Photosynthesis Research

, Volume 113, Issue 1–3, pp 191–206 | Cite as

Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana

  • A. G. Ivanov
  • D. Rosso
  • L. V. Savitch
  • P. Stachula
  • M. Rosembert
  • G. Oquist
  • V. Hurry
  • N. P. A. Hüner
Regular Paper
First Online:
Received:
Accepted:

Abstract

Exposure of control (non-hardened) Arabidopsis leaves to high light stress at 5 °C resulted in a decrease of both photosystem II (PSII) (45 %) and Photosystem I (PSI) (35 %) photochemical efficiencies compared to non-treated plants. In contrast, cold-acclimated (CA) leaves exhibited only 35 and 22 % decrease of PSII and PSI photochemistry, respectively, under the same conditions. This was accompanied by an accelerated rate of P700+ re-reduction, indicating an up-regulation of PSI-dependent cyclic electron transport (CET). Interestingly, the expression of the NDH-H gene and the relative abundance of the Ndh-H polypeptide, representing the NDH-complex, decreased as a result of exposure to low temperatures. This indicates that the NDH-dependent CET pathway cannot be involved and the overall stimulation of CET in CA plants is due to up-regulation of the ferredoxin–plastoquinone reductase, antimycin A-sensitive CET pathway. The lower abundance of NDH complex also implies lower activity of the chlororespiratory pathway in CA plants, although the expression level and overall abundance of the other well-characterized component involved in chlororespiration, the plastid terminal oxidase (PTOX), was up-regulated at low temperatures. This suggests increased PTOX-mediated alternative electron flow to oxygen in plants exposed to low temperatures. Indeed, the estimated proportion of O2-dependent linear electron transport not utilized in carbon assimilation and not directed to photorespiration was twofold higher in CA Arabidopsis. The possible involvement of alternative electron transport pathways in inducing greater resistance of both PSII and PSI to high light stress in CA plants is discussed.

Keywords

Alternative electron flows Cold acclimation Photoprotection Photosystem II Photosystem I PTOX 
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Notes

Acknowledgments

This work was supported by the grants from the Swedish Foundation for International Cooperation in Research and Higher Education (G.Ö and N.P.A.H.), the Swedish Research Council (G.Ö.), the Natural Sciences and Engineering Research Council of Canada (N.P.A.H.), the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (V.H.) and Agriculture and Agri-Food Canada, Project ID #847 (L.V.S).

References

  1. Allen JF (1995) Thylakoid protein phosphorilation, state 1- state 2 transitions, and phosystem stoichiometry adjustment: redox control at multiple levels of gene expression. Physiol Plant 93:196–205CrossRefGoogle Scholar
  2. Aluru MR, Rodermel SR (2004) Control of chloroplast redox by the IMMUTANS terminal oxidase. Physiol Plant 120:4–11PubMedCrossRefGoogle Scholar
  3. Anderson JM (1986) Photoregulation of the composition, function and structure of thylakoid membranes. Annu Rev Plant Physiol 37:93–136CrossRefGoogle Scholar
  4. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134PubMedCrossRefGoogle Scholar
  5. 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 50:601–639PubMedCrossRefGoogle Scholar
  6. Asada K, Heber U, Schreiber U (1992) Pool size of electrons that can be donated to P700+, as determined in intact leaves: donation to P700+ from stromal components via the intersystem chain. Plant Cell Physiol 33:927–932Google Scholar
  7. Asada K, Heber U, Schreiber U (1993) Electron flow to the intersystem chain from stromal components and cyclic electron flow in maize chloroplasts, as determined in intact leaves by monitoring redox change of P700 and chlorophyll fluorescence. Plant Cell Physiol 34:39–50Google Scholar
  8. Baker NR (1994) Chilling stress and photosynthesis. In: Foyer CH, Mullineaux PM (eds) Causes of photooxidative stress and amelioration of defense system in plants. CRC Press, Boca Raton, pp 127–154Google Scholar
  9. Boese SR, Huner NPA (1992) Developmental history affects the susceptibility of spinach leaves to in vivo low temperature photoinhibition. Plant Physiol 99:1141–1145PubMedCrossRefGoogle Scholar
  10. Carol P, Kuntz M (2001) A plastid terminal oxidase comes to light: implications for carotenoid biosynthesis and chlororespiration. Trends Plant Sci 6:31–36PubMedCrossRefGoogle Scholar
  11. Cournac L, Josse E-M, Joët T, Rumeau D, Redding K, Kuntz M, Peltier G (2000a) Flexibility in photosynthetic electron transport: a newly identified chloroplast oxidase involved in chlororespiration. Phil Trans R Soc Lond B 355:1447–1454CrossRefGoogle Scholar
  12. Cournac L, Redding K, Ravenel J, Rumeau D, Josse E-M, Kuntz M, Peltier G (2000b) Electron flow between photosystem II and oxygen in chloroplasts of photosystem I-deficient algae is mediated by a quinol oxidase involved in chlororespiration. J Biol Chem 275:17256–17262PubMedCrossRefGoogle Scholar
  13. Dahal K, Kane K, Gadapati W, Webb E, Savitch LV, Singh J, Sharma P, Sarhan F, Longstaffe FJ, Grodzinski B, Hüner NPA (2012) The effects of phenotypic plasticity on photosynthetic performance in winter rye, winter wheat and Brassica napus. Physiol Plant 144:169–188PubMedCrossRefGoogle Scholar
  14. Demmig-Adams B (1990) Carotenoids and photoprotection: a role for the xanthophyll zeaxanthin. Biochim Biophys Acta 1020:1–24CrossRefGoogle Scholar
  15. Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626CrossRefGoogle Scholar
  16. Demmig-Adams B, Adams WW III (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21PubMedCrossRefGoogle Scholar
  17. Depege N, Bellafiore S, Rochaix J-D (2003) Role of chloroplast protein kinase Stt7 in LHCII phosphorylation and state transition in Chlamydomonas. Science 299:1572–1575PubMedCrossRefGoogle Scholar
  18. Diaz M, De Haro V, Munoz R, Quiles MJ (2007) Chlororespiration is involved in the adaptation of Brassica plants to heat and high light intensity. Plant Cell Environ 30:1578–1585PubMedCrossRefGoogle Scholar
  19. Farineau J (1999) Study of the non-photochemical dark rise in chlorophyll fluorescence in pre-illuminated leaves of various C3 and C4 plants submitted to partial anaerobiosis. Plant Physiol Biochem 37:911–918CrossRefGoogle Scholar
  20. Gilmore AM (1997) Mechanistic aspects of xanthophylls cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant 99:197–209CrossRefGoogle Scholar
  21. Gray GR, Boese SR, Huner NPA (1994) A comparison of low temperature growth versus low temperature shifts to induce resistance to photoinhibition in spinach (Spinacia oleracea). Physiol Plant 90:560–566CrossRefGoogle Scholar
  22. Gray GR, Savitch LV, Ivanov AG, Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. II. Adjustment of photosynthetic capacity in winter wheat and winter rye. Plant Physiol 110:61–71PubMedGoogle Scholar
  23. Gray GR, Ivanov AG, Król M, Huner NPA (1998) Adjustment of thylakoid plastoquinone content and photosystem I electron donor pool size in response to growth temperature and growth irradiance in winter rye (Secale cereale L.). Photosynth Res 56:209–221CrossRefGoogle Scholar
  24. Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305PubMedCrossRefGoogle Scholar
  25. Harrison MA, Melis A (1992) Organization and stability of polypeptides associated with the chlorophyll a–b light-harvesting complex of photosystem II. Plant Cell Physiol 33:627–637Google Scholar
  26. Hendrickson L, Furbank RT, Chow WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81PubMedCrossRefGoogle Scholar
  27. Hohmann-Marriott MF, Takizawa K, Eaton-Rye JJ, Mets L, Minagawa J (2010) The redox state of the plastoquinone pool directly modulates minimum chlorophyll fluorescence yield in Chlamydomonas reinhardtii. FEBS Lett 584:1021–1026PubMedCrossRefGoogle Scholar
  28. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684PubMedCrossRefGoogle Scholar
  29. Huner NPA, Öquist G, Hurry VM, Krol M, Falk S, Griffith M (1993) Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynth Res 37:19–39CrossRefGoogle Scholar
  30. Huner NPA, Maxwell DP, Gray GR, Savitch LV, Krol M, Ivanov AG, Falk S (1996) Sensing environmental change: PSII excitation pressure and redox signalling. Physiol Plant 98:358–364CrossRefGoogle Scholar
  31. Huner NPA, Öquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230CrossRefGoogle Scholar
  32. Hurry VM, Huner NPA (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
  33. Hurry VM, Gardeström P, Öquist G (1993) Reduced sensitivity to photoinhibition following frost-hardening of winter rye is due to increased phosphate availability. Planta 190:484–490CrossRefGoogle Scholar
  34. Hurry VM, Malmberg G, Gardeström P, Öquist G (1994) Effects of a short-term shift to low temperature and of long-term cold hardening on photosynthesis and ribulose 1,5-bisphosphate carboxylase/oxygenase and sucrose phosphate synthase activity in leaves of winter rye (Secale cereale L.). Plant Physiol 106:983–990PubMedGoogle Scholar
  35. Hurry VM, Strand A, Tobiaeson M, Gardeström P, Öquist G (1995) Cold hardening of spring and winter wheat and rape results in differential effects on growth, carbon metabolism, and carbohydrate content. Plant Physiol 109:697–706PubMedGoogle Scholar
  36. Ivanov AG, Krol M, Maxwell DP, Huner NPA (1995) Abscisic acid induced protection against photoinhibition of PSII correlates with enhanced activity of the xanthophyll cycle. FEBS Lett 371:61–64PubMedCrossRefGoogle Scholar
  37. Ivanov AG, Morgan RM, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance to photoinhibition of photosystem I. FEBS Lett 430:288–292PubMedCrossRefGoogle Scholar
  38. Ivanov AG, Sane PV, Zeinalov Y, Malmberg G, Gardeström P, Huner NPA, Öquist G (2001) Photosynthetic electron transport adjustments in overwintering Scots pine (Pinus sylvestris L.). Planta 213:575–585PubMedCrossRefGoogle Scholar
  39. Ivanov AG, Sane PV, Zeinalov Y, Simidjiev I, Huner NPA, Öquist G (2002) Seasonal responses of photosynthetic electron transport in Scots pine (Pinus sylvestris L.) studied by thermoluminescence. Planta 215:457–465PubMedCrossRefGoogle Scholar
  40. Ivanov AG, Sane P, Hurry V, Krol M, Sveshnikov D, Huner NPA, Öquist G (2003) Low-temperature modulation of the redox properties of the acceptor side of photosystem II: photoprotection through reaction centre quenching of excess energy. Physiol Plant 119:376–383CrossRefGoogle Scholar
  41. Ivanov AG, Hendrickson L, Krol M, Selstam E, Öquist G, Hurry V, Huner NPA (2006a) Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to photosystem I acceptor-side limitations. Plant Cell Physiol 47:1146–1157PubMedCrossRefGoogle Scholar
  42. Ivanov AG, Sane PV, Krol M, Gray GR, Balseris A, Savitch LV, Öquist G, Hüner NPA (2006b) Acclimation to temperature and irradiance modulates PSII charge recombination. FEBS Lett 580:2797–2802PubMedCrossRefGoogle Scholar
  43. Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NPA (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98:565–574PubMedCrossRefGoogle Scholar
  44. Ivanov AG, Allakhverdiev SI, Huner NPA, Murata N (2012) Genetic decrease in fatty acid unsaturation of phosphatidylglycerol increased photoinhibition of photosystem I at low temperature in tobacco leaves. Biochim Biophys Acta 1877:1374–1379Google Scholar
  45. Joët T, Genty B, Josse E-M, Kuntz M, Cournac L, Peltier G (2002) Involvement of a plastid terminal oxidase in plastoquinone oxidation as evidenced by expression of the Arabidopsis thaliana enzyme in tobacco. J Biol Chem 277:31623–31630PubMedCrossRefGoogle Scholar
  46. Josse E-M, Alcaraz J-P, Labouré A-M, Kuntz M (2003) In vitro characterization of a plastid terminal oxidase (PTOX). Eur J Biochem 270:3787–3794PubMedCrossRefGoogle Scholar
  47. Kim S-J, Lee C-H, Hope AB, Chow WS (2001) Inhibition of photosystems I and II and enhanced back flow of photosystem I electrons in cucmber leaf discs chilled in the light. Plant Cell Physiol 42:842–848PubMedCrossRefGoogle Scholar
  48. Kim J-H, Kim S-J, Cho SH, Chow WS, Lee C-H (2005) Photosystem I acceptor side limitation is a prerequisite for the reversible decrease in the maximum extent of P700 oxidation after short-term chilling in the light in four plant species with different chilling sensitivities. Physiol Plant 123:100–107CrossRefGoogle Scholar
  49. Klughammer C, Schreiber U (1991) Analysis of light-induced absorbency changes in the near-infrared spectral region. 1. Characterization of various components in isolated chloroplasts. Z Naturforsch C 46:233–244Google Scholar
  50. Krol M, Ivanov AG, Jansson S, Kloppstech K, Huner NPA (1999) Greening under high light or cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in wild-type barley and the chlorina f2 mutant. Plant Physiol 120:193–204PubMedCrossRefGoogle Scholar
  51. Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  52. Laisk A, Loreto F (1996) Determining photosynthetic parameters from leaf CO2 exchange and chlorophyll fluorescence. Ribulose-1,5-bisphosphate carboxylase/oxygenase specificity factor, dark respiration in the light, excitation distribution between photosystems, alternative electron transport rate, and mesophyll diffusion resistance. Plant Physiol 110:903–912PubMedGoogle Scholar
  53. Laureau C, Bligny R, Streb P (2011) The significance of glutathione for photoprotection at contrasting temperatures in the alpine plant species Soldanella alpina and Ranunculus glacialis. Physiol Plant 143:246–260PubMedCrossRefGoogle Scholar
  54. Li X-P, Björkman O, Shin C, Grossman A, Rosenquist M, Jansson S, Niyogi KK (2000) A pigment-binding protein essential for regulation of photosynthetic light harvesting. Nature 403:391–395PubMedCrossRefGoogle Scholar
  55. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–642CrossRefGoogle Scholar
  56. Loreto F, DiMarco G, Tricoli D, Sharkey TD (1994) Measurements of mesophyll conductance, photosynthetic electron transport and alternative electron sinks of field grown wheat leaves. Photosynth Res 41:397–403CrossRefGoogle Scholar
  57. Losciale P, Oguchi R, Hendrickson L, Hope AB, Corelli-Grappadelli L, Chow WS (2008) A rapid, whole-tissue determination of the functional fraction of PSII after photoinhibition of leaves based on flash-induced P700 redox kinetics. Physiol Plant 132:23–32PubMedGoogle Scholar
  58. Lovelock CE, Winter K (1996) Oxygen-dependent electron transport and protection from photoinhibition in leaves of tropical tree species. Planta 198:580–587CrossRefGoogle Scholar
  59. Lunde C, Jensen PE, Haldrup A, Knoetzel J, Scheller HV (2000) The PSI-H subunit of photosystem I is essential for state transitions in plant photosynthesis. Nature 408:613–615PubMedCrossRefGoogle Scholar
  60. Mano J, Miyake C, Schreiber U, Asada K (1995) Photoactivation of electron flow from NADPH to plastoquinone in spinach chloroplasts. Plant Cell Physiol 36:1589–1598Google Scholar
  61. Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by turnover of P700 in vivo. Biochemistry 15:3975–3981PubMedCrossRefGoogle Scholar
  62. Maxwell DP, Falk S, Huner NPA (1995) Photosystem II excitation pressure and development of resistance to photoinhibition: I. Light-harvesting complex II abundance and zeaxanthin content in Chlorella vulgaris. Plant Physiol 107:687–694PubMedGoogle Scholar
  63. McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Hüner NPA (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967PubMedCrossRefGoogle Scholar
  64. Munekage Y, Hoja M, Meurer J, Endo T, Tasaka M, Shikamai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371PubMedCrossRefGoogle Scholar
  65. Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767:414–421PubMedCrossRefGoogle Scholar
  66. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50:333–359PubMedCrossRefGoogle Scholar
  67. Öquist G, Huner NPA (1991) Effects of cold acclimation on the susceptibility of photosynthesis to photoinhibition in Scots pine and in winter and spring cereals: a fluorescence analysis. Funct Ecol 5:91–100CrossRefGoogle Scholar
  68. Öquist G, Huner NPA (1993) Cold-hardening induced resistance to photoinhibition in winter rye is dependent upon an increased capacity for photosynthesis. Planta 189:150–156CrossRefGoogle Scholar
  69. Öquist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355PubMedCrossRefGoogle Scholar
  70. Öquist G, Hurry VM, Huner NPA (1993) The temperature dependence of the redox state of Q A and the susceptibility of photosynthesis to photoinhibition. Plant Physiol Biochem 31:683–691Google Scholar
  71. Ort DR (2001) When there is too much light. Plant Physiol 125:29–32PubMedCrossRefGoogle Scholar
  72. Ort DR, Baker NR (2002) A photoprotective role for O2 as an alternative electron sink in photosynthesis? Curr Opin Plant Biol 5:193–198PubMedCrossRefGoogle Scholar
  73. Osmond B, Badger M, Maxwell K, Björkman O, Leegood R (1997) Too many photons: photorespiration, photoinhibition and photooxidation. Trends Plant Sci 2:119–121CrossRefGoogle Scholar
  74. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29:e45PubMedCrossRefGoogle Scholar
  75. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44CrossRefGoogle Scholar
  76. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66PubMedCrossRefGoogle Scholar
  77. Ravenel J, Peltier G, Havaux M (1994) The cyclic electron pathways around photosystem I in Chlamydomonas reinhardtii as determined in vivo by photoacoustic measurements of energy storage. Planta 193:251–259CrossRefGoogle Scholar
  78. Rosso D, Ivanov AG, Fu A, Geisler-Lee J, Hendrickson L, Geisler M, Stewart G, Krol M, Hurry V, Rodermel SR, Maxwell DP, Hüner NPA (2006) IMMUTANS does not act as a stress-induced safety valve in the protection of the photosynthetic apparatus of Arabidopsis thaliana during steady state photosynthesis. Plant Physiol 142:574–585PubMedCrossRefGoogle Scholar
  79. Rosso D, Bode R, Li W, Krol M, Saccon D, Wang S, Schillaci LA, Rodermel SR, Maxwell DP, Hüner NPA (2009) Photosynthetic redox imbalance governs leaf sectoring in the Arabidopsis thaliana variegation mutants immutans, spotty, var1, and var2. Plant Cell 21:3473–3492PubMedCrossRefGoogle Scholar
  80. Rumeau D, Peltier G, Cournac L (2007) Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant Cell Environ 30:1041–1051PubMedCrossRefGoogle Scholar
  81. Sane PV, Ivanov AG, Hurry V, Huner NPA, Öquist G (2003) Changes in the redox potential of primary and secondary electron-accepting quinones in photosystem II confer increased resistance to photoinhibition in low-temperature-acclimated Arabidopsis. Plant Physiol 132:2144–2151PubMedCrossRefGoogle Scholar
  82. Savitch LV, Gray GR, Huner NPA (1997) Feedback-limited photosynthesis and regulation of sucrose-starch accumulation during cold acclimation and low-temperature stress in a spring and winter wheat. Planta 201:18–26CrossRefGoogle Scholar
  83. Savitch LV, Harney T, Huner NPA (2000a) Sucrose metabolism in spring and winter wheat in response to high irradiance, cold stress and cold acclimation. Physiol Plant 108:270–278CrossRefGoogle Scholar
  84. Savitch LV, Massacci A, Gray GR, Huner NPA (2000b) Acclimation to low temperature or high light mitigates sensitivity to photoinhibition: roles of the Calvin cycle and Mehler reaction. Aust J Plant Physiol 27:253–264Google Scholar
  85. Savitch LV, Barker-Åström J, Ivanov AG, Hurry V, Öquist G, Huner NPA, Gardeström P (2001) Cold acclimation of Arabidopsis thaliana results in incomplete recovery of photosynthetic capacity, associated with an increased reduction of the chloroplast stroma. Planta 214:295–303PubMedCrossRefGoogle Scholar
  86. Savitch LV, Ivanov AG, Gudynaite-Savitch L, Huner NPA, Simmonds J (2009) Effects of low temperature stress on excitation energy partitioning and photoprotection in Zea mays. Funct Plant Biol 36:37–49CrossRefGoogle Scholar
  87. Savitch LV, Ivanov AG, Krol M, Sprott DP, Öquist G, Huner NPA (2010) Regulation of energy partitioning and alternative electron transport pathways during cold acclimation of Lodgepole pine is oxygen dependent. Plant Cell Physiol 51:1555–1570PubMedCrossRefGoogle Scholar
  88. Savitch LV, Ivanov AG, Gudynaite-Savitch L, Huner NPA, Simmonds J (2011) Cold stress effects on PSI photochemistry in Zea mays: differential increase of FQR-dependent cyclic electron flow and functional implications. Plant Cell Physiol 52:1042–1054PubMedCrossRefGoogle Scholar
  89. Scheller H, Haldrup A (2005) Photoinhibition of photosystem I. Planta 221:5–8PubMedCrossRefGoogle Scholar
  90. Schreiber U, Shliwa W, Bilger U (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorimeter. Photosynth Res 10:51–62CrossRefGoogle Scholar
  91. Sonoike K (1996) Photoinhibition of photosystem I: its physiological significance in the chilling sensitivity of plants. Plant Cell Physiol 37:239–247CrossRefGoogle Scholar
  92. Sonoike K (1999) The different roles of chilling temperatures in the photoinhibition of photosystem I and photosystem II. J Photochem Photobiol B 48:136–141CrossRefGoogle Scholar
  93. Sonoike K, Kamo M, Hihara Y, Hiyama T, Enami I (1997) The mechanism of the degradation of PsaB gene product, one of the photosynthetic reaction centre subunits of photosystem I, upon photoinhibition. Photosynth Res 53:55–63CrossRefGoogle Scholar
  94. Stepien P, Johnson GN (2009) Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis thaliana and the halophyte Tellungiella halophila. Role of the plastid terminal oxidase as an alternative electron sink. Plant Physiol 149:1154–1165PubMedCrossRefGoogle Scholar
  95. Stitt M, Hurry V (2002) A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Curr Opin Plant Biol 5:199–206PubMedCrossRefGoogle Scholar
  96. Strand Å, Hurry V, Gustafsson P, Gardeström P (1997) Development of Arabidopsis thaliana leaves at low temperatures releases the suppression of photosynthesis and photosynthetic gene expression despite the accumulation of soluble carbohydrates. Plant J 12:605–614PubMedCrossRefGoogle Scholar
  97. Strand Å, Foyer CH, Gustafsson P, Gardeström P, Hurry V (2003) Altering flux through the sucrose biosynthesis pathway in transgenic Arabidopsis thaliana modifies photosynthetic acclimation at low temperatures and the development of freezing tolerance. Plant Cell Environ 26:523–535CrossRefGoogle Scholar
  98. Streb P, Cornic G (2012) Photosynthesis and antioxidant protection in alpine herbs. In: Lütz C (ed) Plants in alpine regions. Springer, Wien, pp 75–97CrossRefGoogle Scholar
  99. Streb P, Josse E-M, 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 28:1123–1135CrossRefGoogle Scholar
  100. Sveshnikov D, Ensminger I, Ivanov AG, Campbell D, Lloyd J, Funk C, Huner NPA, Öquist G (2006) Excitation energy partitioning and quenching during cold acclimation in Scots pine. Tree Physiol 26:325–336PubMedCrossRefGoogle Scholar
  101. 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 193:300–306CrossRefGoogle Scholar
  102. Thayer SS, Björkman O (1992) Carotenoid distribution and deepoxidation in thylakoid pigment-protein complexes from cotton leaves and bundle-sheath cells of maize. Photosynth Res 33:213–225CrossRefGoogle Scholar
  103. van Kooten O, Snel JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • A. G. Ivanov
    • 1
  • D. Rosso
    • 1
  • L. V. Savitch
    • 2
  • P. Stachula
    • 3
  • M. Rosembert
    • 2
  • G. Oquist
    • 3
  • V. Hurry
    • 3
  • N. P. A. Hüner
    • 1
  1. 1.Department of BiologyWestern UniversityLondonCanada
  2. 2.Agriculture and Agri-Food CanadaEastern Cereal and Oilseed Research CentreOttawaCanada
  3. 3.Umeå Plant Science Centre, Department of Plant PhysiologyUmeå UniversityUmeåSweden

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