubMedCentralCrossRefGoogle Scholar
  129. Sassenrath-Cole GF, Pearcy RW (1992) The role of ribulose-1,5-bisphosphate regeneration in the induction requirement of photosynthetic CO2 exchange under transient light conditions. Plant Physiol 99:227–234PubMedPubMedCentralCrossRefGoogle Scholar
  130. Sassenrath-Cole GF, Pearcy RW (1994) Regulation of photosynthetic induction state by the magnitude and duration of low light exposure. Plant Physiol 105:1115–1123. doi: 10.1104/pp.105.4.1115 PubMedPubMedCentralGoogle Scholar
  131. Scheibe R (2004) Malate valves to balance cellular energy supply. Physiol Plant 120:21–26. doi: 10.1111/j.0031-9317.2004.0222.x PubMedCrossRefGoogle Scholar
  132. Scheibe R, Backhausen JE, Emmerlich V, Holtgrefe S (2005) Strategies to maintain redox homeostasis during photosynthesis under changing conditions. J Exp Bot 56:1481–1489. doi: 10.1093/jxb/eri181 PubMedCrossRefGoogle Scholar
  133. Schymanski SJ, Or D, Zwieniecki M (2013) Stomatal control and leaf thermal and hydraulic capacitances under rapid environmental fluctuations. PLoS One 8:e54231. doi: 10.1371/journal.pone.0054231 PubMedPubMedCentralCrossRefGoogle Scholar
  134. Shikanai T, Endo T, Hashimoto T et al (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95:9705–9709PubMedPubMedCentralCrossRefGoogle Scholar
  135. Sims DA, Pearcy RW (1993) Sunfleck frequency and duration affect growth-rate of the understorey plant, Alocasia macrorrhiza. Funct Ecol 7:683–689. doi: 10.2307/2390189 CrossRefGoogle Scholar
  136. Singsaas EL, Sharkey TD (1998) The regulation of isoprene emission responses to rapid leaf temperature fluctuations. Plant Cell Environ 21:1181–1188. doi: 10.1046/j.1365-3040.1998.00380.x CrossRefGoogle Scholar
  137. Singsaas EL, Laporte MM, Shi JZ et al (1999) Leaf temperature fluctuation affects isoprene emission from red oak (Quercus rubra) leaves. Tree Physiol 19:917–924. doi: 10.1093/treephys/19.14.917 PubMedCrossRefGoogle Scholar
  138. Smith H (1982) Light quality, photoperception, and plant strategy. Ann Rev Plant Physiol 33:481–518. doi: 10.1146/annurev.pp.33.060182.002405 CrossRefGoogle Scholar
  139. Sonoike K (2011) Photoinhibition of photosystem I. Physiol Plant 142:56–64. doi: 10.1111/j.1399-3054.2010.01437.x PubMedCrossRefGoogle Scholar
  140. Sonoike K, Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194:287–293. doi: 10.1007/BF00196400 CrossRefGoogle Scholar
  141. Streb P, Josse EM, Gallouet E, Baptist F, Kuntz M, Cornic G (2005) Evidence for alternative electron sinks to photosynthetic carbon assimilation in the high mountain plant species Ranunculus glacialis. Plant Cell Environ 28:1123–1135. doi: 10.1111/j.1365-3040.2005.01350.x CrossRefGoogle Scholar
  142. Suetsugu N, Wada M (2007) Chloroplast photorelocation movement mediated by phototropin family proteins in green plants. Biol Chem 388:927–935. doi: 10.1515/BC.2007.118 PubMedCrossRefGoogle Scholar
  143. Suorsa M, Järvi S, Grieco M et al (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell 24:2934–2948. doi: 10.1105/tpc.112.097162 PubMedPubMedCentralCrossRefGoogle Scholar
  144. Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:53–60. doi: 10.1016/j.tplants.2010.10.001 PubMedCrossRefGoogle Scholar
  145. Takahashi S, Murata N (2008) How do environmental stresses accelerate photoinhibition? Trends Plant Sci 13:178–182. doi: 10.1016/j.tplants.2008.01.005 PubMedCrossRefGoogle Scholar
  146. Takahashi S, Bauwe H, Badger M (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair process and not acceleration of damage process in Arabidopsis thaliana. Plant Physiol 144:487–494. doi: 10.1104/pp.107.097253 PubMedPubMedCentralCrossRefGoogle Scholar
  147. Takahashi S, Milward SE, Fan DY, Chow WS, Badger MR (2009) How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiol 149:1560–1567. doi: 10.1104/pp.108.134122 PubMedPubMedCentralCrossRefGoogle Scholar
  148. Terashima I, Funayama S, Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193:300–306. doi: 10.1007/BF00192544 CrossRefGoogle Scholar
  149. Terashima I, Araya T, Miyazawa SI, Sone K, Yano S (2005) Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: an eco-developmental treatise. Ann Bot 95:507–519. doi: 10.1093/aob/mci049 PubMedPubMedCentralCrossRefGoogle Scholar
  150. Tikkanen M, Aro EM (2012) Thylakoid protein phosphorylation in dynamic regulation of photosystem II in higher plants. Biochim Biophys Acta 1817:232–238. doi: 10.1016/j.bbabio.2011.05.005 PubMedCrossRefGoogle Scholar
  151. Tikkanen M, Grieco M, Kangasjärvi S, Aro EM (2010) Thylakoid protein phosphorylation in higher plant chloroplasts optimizes electron transfer under fluctuating light. Plant Physiol 152:723–735. doi: 10.1104/pp.109.150250 PubMedPubMedCentralCrossRefGoogle Scholar
  152. Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition-repair cycle protects photosystem I from irreversible damage. Biochim Biophys Acta 1837:210–215. doi: 10.1016/j.bbabio.2013.10.001 PubMedCrossRefGoogle Scholar
  153. Tikkanen M, Rantala S, Aro EM (2015) Electron flow from PSII to PSI under high light is controlled by PGR5 but not by PSBS. Front Plant Sci 6:521. doi: 10.3389/fpls.2015.00521 PubMedPubMedCentralCrossRefGoogle Scholar
  154. Timm HC, Küppers M, Stegemann J (2004) Non-destructive analysis of architectural expansion and assimilate allocation in different tropical tree saplings: consequences of using steady-state and dynamic photosynthesis models. Ecotropica 10:101–121Google Scholar
  155. Trouillard M, Shahbazi M, Moyet L, Rappaport F, Joliot P, Kuntz M, Finazzi G (2012) Kinetic properties and physiological role of the plastoquinone terminal oxidase (PTOX) in a vascular plant. Biochim Biophys Acta 1817:2140–2148. doi: 10.1016/j.bbabio.2012.08.006 PubMedCrossRefGoogle Scholar
  156. Valladares F, Allen MT, Pearcy RW (1997) Photosynthetic responses to dynamic light under field conditions in six tropical rainforest shrubs occurring along a light gradient. Oecologia 111:505–514. doi: 10.1007/s004420050264 CrossRefGoogle Scholar
  157. Wada M, Kagawa T, Sato Y (2003) Chloroplast movement. Annu Rev Plant Biol 54:455–468. doi: 10.1146/annurev.arplant.54.031902.135023 PubMedCrossRefGoogle Scholar
  158. Watling JR, Ball MC, Woodrow IE (1997) The utilization of lightflecks for growth in four Australian rain-forest species. Funct Ecol 11:231–239. doi: 10.1046/j.1365-2435.1997.00073.x CrossRefGoogle Scholar
  159. Way DA, Pearcy RW (2012) Sunflecks in trees and forests: from photosynthetic physiology to global change biology. Tree Physiol 32:1066–1081. doi: 10.1093/treephys/tps064 PubMedCrossRefGoogle Scholar
  160. Way DA, Yamori W (2014) Thermal acclimation of photosynthesis: on the importance of definitions and accounting for thermal acclimation of respiration. Photosynth Res 119:89–100. doi: 10.1007/s11120-013-9873-7 PubMedCrossRefGoogle Scholar
  161. Wise RR, Olson AJ, Schrader SM, Sharkey TD (2004) Electron transport is the functional limitation of photosynthesis in field-grown pima cotton plants at high temperature. Plant Cell Environ 27:717–724. doi: 10.1111/j.1365-3040.2004.01171.x CrossRefGoogle Scholar
  162. Yamamoto H, Shikanai T (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 288:36328–36337. doi: 10.1074/jbc.M113.511584 PubMedPubMedCentralCrossRefGoogle Scholar
  163. Yamamoto H, Peng L, Fukao Y, Shikanai T (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 23:1480–1493. doi: 10.1105/tpc.110.080291 PubMedPubMedCentralCrossRefGoogle Scholar
  164. Yamori W (2013) Improving photosynthesis to increase food and fuel production by biotechnological strategies in crops. J Plant Biochem Physiol 1:113. doi: 10.4172/2329-9029.1000113 Google Scholar
  165. Yamori W, Shikanai T (2016) Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annu Rev Plant Biol. doi: 10.1146/annurev-arplant-043015-112002 PubMedGoogle Scholar
  166. Yamori W, von Caemmerer S (2009) Effect of Rubisco activase deficiency on the temperature response of CO2 assimilation rate and Rubisco activation state: insights from transgenic tobacco with reduced amounts of Rubisco activase. Plant Physiol 151:2073–2082. doi: 10.1104/pp.109.146514 PubMedPubMedCentralCrossRefGoogle Scholar
  167. Yamori W, Noguchi K, Terashima I (2005) Temperature acclimation of photosynthesis in spinach leaves: analyses of photosynthetic components and temperature dependencies of photosynthetic partial reactions. Plant Cell Environ 28:536–547. doi: 10.1111/j.1365-3040.2004.01299.x CrossRefGoogle Scholar
  168. Yamori W, Suzuki K, Noguchi K, Nakai M, Terashima I (2006) Effects of Rubisco kinetics and Rubisco activation state on the temperature dependence of the photosynthetic rate in spinach leaves from contrasting growth temperatures. Plant Cell Environ 29:1659–1670. doi: 10.1111/j.1365-3040.2006.01550.x PubMedCrossRefGoogle Scholar
  169. Yamori W, Evans JR, von Caemmerer S (2010a) Effects of growth and measurement light intensities on temperature dependence of CO2 assimilation rate in tobacco leaves. Plant Cell Environ 33:332–343. doi: 10.1111/j.1365-3040.2009.02067.x PubMedCrossRefGoogle Scholar
  170. Yamori W, Noguchi K, Hikosaka K, Terashima I (2010b) Phenotypic plasticity in photosynthetic temperature acclimation among crop species with different cold tolerances. Plant Physiol 152:388–399. doi: 10.1104/pp.109.145862 PubMedPubMedCentralCrossRefGoogle Scholar
  171. Yamori W, Sakata N, Suzuki Y, Shikanai T, Makino A (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 68:966–976. doi: 10.1111/j.1365-313X.2011.04747.x PubMedCrossRefGoogle Scholar
  172. Yamori W, Masumoto C, Fukayama H, Makino A (2012) Rubisco activase is a key regulator of non steady-state photosynthesis at any leaf temperature and to a lesser extent, of steady-state photosynthesis at high temperature. Plant J 71:871–880. doi: 10.1111/j.1365-313X.2012.05041.x PubMedCrossRefGoogle Scholar
  173. Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4 and CAM plants: temperature acclimation and temperature adaptation. Photosynth Res 119:101–117. doi: 10.1007/s11120-013-9874-6 PubMedCrossRefGoogle Scholar
  174. Yamori W, Shikanai T, Makino A (2015) Photosystem I cyclic electron flow via chloroplast NADH dehydrogenease-like complex performs a physiological role for photosynthesis at low light. Sci Rep 5:13908. doi: 10.1038/srep13908 PubMedPubMedCentralCrossRefGoogle Scholar
  175. Yamori W, Makino A, Shikanai T (2016a) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep 6:20147. doi: 10.1038/srep20147 PubMedPubMedCentralCrossRefGoogle Scholar
  176. Yamori W, Kondo E, Sugiura D et al (2016b) 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. doi: 10.1111/pce.12594 PubMedCrossRefGoogle Scholar
  177. Yin ZH, Johnson GN (2000) Photosynthetic acclimation of higher plants to growth in fluctuating light environments. Photosynth Res 63:97–107. doi: 10.1023/A:1006303611365 PubMedCrossRefGoogle Scholar
  178. Zhu XG, Portis AR, Long SP (2004) Would transformation of C3 crop plants with foreign Rubisco increase productivity? A computational analysis extrapolating from kinetic properties to canopy photosynthesis. Plant Cell Environ 27:155–165. doi: 10.1046/j.1365-3040.2004.01142.x CrossRefGoogle Scholar
  179. Zhu XG, Long SP, Ort DR (2010) Improving photosynthetic efficiency for greater yield. Annu Rev Plant Biol 61:235–261. doi: 10.1146/annurev-arplant-042809-112206 PubMedCrossRefGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  1. 1.Department of Biological Sciences, Graduate School of ScienceThe University of TokyoTokyoJapan
  2. 2.Precursory Research for Embryonic Science and Technology (PRESTO), Japan Science and Technology Agency (JST)KawaguchiJapan

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