Advertisement

Photosynthesis pp 275-297 | Cite as

Photosynthetic Responses of Plants to Excess Light: Mechanisms and Conditions for Photoinhibition, Excess Energy Dissipation and Repair

  • Yagut Allahverdiyeva
  • Eva-Mari Aro
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 34)

Summary

Plants as sessile organisms must be capable of rapidly coping with changes in environmental conditions. In nature light is the most variable environmental parameter. During the day, plants must deal with changes of several orders of magnitude in the light quantity but also changes in light quality take place. Light is an absolute prerequisite for photosynthesis as an energy source; however, excess light can also be harmful and lead to a destruction of the photosynthetic apparatus. Photoinhibition of photosynthesis has been defined as a light-dependent decline in photosynthetic efficiency as a result of absorption of light. However, a strong consensus is still missing concerning the term photoinhibition and whether it describes a decrease in photosynthetic efficiency due to photodamage and thereby a reduction in the population of functional photosystems or regulatory adjustments, like reduced energy transfer from the antenna to reaction centers or both of these processes. Diurnal photoinhibition is a common phenomenon in most plants exposed to direct sunlight. Depending on the season and also on the diurnal cycle, plants have developed various adaptation systems to cope with highly, as well as frequently, changing light intensity and quality. Although a number of mechanisms have evolved to dissipate excess absorbed light energy by harmless pathways, the photosynthetic apparatus still remains a fragile system and vulnerable to damage by light. This chapter describes briefly the mechanisms of photoinhibition and plant response to light stress. In this chapter, we have used the term photoinhibition to describe the process that finally leads to a photodamage and repair of the reaction centers, while the dissipative regulatory processes are regarded as sole photoprotective processes.

Keywords

Thylakoid Membrane Photosynthetic Apparatus Cyclic Electron Transport Plastoquinone Pool Repair Cycle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations:

Cyt –

Cytochrome;

ELIP –

Early light-induced protein;

LHCI –

Light-harvesting complex of PS I;

LHCII –

Light-harvesting complex of PS II;

NPQ –

Non-photochemical quenching;

PAR –

Photosynthetically active radiation;

PS I –

Photosystem I;

PS II –

Photosystem II;

ROS –

Reactive ­oxygen species;

SOD –

Superoxide dismutase; Viol – violaxanthin; Zea – zeaxanthin

Notes

Acknowledgements

Research in our laboratory is financially supported by Academy of Finland. We would like to thank Dr. Marja Hakala for critical reading of this manuscript and for her helpful comments.

References

  1. Adams WW III, Hoehn A and Demmig-Adams B (1995) Chilling temperatures and the xanthophyll cycle. A comparison of warm-grown and overwintering spinach. Aust J Plant Physiol 22: 75–85CrossRefGoogle Scholar
  2. Adamska I (1997) ELIPs - light-induced stress proteins. Physiol Plant 100: 794–805CrossRefGoogle Scholar
  3. Adamska I, Kruse E and Kloppstech K (2001) Stable insertion of the early light-induced proteins into etioplast membranes requires chlorophyll-a. J Biol Chem 276: 8582–8587PubMedCrossRefGoogle Scholar
  4. Adir N, Zer H, Shochat S and Ohad I (2003) Photoinhibition – a historical perspective. Photosynth Res 76: 343–370PubMedCrossRefGoogle Scholar
  5. Allahverdiyeva Y, Deak Z, Szilard A, Diner B, Nixon P and Vass I (2004) The function of D1-H332 in photosystem II electron transport studied by thermoluminescence and chlorophyll fluorescence in site-directed mutants of Synechocystis 6803. Eur J Biochem 271: 3523–3532PubMedCrossRefGoogle Scholar
  6. Allahverdiyeva Y, Mamedov F, Maenpaa P, Vass I and Aro EM (2005) Modulation of photosynthetic electron transport in the absence of terminal electron acceptors: characterization of the rbcL deletion mutant of tobacco. Biochim Biophys Acta 1709: 69–83PubMedCrossRefGoogle Scholar
  7. Allen DJ and Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6: 36–42PubMedCrossRefGoogle Scholar
  8. Allen JF (2003) State transitions - a question of balance. Science 299: 1530–1532PubMedCrossRefGoogle Scholar
  9. Allen JF and Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends Plant Sci 6: 317–326PubMedCrossRefGoogle Scholar
  10. Amunts A, Drory O and Nelson N (2007) The structure of a plant photosystem I supercomplex at 3.4  Å resolution. Nature 447: 58–63PubMedCrossRefGoogle Scholar
  11. Anderson J, Park YI and Chow WS (1998) Unifying model for the photoinactivation of photosystem II in vivo and steady-state photosynthesis. Photosynth Res 56: 1–13CrossRefGoogle Scholar
  12. Andersson B and Aro EM (2001) Photodamage and D1 ­protein turnover in photosystem II. In: Aro EM and Andersson B (eds) Regulation of photosynthesis, Advances in Photosynthesis and Respiration, Vol 11, pp 377–393. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  13. Andersson B and Barber J (1996) Mechanisms of photodamage and protein degradation during photoinhibition of photosystem II. In: Baker NR (ed) Photosynthesis and the Environment, Advances in Photosynthesis, Vol 5, pp 101–121. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  14. Andersson B and Styring S (1991) Photosystem II: molecular organization, function, and acclimation. Curr Top Bioenerg 16: 1–81CrossRefGoogle Scholar
  15. Aro EM, Tyystjärvi E and Nurmi A (1990) Temperature-dependent changes in photosystem II heterogeneity of attached leaves under high light. Physiol Plant 79: 585–592PubMedCrossRefGoogle Scholar
  16. Aro EM, Virgin I and Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143: 113–134PubMedCrossRefGoogle Scholar
  17. Aro EM, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N and Rintamaki E (2005) Dynamics of photosystem II: a proteomic approach to thylakoid protein complexes. J Exp Bot 56: 347–356PubMedCrossRefGoogle Scholar
  18. Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50: 601–639PubMedCrossRefGoogle Scholar
  19. Bailey S, Silva P, Nixon P, Mullineaux C, Robinson C and Mann N (2001a) Auxiliary functions in photosynthesis: the role of the FtsH protease. Biochem Soc Trans 29: 455–459PubMedCrossRefGoogle Scholar
  20. Bailey S, Walters RG, Jansson S and Horton P (2001b) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213: 794–801PubMedCrossRefGoogle Scholar
  21. Bailey S, Thompson E, Nixon PJ, Horton P, Mullineaux CW, Robinson C and Mann NH (2002) A critical role for the Var2 FtsH homologue of Arabidopsis thaliana in the photosystem II repair cycle in vivo. J Biol Chem 277: 2006–2011PubMedCrossRefGoogle Scholar
  22. Ballottari M, Dall’Osto L, Morosinotto T and Bassi R (2007) Contrasting behavior of higher plant photosystem I and II antenna system during acclimation. J Biol Chem 282: 8947–8958PubMedCrossRefGoogle Scholar
  23. Barber J (2006) Photosystem II: an enzyme of global significance. Biochem Soc Trans 34: 619–631PubMedCrossRefGoogle Scholar
  24. Barber J and Andersson B (1992) Too much of a good thing – light can be bad for photosynthesis. Trends Biochem Sci 17: 61–66PubMedCrossRefGoogle Scholar
  25. Barth C and Krause GH (1999) Inhibition of photosystems I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress. Z Naturforsch 54c: 645–657Google Scholar
  26. Barth C, Krause GH and Winter K (2001) Responses of photosystem I compared with photosystem II to high-light stress in tropical shade and sun leaves. Plant Cell Environ 24: 163–176CrossRefGoogle Scholar
  27. Bellafiore S, Barneche F, Peltier G and Rochaix JD (2005) State transitions and light adaptation require chloroplast thylakoid protein kinase STN7. Nature 433: 892–895PubMedCrossRefGoogle Scholar
  28. Berry J and Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31: 491–543CrossRefGoogle Scholar
  29. Björkman O and Powles SB (1984) Inhibition of photosynthetic reactions under water stress: interaction with light level. Planta 161: 490–504CrossRefGoogle Scholar
  30. Bongi G and Long SP (1987) Light-dependent damage to photosynthesis in olive leaves during chilling and high temperature stress. Plant Cell Environ 10: 241–249Google Scholar
  31. Bukhov NG, Govindachary S, Rajagopal S, Joly D and Carpentier R (2004) Enhanced rates of P700 + dark-reduction in leaves of Cucumis sativus L. photoinhibited at chilling temperature. Planta 218: 852–861PubMedCrossRefGoogle Scholar
  32. Burrows PA, Sazanov LA, Svab Z, Maliga P and Nixon PJ (1998) Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. EMBO J 17: 868–876PubMedCrossRefGoogle Scholar
  33. Chaves MM (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–46CrossRefGoogle Scholar
  34. Chen GX, Kazimir J and Cheniae GM (1992) Photoinhibition of hydroxylamine-extracted photosystem II membranes: studies of the mechanism. Biochemistry 31:11072–11083PubMedCrossRefGoogle Scholar
  35. Chen M, Choi YD, Voytas DF and Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22: 303–313PubMedCrossRefGoogle Scholar
  36. Choi S, Jeong S, Jeong W, Kwon S, Chow W and Park Y (2002) Chloroplast Cu/Zn-superoxide dismutase is a highly sensitive site in cucumber leaves chilled in the light. Planta 216: 315–324PubMedCrossRefGoogle Scholar
  37. Chung SK and Jung J (1995) Inactivation of the acceptor side and degradation of the D1 protein of photosystem II by singlet oxygen photogenerated from the outside. Photochem Photobiol 61: 383–389CrossRefGoogle Scholar
  38. Clark RD, Hawkesford MJ, Coughlan SJ, Bennett J and Hind G (1984) Association of ferredoxin-NADP+ oxidoreductase with the chloroplast cytochrome b-f complex. FEBS Lett 174: 137–142CrossRefGoogle Scholar
  39. Cornic G (2000) Drought stress inhibits photosynthesis by decreasing stomatal aperture – not by affecting ATP synthesis. Trends in Plant Sci 5: 187–188CrossRefGoogle Scholar
  40. Cornic G and Briantais JM (1991) Partitioning of photosynthetic electron flow between CO2 and O2 reduction in a C3 leaf (Phaseolus vulgaris L.) at different CO2 concentrations and during drought stress. Planta 183: 178–184CrossRefGoogle Scholar
  41. Crafts-Brandner SJ, Van de Loo FJ and Salvucci ME (1997) The two forms of ribulose-1,5-bisphosphate carboxylase/oxygenase activase differ in sensitivity to elevated temperature. Plant Physiol 114: 439–444PubMedGoogle Scholar
  42. Danielius RV, Satoh K, Van Kan PJM, Plijter JJ, Nuijs AM and Van Gorkom HJ (1987) The primary reaction of photosystem II in the D1-D2-cytochrome b-559 complex. FEBS Lett 213: 241–244CrossRefGoogle Scholar
  43. Debus RJ (2001) Amino acid residues that modulate the properties of tyrosine YZ and the manganese cluster in the water oxidizing complex of Photosystem II. Biochim Biophys Acta 1503: 164–186PubMedCrossRefGoogle Scholar
  44. Demmig-Adams B and Adams WW III (1996) The role of xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1: 21–26CrossRefGoogle Scholar
  45. Demmig-Adams B and Adams WW III (2003) Photoinhibtion. In: Thomas B, Murphy D and Murray B (eds) Encyclopedia of Applied Plant Science, pp 707–717. Academics Press, LondonGoogle Scholar
  46. Diner BA and Rappaport F (2002) Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol 53: 551–580PubMedCrossRefGoogle Scholar
  47. Durrant JR, Giorgi LB, Barber J, Klug DR and Porter G (1990) Characterization of triplet states in isolated photosystem II reaction centres: oxygen quenching as a mechanism for photodamage. Biochim Biophys Acta 1017: 167–175CrossRefGoogle Scholar
  48. Edge R and Truscott GT (1999) Carotenoid radicals and the interaction of carotenoids with active oxygen species. In: Frank HA, Young AJ, Britton G and Cogdell RJ (eds) The Photochemistry of Carotenoids, Advances in Photosynthesis, Vol 8, pp 223–234. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  49. Endo T, Shikanai T, Takabayashi A, Asada K and Sato F (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett 457: 5–8PubMedCrossRefGoogle Scholar
  50. Feller U, Crafts-Brandner SJ and Salvucci ME (1998) Moderately high temperatures inhibit ribulose-1,5-­bisphosphate carboxylase/oxygenase (Rubisco) activase-mediated activation of Rubisco. Plant Physiol 116: 539–546PubMedCrossRefGoogle Scholar
  51. Forsberg J, Strom J, Kieselbach T, Larsson H, Alexciev K, Engstrom A and Akerlund HE (2005) Protease activities in the chloroplast capable of cleaving an LHCII N-terminal peptide. Physiol Plant 123: 21–29CrossRefGoogle Scholar
  52. Flexas J and Medrano H (2002) Drought-inhibition of photosynthesis in C3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89: 183–189PubMedCrossRefGoogle Scholar
  53. Fufezan C, Gross CM, Sjodin M, Rutherford AW, Krieger-Liszkay A and Kirilovsky D (2007) Influence of the redox potential of the primary quinone electron acceptor on photoinhibition in photosystem II. J Biol Chem 282: 12492–12502PubMedCrossRefGoogle Scholar
  54. Garab G, Cseh Z, Kovacs L, Rajagopal S, Varkonyi Z, Wentworth M, Mustardy L, Der A, Ruban AV, Papp E, Holzenburg A and Horton P (2002) Light-induced trimer to monomer transition in the main light-harvesting antenna complex of plants: thermo-optic mechanism. Biochemistry 41: 15121–15129PubMedCrossRefGoogle Scholar
  55. Golding AJ and Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218: 107–114PubMedCrossRefGoogle Scholar
  56. Hakala M, Tuominen I, Keränen M, Tyystjärvi T and Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of Photosystem II. Biochim Biophys Acta 1706: 68–80PubMedCrossRefGoogle Scholar
  57. Haldrup A, Jensen PE, Lunde C and Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6: 301–305PubMedCrossRefGoogle Scholar
  58. Hankamer B, Morris E; Nield J, Gerle C and Barber J (2001) Three-dimensional structure of the photosystem II core dimer of higher plants determined by electron microscopy. J Struct Biol 135: 262–269PubMedCrossRefGoogle Scholar
  59. Haussuhl K, Andersson B and Adamska I (2001) A chloroplast DegP2 protease performs the primary cleavage of the photodamaged D1 protein in plant photosystem II. EMBO J 20: 713–722PubMedCrossRefGoogle Scholar
  60. Havaux M and Davaud A (1994) Photoinhibition of photosynthesis in chilled potato leaves is not correlated with a loss of photosystem-II activity. Photosynth Res 40: 75–92CrossRefGoogle Scholar
  61. Havaux M and Kloppstech K (2001) The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. Planta 213: 953–966CrossRefGoogle Scholar
  62. Havaux M and Tardy F (1996) Temperature-dependent adjustment of the thermal stability of photosystem II in vivo: possible involvement of xanthophyll-cycle pigments. Planta 198: 324–333CrossRefGoogle Scholar
  63. Havaux M, Dall’Osto L, Cuine S, Giuliano G and Bassi R (2004) The effect of zeaxanthin as the only xanthophyll on the structure and function of the photosynthetic apparatus in Arabidopsis thaliana. J Biol Chem 279: 13878–13888PubMedCrossRefGoogle Scholar
  64. Heddad M, Noren H, Reiser V, Dunaeva M, Andersson B and Adamska I (2006) Differential expression and localization of early light-induced proteins in Arabidopsis. Plant Physiol 142: 75–87PubMedCrossRefGoogle Scholar
  65. Herrig R and Falkowski PG (1989) Nitrogen limitation in Isochrysis galbana (Haptophyceae). I. Photosynthetic energy conversion and growth efficiencies. J Phycol 25: 462–471CrossRefGoogle Scholar
  66. Hideg E and Vass I (1995) Singlet oxygen is not produced in photosystem I under photoinhibitory conditions. Photochem Photobiol 62: 949–952CrossRefGoogle Scholar
  67. Hideg E, Kalai T, Hideg K and Vass I (2000) Do oxidative stress conditions impairing photosynthesis in the light manifest as photoinhibition? Philos Trans R Soc Lond B Biol Sci 355: 1511–1516PubMedCrossRefGoogle Scholar
  68. Holt NE, Fleming GR and Niyogi KK (2004) Toward an understanding of the mechanism of nonphotochemical quenching in green plants. Biochemistry 43: 8281–8289PubMedCrossRefGoogle Scholar
  69. Huesgen PF, Schuhmann H and Adamska I (2006) Photodamaged D1 protein is degraded in Arabidopsis mutants lacking the Deg2 protease. FEBS Lett 580: 6929–6932PubMedCrossRefGoogle Scholar
  70. Huner NPA, Öquist G and Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3: 224–230CrossRefGoogle Scholar
  71. Hurry VM and Huner NP (1992) Effect of cold hardening on sensitivity of winter and spring wheat leaves to short-term photoinhibition and recovery of photosynthesis. Plant Physiol 100: 1283–1290PubMedCrossRefGoogle Scholar
  72. Hwang HJ, Kim JH, Eu YJ, Moon BY, Cho SH and Lee CH (2004) Photoinhibition of photosystem I is accelerated by dimethyldithiocarbamate, an inhibitor of superoxide dismutase, during light-chilling of spinach leaves. J Photochem Photobiol B: Biol 73: 79–85CrossRefGoogle Scholar
  73. Itzhaki H, Naveh L, Lindahl M, Cook M and Adam Z (1998) Identification and characterization of DegP, a serine protease associated with the lumenal side of the thylakoid membrane. J Biol Chem 273: 7094–7098PubMedCrossRefGoogle Scholar
  74. Ivanov AG, Morgan RM, Gray GR, Velitchkova MY and Huner NP (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430: 288–292PubMedCrossRefGoogle Scholar
  75. Iwai M, Takizawa K, Tokutsu R, Okamura A, Takahashi Y and Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464: 1210–1213Google Scholar
  76. Jegerschold C, Virgin I and Styring S (1990) Light-dependent degradation of the D1 protein in photosystem II is accelerated after inhibition of the water splitting reaction. Biochemistry 29: 6179–6186PubMedCrossRefGoogle Scholar
  77. Jegerschold C and Styring S (1996) Spectroscopic characteri­zation of intermediate steps involved in donor-side-induced photoinhibition of photosystem II. Biochemistry 35: 7794–7801PubMedCrossRefGoogle Scholar
  78. Joliot P, Joliot A (2006) Quantification of cyclic and linear flows in plants. Proc Natl Acad Sci USA 102: 4913–4918CrossRefGoogle Scholar
  79. Kanervo E, Suorsa M and Aro EM (2005) Functional flexibility and acclimation of the thylakoid membrane. Photochem Photobiol Sci 4: 1072–1080PubMedCrossRefGoogle Scholar
  80. Kapri-Pardes E, Naveh L and Adam Z (2007) The thylakoid lumen protease Deg1 is involved in the repair of photosystem II from photoinhibition in Arabidopsis. Plant Cell 19: 1039–1047PubMedCrossRefGoogle Scholar
  81. Keren N, Gong H and Ohad I (1995) Oscillations of reaction center II-D1 protein degradation in vivo induced by repetitive flashes. Correlation between the level of RCII-QB- and protein degradation in low light. J Biol Chem 270: 806–814PubMedCrossRefGoogle Scholar
  82. Kingston-Smith AH, Harbinson J, Williams J and Foyer CH (1997) Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leaves. Plant Physiol 114: 1039–1046PubMedGoogle Scholar
  83. Koivuniemi A, Swiezewska E, Aro EM, Styring S and Andersson B (1993) Reduced content of the quinone acceptor QA in photosystem II complexes isolated from thylakoid membranes after prolonged photoinhibition under anaerobic conditions. FEBS Lett 327: 343–346PubMedCrossRefGoogle Scholar
  84. Koivuniemi A, Aro EM and Andersson B (1995) Degradation of the D1- and D2-proteins of photosystem II in higher plants is regulated by reversible phosphorylation. Biochemistry 34: 16022–16029PubMedCrossRefGoogle Scholar
  85. Kozaki A and Takeba G (1996) Photorespiration protects C3 plants from photooxidation. Nature 384: 557–560CrossRefGoogle Scholar
  86. Komayama K, Khatoon M, Takenaka D, Horie J, Yamashita A, Yoshioka M, Nakayama Y, Yoshida M, Ohira S, Morita N, Velitchkova M, Enami I and Yamamoto Y (2007) Quality control of photosystem II: cleavage and aggregation of heat-damaged D1 protein in spinach thylakoids. Biochim Biophys Acta 1767: 838–846PubMedCrossRefGoogle Scholar
  87. Kok B (1956) On the inhibition of photosynthesis by intense light. Biochim Biophys Acta 21: 234–244PubMedCrossRefGoogle Scholar
  88. Krieger-Liszkay A and Rutherford AW (1998) Influence of herbicide binding on the redox potential of the quinone acceptor in photosystem II: relevance to photodamage and phytotoxicity. Biochemistry 37: 17339–17344PubMedCrossRefGoogle Scholar
  89. Krinsky NI (1979) Carotenoid protection against oxidation. Pure Appl Chem 51: 649–660CrossRefGoogle Scholar
  90. Kudoh H and 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: 541–548PubMedCrossRefGoogle Scholar
  91. Kulheim C, Agren J and Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297: 91–93PubMedCrossRefGoogle Scholar
  92. Law RD and Crafts-Brandner SJ (1999) Inhibition and acclimation of photosynthesis to heat stress is closely correlated with activation of rubilose-1,5-bisphosphate carboxylase/oxygenase. Plant Physiol 120: 173–182PubMedCrossRefGoogle Scholar
  93. Li XP, Björkman O, Shih C, Grossman AR, Rosenquist M, Jansson S and Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403: 391–395PubMedCrossRefGoogle Scholar
  94. Lindahl M, Yang DH and Andersson B (1995) Regulatory proteolysis of the major light-harvesting chlorophyll a/b protein of photosystem II by a light induced membrane-associated enzymic system. Eur J Biochem 231: 503–509PubMedCrossRefGoogle Scholar
  95. Lindahl M, Tabak S, Cseke L, Pichersky E, Andersson B and Adam Z (1996) Identification, characterization, and molecular cloning of a homologue of the bacterial FtsH protease in chloroplasts of higher plants. J Biol Chem 271: 29329–29334PubMedCrossRefGoogle Scholar
  96. Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z and Andersson B (2000) The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 12: 419–431PubMedGoogle Scholar
  97. Loggini B, Scartazza A, Brugnoli E and Navari-Izzo F (1999) Antioxidative defense system, pigment composition, and photosynthetic efficiency in two wheat cultivars subjected to drought. Plant Physiol 119: 1091–1099PubMedCrossRefGoogle Scholar
  98. Long SP, Humphries S and Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45: 633–662CrossRefGoogle Scholar
  99. Matsubara S and Chow WS (2004) Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo. Proc Natl Acad Sci USA 101: 18234–18239PubMedCrossRefGoogle Scholar
  100. Medrano H, Escalona JM, Bota J, Gulias J and Flexas J (2002) Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. Ann Bot 89: 895–905PubMedCrossRefGoogle Scholar
  101. Mizusawa N, Tomo T, Satoh K and Miyao M (2003) Degradation of the D1 protein of photosystem II under illumination in vivo: Two different pathways involving cleavage or intermolecular cross-linking. Biochemistry 42: 10034–10044PubMedCrossRefGoogle Scholar
  102. Moon BY, Higashi S, Gombos Z and Murata N (1995) Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. Proc Natl Acad Sci USA 92: 6219–6223PubMedCrossRefGoogle Scholar
  103. Montane MH and Kloppstech K (2000) The family of light-harvesting-related proteins (LHCs, ELIPs, HLIPs): was the harvesting of light their primary function? Gene 258: 1–8PubMedCrossRefGoogle Scholar
  104. Miyake C, Yonekura K, Kobayashi Y and Yokota A (2002) Cyclic electron flow within PS II functions in intact chloroplasts from spinach leaves. Plant Cell Physiol 43: 951–957PubMedCrossRefGoogle Scholar
  105. Muller P, Li XP and Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125: 1558–1566PubMedCrossRefGoogle Scholar
  106. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M and Shikanai T (2002) PGR5 Is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110: 361–371PubMedCrossRefGoogle Scholar
  107. Murchie EH and Horton P (1997) Acclimation of photosynthesis to irradiance and spectral quality in British plant species: chlorophyll content, photosynthetic capacity and habitat preference. Plant Cell Environ 20: 438–448CrossRefGoogle Scholar
  108. Nakano R, Ishida H, Makino A and Mae T (2006) In vivo fragmentation of the large subunit of Ribulose-1,5-bisphosphate carboxylase by reactive oxygen species in an intact leaf of cucumber under chilling-light conditions. Plant Cell Physiol 47: 270–276PubMedCrossRefGoogle Scholar
  109. Nelson N and Yocum CF (2006) Structure and function of photosystem I and II. Annu Rev Plant Biol 57: 521–565PubMedCrossRefGoogle Scholar
  110. Nixon PJ, Barker M, Boehm M, de Vries R and Komenda J (2005) FtsH-mediated repair of the photosystem II complex in response to light stress. J Exp Bot 56: 357–363PubMedCrossRefGoogle Scholar
  111. Nixon PJ, Michoux F, Yu J, Boehm M and Komenda J (2010) Recent advances in understanding the assembly and repair of photosystem II. Ann Bot 106: 1–16Google Scholar
  112. Niyogi KK, Li XP, Rosenberg V and Jung HS (2005) Is PsbS the site of non-photochemical quenching in photosynthesis? J Exp Bot 56: 375–382PubMedCrossRefGoogle Scholar
  113. Ohad I, Kyle DJ and Arntzen CJ (1984) Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptide in chloroplast membranes. J Cell Biol 99: 481–485PubMedCrossRefGoogle Scholar
  114. Ohad I, Adir N, Koike H, Kyle DJ and Inoue Y (1990) Mechanism of photoinhibition in vivo. A reversible light-induced conformational change of reaction center II is related to an irreversible modification of the D1 protein. J Biol Chem 265: 1972–1979PubMedGoogle Scholar
  115. Ohira S, Morita N, Suh HJ, Jung J and Yamamoto Y (2005) Quality control of photosystem II under light stress - turnover of aggregates of the D1 protein in vivo. Photosynth Res 84: 29–33PubMedCrossRefGoogle Scholar
  116. Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y and Murata N (2005) Two-step mechanism of photodamage to photosystem II: step 1 occurs at the oxygen-evolving complex and step 2 occurs at the photochemical reaction center. Biochemistry 44: 8494–8499PubMedCrossRefGoogle Scholar
  117. Ortega JM, Roncel M and Losada M (1999) Light-induced degradation of cytochrome b 559 during photoinhibition of the photosystem II reaction center. FEBS Lett 458: 87–92PubMedCrossRefGoogle Scholar
  118. Osmond CB (1981) Photorespiration and photoinhibition. Some implications for the energetics of photosynthesis. Biochim Biophys Acta 639: 77–98CrossRefGoogle Scholar
  119. Osmond B, Badger M, Maxwell K, Björkman O and Leegood R (1997) Too many photons: photorespiration, photoinhibition and photooxidation. Trends Plant Sci 2: 119–121CrossRefGoogle Scholar
  120. Osmond B and Förster B (2005) Photoinhibition: Then and now. In: Demmig-Adams B, Adams WW III and Mattoa AK (eds) Photoprotection, Photoinhibition, Gene Regulation, and Environment, Advances in Photosynthesis and Respiration, Vol 21, pp 11–22. Springer, DordrechtCrossRefGoogle Scholar
  121. Ott T, Clarke J, Birks K and Johnson G (1999) Regulation of the photosynthetic electron transport chain. Planta 209: 250–258PubMedCrossRefGoogle Scholar
  122. Oquist G, Hurry VM and Huner NPA (1993) The temperature dependence of the redox state of QA and the susceptibility of photosynthesis to photoinhibition. Plant Physiol Biochem 31: 683–691Google Scholar
  123. Park YII, Chow WS, Osmond CB and Anderson JM (1996) Electron transport to oxygen mitigates against the photoinactivation of photosystem II in vivo. Photosynth Res 50: 23–31CrossRefGoogle Scholar
  124. Peltier JB, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Soderberg L, Roepstorff P, von Heijne G and Van Wijk KJ (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14: 211–236PubMedCrossRefGoogle Scholar
  125. Peng L and Shikanai T (2011) Supercomplex formation with photosystem I is required for the stabilization of the chloroplast NADH dehydrogenase-like complex in Arabidopsis. Plant Physiol 155: 1629–1639Google Scholar
  126. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35: 15–44CrossRefGoogle Scholar
  127. Rajagopal S, Bukhov NG, Tajmir-Riahi HA and Carpentier R (2003) Control of energy dissipation and photochemical activity in photosystem I by NADP-dependent reversible conformational changes. Biochemistry 42: 11839–11845PubMedCrossRefGoogle Scholar
  128. Rappaport F, Guergova-Kuras M, Nixon PJ, Diner BA and Lavergne J (2002) Kinetics and pathways of charge recombination in Photosystem II. Biochemistry 41: 8518–8527PubMedCrossRefGoogle Scholar
  129. Renger G (2011) light induced oxidative water splitting in photosynthesis: Energetics, kinetics and mechanism. J Photochem Photobiol B: Biol 104: 35–43Google Scholar
  130. Renger G and Renger T (2008) Photosystem II: the machinery of photosynthetic water splitting. Photosynth Res 98: 53–80Google Scholar
  131. Rintamaki E, Kettunen R and Aro EM (1996) Differential D1 dephosphorylation in functional and photodamaged photosystem II centers. Dephosphorylation is a prerequisite for degradation of damaged D1. J Biol Chem 271: 14870–14875PubMedCrossRefGoogle Scholar
  132. Rokka A, Suorsa M, Saleem A, Battchikova N and Aro EM (2005) Synthesis and assembly of thylakoid protein complexes: multiple assembly steps of photosystem II. Biochem J 388: 159–168PubMedCrossRefGoogle Scholar
  133. Rutherford AW and Krieger-Liszkay A (2001) Herbicide-induced oxidative stress in photosystem II. Trends Biochem Sci 26: 648–653PubMedCrossRefGoogle Scholar
  134. Sakamoto W (2006) Protein degradation machineries in plastids. Annu Rev Plant Biol 57: 599–621PubMedCrossRefGoogle Scholar
  135. Sakamoto W, Tamura T, Hanba-Tomita Y, Sodmergen and Murata M (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7: 769–780Google Scholar
  136. Sakamoto W, Zaltsman A, Adam Z and Takahashi Y (2003) Coordinated regulation and complex formation of yellow variegated1 and yellow variegated2, chloroplastic FtsH metalloproteases involved in the repair cycle of photosystem II in Arabidopsis thylakoid membranes. Plant Cell 15: 2843–2855PubMedCrossRefGoogle Scholar
  137. Salonen M, Aro EM and Rintamäki E (1998) Reversible phosphorylation and turnover of the D1 protein under various redox states of photosystem II induced by low temperature photoinhibition. Photosynth Res 58: 143–151CrossRefGoogle Scholar
  138. Satoh K (1970) Mechanism of photoinactivation in photosynthetic systems III. Site and mode of photoinactivation in photosystem I. Plant Cell Physiol 11: 187–197Google Scholar
  139. Satoh K and Fork DC (1982) Photoinhibition of reaction centers of photosystem I and II in intact Bryopsis chloroplasts under anaerobic conditions. Plant Physiol 70: 1004–1008PubMedCrossRefGoogle Scholar
  140. Scheller HV and Haldrup A (2005) Photoinhibition of photosystem I. Planta 221: 5–8PubMedCrossRefGoogle Scholar
  141. Schubert M, Petersson UA, Haas BJ, Funk C, Schroder WP and Kieselbach T (2002) Proteome map of the chloroplast lumen of Arabidopsis thaliana. J Biol Chem 277: 8354–8365PubMedCrossRefGoogle Scholar
  142. Seemann JR, Sharkey TD, Wang J and Osmond CB (1987) Environmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. Plant Physiol 84: 796–802PubMedCrossRefGoogle Scholar
  143. Silva P, Thompson E, Bailey S, Kruse O, Mullineaux CW, Robinson C, Mann NH and Nixon PJ (2003) FtsH is involved in the early stages of repair of photosystem II in Synechocystis sp. PCC 6803. Plant Cell 15: 2152–2164PubMedCrossRefGoogle Scholar
  144. Sonoike K (1996) Photoinhihition of photosystem I: Its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37: 239–247CrossRefGoogle Scholar
  145. Sonoike K and Terashima I (1994) Mechanism of photosystem-I photoinhibition in leaves of Cucumis sativus L. Planta 194: 287–293CrossRefGoogle Scholar
  146. Sonoike K, Terashima I, Iwaki M and Itoh S (1995) Destruction of photosystem I iron-sulfur centers in leaves of Cucumis sativus L. by weak illumination at chilling temperatures. FEBS Lett 362: 235–238PubMedCrossRefGoogle Scholar
  147. Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K and Yokota A (1998) Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proc Natl Acad Sci USA 95: 9705–9709PubMedCrossRefGoogle Scholar
  148. Stitt M (1986) Limitation of photosynthesis by carbon metabolism: I. Evidence for excess electron transport capacity in leaves carrying out photosynthesis in saturating light and CO2. Plant Physiol 81: 1115–1122PubMedCrossRefGoogle Scholar
  149. Styring S and Jegerschöld C (1994) Light-induced reactions impairing electron transfer through photosystem II. In: Baker NR and Bowyer J (eds) Photoinhibition of Photosynthesis; from Molecular Mechanisms to the Field, pp 51–74. BIOS Scientific Publishers, OxfordGoogle Scholar
  150. Sun ZL, Lee HY, Matsubara S, Hope AB, Pogson BJ, Hong YN and Chow WS (2006) Photoprotection of residual functional photosystem II units that survive illumination in the absence of repair, and their critical role in subsequent recovery. Physiol Plant 128: 415–424CrossRefGoogle Scholar
  151. Takahashi S and Murata N (2006) Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. Biochim Biophys Acta 1757: 198–205PubMedCrossRefGoogle Scholar
  152. Takahashi S, Bauwe H and Badger M (2007) Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol 144: 487–494PubMedCrossRefGoogle Scholar
  153. Teardo E, de Laureto PP, Bergantino E, Dalla Vecchia F, Rigoni F, Szabo I and Giacometti GM (2007) Evidences for interaction of PsbS with photosynthetic complexes in maize thylakoids. Biochim Biophys Acta 1767: 703–711PubMedCrossRefGoogle Scholar
  154. Teicher HB, Møller BL and Scheller HV (2000) Photoinhibition of photosystem I in field-grown barley (Hordeum vulgare L.): Induction, recovery and acclimation. Photosynth Res 64: 53–61CrossRefGoogle Scholar
  155. Terashima I, Sonoike K, Kawazu T and Katoh S (1991) Exposure of leaves of Cucumis sativus L. to low temperatures in the light causes uncoupling of thylakoids II. Non-destructive measurements with intact leaves. Plant Cell Physiol 32: 1275–1283Google Scholar
  156. Terashima I, Funayama S and Sonoike K (1994) The site of photoinhibition in leaves of Cucumis sativus L. at low temperatures is photosystem I, not photosystem II. Planta 193: 300–306CrossRefGoogle Scholar
  157. Tikkanen M, Piippo M, Suorsa M, Sirpiö S, Mulo P, Vainonen J, Vener AV, Allahverdiyeva Y and Aro EM (2006) State transitions revisited - a buffering system for dynamic low light acclimation of Arabidopsis. Plant Mol Biol 62: 779–793PubMedCrossRefGoogle Scholar
  158. Tjus SE, Moller BL and Scheller HV (1998) Photosystem I is an early target of photoinhibition in barley illuminated at chilling temperatures. Plant Physiol 116: 755–764PubMedCrossRefGoogle Scholar
  159. Tjus SE, Moller BL and Scheller HV (1999) Photoinhibition of photosystem I damages both reaction centre proteins PS I-A and PS I-B and acceptor-side located small photosystem I polypeptides. Photosynth Res 60: 75–86CrossRefGoogle Scholar
  160. Tjus SE, Scheller HV, Andersson B and Moller BL (2001) Active oxygen produced during selective excitation of photosystem I is damaging not only to photosystem I, but also to photosystem II. Plant Physiol 125: 2007–2015PubMedCrossRefGoogle Scholar
  161. Tourneux C and Peltier G (1995) Effect of water deficit on photosynthetic oxygen measured using 18O2 and mass spectrometry in Solanum tuberosum L. leaf discs. Planta 195: 570–577CrossRefGoogle Scholar
  162. Tyystjärvi E (2008) Photoinhibition of photosystem II and photodamage of the oxygen-evolving manganese cluster. Coord Chem Rev 252: 361–376Google Scholar
  163. Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. Physiol Plant 142: 6–16Google Scholar
  164. Vass I and Aro EM (2007) Photoinhibition of photosystem II electron transport. In: Renger G (ed) Primary Processes of Photosynthesis: Basic Principles and Apparatus. Comprehensive Series in Photochemical and Photobiological Sciences, pp 393–411. Royal Society Chemistry, CambridgeCrossRefGoogle Scholar
  165. Vass I, Styring S, Hundal T, Koivuniemi A, Aro E and Andersson B (1992) Reversible and irreversible intermediates during photoinhibition of photosystem II: Stable reduced QA species promote chlorophyll triplet formation. Proc Natl Acad Sci USA 89: 1408–1412PubMedCrossRefGoogle Scholar
  166. Wingler A, Lea PJ, Quick WP and Leegood RC (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos Trans R Soc Lond Ser B Biol Sci 355: 1517–1529CrossRefGoogle Scholar
  167. Weis E (1981) The temperature sensitivity of dark-inactivation and light-activation of the ribulose-1,5-bisphosphate carboxylase in spinach chloroplasts. FEBS Lett 129: 197–200CrossRefGoogle Scholar
  168. Wollman FA (2001) State transitions reveal the dynamics and flexibility of the photosynthetic apparatus. EMBO J 20: 3623–3630PubMedCrossRefGoogle Scholar
  169. Yamamoto Y (2001) Quality control of photosystem II. Plant Cell Physiol 42: 121–128PubMedCrossRefGoogle Scholar
  170. Yamamoto Y, Ishikawa Y, Nakatani E, Yamada M, Zhang H and Wydrzynski T (1998) Role of an extrinsic 33 kilodalton protein of photosystem II in the turnover of the reaction center-binding protein D1 during photoinhibition. Biochemistry 37: 1565–1574PubMedCrossRefGoogle Scholar
  171. Yang DH, Paulsen H and Andersson B (2000) The N-terminal domain of the light-harvesting chlorophyll a/b-binding protein complexes (LHCII) is essential for its acclimative proteolysis. FEBS Lett 466: 385–388PubMedCrossRefGoogle Scholar
  172. Yoshioka M and Yamamoto Y (2011) Quality control of photosystem II: Where and how does the degradation of the D1 protein by FtsH protease start under light stress? Facts and hypotheses. J Photochem Photobiol B: Biol 104: 229–235Google Scholar
  173. Zaltsman A, Feder A and Adam Z (2005a) Developmental and light effects on the accumulation of FtsH protease in Arabidopsis chloroplasts-implications for thylakoid formation and photosystem II maintenance. Plant J 42: 609–617PubMedCrossRefGoogle Scholar
  174. Zaltsman A, Ori N and Adam Z (2005b) Two types of FtsH protease subunits are required for chloroplast biogenesis and photosystem II repair in Arabidopsis. Plant Cell 17: 2782–2790PubMedCrossRefGoogle Scholar
  175. Zhang LX, Paakkarinen V, Van Wijk KJ and Aro EM (2000) Biogenesis of the chloroplast-encoded D1 protein: regulation of translation elongation, insertion, and assembly into photosystem II. Plant Cell 12: 1769–1782PubMedGoogle Scholar
  176. Zhang H, Whitelegge JP and Cramer WA (2001) Ferredoxin:NADP  +  oxidoreductase is a subunit of the chloroplast cytochrome b 6 f complex. J Biol Chem 276: 38159–38165PubMedGoogle Scholar
  177. Zhang S and Scheller HV (2004) Photoinhibition of ­photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. Plant Cell Physiol 45: 1595–1602PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.Laboratory of Plant Physiology and Molecular Biology, Biology DepartmentUniversity of TurkuTurkuFinland

Personalised recommendations