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Photosynthesis Research

, Volume 139, Issue 1–3, pp 367–385 | Cite as

Differential temperature effects on dissipation of excess light energy and energy partitioning in lut2 mutant of Arabidopsis thaliana under photoinhibitory conditions

  • Antoaneta V. PopovaEmail author
  • Konstantin Dobrev
  • Maya Velitchkova
  • Alexander G. Ivanov
Original Article
  • 129 Downloads

Abstract

The high-light-induced alterations in photosynthetic performance of photosystem II (PSII) and photosystem I (PSI) as well as effectiveness of dissipation of excessive absorbed light during illumination for different periods of time at room (22 °C) and low (8–10 °C) temperature of leaves of Arabidopsis thaliana, wt and lut2, were followed with the aim of unraveling the role of lutein in the process of photoinhibition. Photosynthetic parameters of PSII and PSI were determined on whole leaves by PAM fluorometer and oxygen evolving activity—by a Clark-type electrode. In thylakoid membranes, isolated from non-illuminated and illuminated for 4.5 h leaves of wt and lut2 the photochemical activity of PSII and PSI and energy interaction between the main pigment–protein complexes was determined. Results indicate that in non-illuminated leaves of lut2 the maximum rate of oxygen evolution and energy utilization in PSII is lower, excitation pressure of PSII is higher and cyclic electron transport around PSI is faster than in wt leaves. Under high-light illumination, lut2 leaves are more sensitive in respect to PSII performance and the extent of increase of excitation pressure of PSII, ΦNO, and cyclic electron transport around PSI are higher than in wt leaves, especially when illumination is performed at low temperature. Significant part of the excessive light energy is dissipated via mechanism, not dependent on ∆pH and to functioning of xanthophyll cycle in LHCII, operating more intensively in lut2 leaves.

Keywords

Arabidopsis thaliana lut2 mutant Photosynthetic performance High-light treatment Energy partitioning 

Abbreviations

BQ

1,4-Benzoquinone

CEF

Cyclic electron flow around PSI

DCMU

3-(3,4-dichlorophenyl)1,1-dimethyl urea

DCPIP

2,6-dichlorophenolindophenol

EDTA

Ethylenediamine-tetraacetic acid

ETR

Electron transport rate

Fo

Minimum yield of chlorophyll fluorescence in open PSII centers

Fm

Maximal chlorophyll fluorescence in dark-adapted state

\(F^{\prime}_{{\text{m}}}\)

Maximal chlorophyll fluorescence in light-adapted state

Fv

Variable chlorophyll fluorescence

ΦPSII

Effective quantum yield of PSII

ΦNPQ

Quantum yield of the regulated energy dissipation of PSII

ΦNO

Quantum yield of non-regulated energy dissipation of PSII

Fv/Fm

Maximum photochemical efficiency of PSII in the dark-adapted state

LCP

Light compensation point

LHCII

Light-harvesting chlorophyll a/b-protein complex of PSII

LHCI

Light-harvesting chlorophyll a/b-protein complex of PSI

MES

2(N-morpholino)ethanesulfonic acid

MV

Methyl viologen

NPQ

Non-photochemical quenching

P700

Reaction center chlorophyll of PSI

P700+

Oxidized form of PSI reaction center

PFD

Photon flux density

PQ

Plastoquinone

PSI

Photosystem I

PSII

Photosystem II

QA, QB

Primary and secondary electron-accepting quinone in PSII

TES

N-tris[hydroxymethyl]methyl-2-aminoethanesulfonic acid

TRICINE

N-tris[hydroxymethyl]methyl glycine

Notes

Acknowledgements

This work was partially supported by Bulgarian-Swiss Research Program, Project IZEBZO-143169/1. The seeds of the wt and mutant lut2 of A. thaliana were a generous gift from Prof. R. Bassi.

References

  1. Adams WW III, Zarter CR, Mueh KE, Amiard V, Demmig-Adams B (2008) Energy dissipation and photoinhibition: a continuum of photoprotection. In: Demmig-Adams B, Adams W, Mattoo A (eds) Photoprotection, photoinhibition, gene regulation, and environment, Springer, Dordrecht, pp 49–64Google Scholar
  2. Allen JF (1995) Thylakoid protein phosphorylation, state 1- state 2 transitions, and photosystem stoichiometry adjustment: redox control at multiple levels of gene expression. Physiol Plant 93:196–205Google Scholar
  3. Allen DJ, Ort DR (2001) Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends Plant Sci 6(1):36–42Google Scholar
  4. Andersson J (1981) Consequence of spatial separation of photosystem I and II in thylakoid membranes from higher plants chloroplasts. FEBS Lett 124:1–10Google Scholar
  5. Andrizhiyevskaya EG, Chojnicka A, Bautista JA, Diner BA, van Grondelle R, Dekker JP (2005) Origin of the F685 and F695 fluorescence in photosystem II. Photosynth Res 84:173–180Google Scholar
  6. Aro E-M, Virgin I, Andersson B (1993) Photoinhibition of photosystem II. Inactivation, protein damage and turnover. Biochim Biophys Acta 1143:113–134Google Scholar
  7. Baker NR, East TM, Long SP (1983) Chilling damage to photosynthesis in young Zea mays II. Photochemical function of thylakoids in vivo. J Exp Bot 34:189–197Google Scholar
  8. Barenyi B, Krause GH (1985) Inhibition of photosynthetic reactions by light. A study with isolated spinach chloroplasts. Planta 163:218–226Google Scholar
  9. Bassi R, Pineau B, Dainese P, Marquardt J (1993) Carotenoid binding proteins of photosystem II. Eur J Biochem 212:297–303Google Scholar
  10. Bravo LA, Saavedra-Mella FA, Vera F, Guerra A, Cavieres LA, Ivanov AG, Huner NPA, Corcuera LJ (2007) Effect of cold acclimation on the photosynthetic performance of two ecotypes of Colobanthus quitensis (Kunth) Bartl. J Exp Bot 58(13):3581–3590Google Scholar
  11. Brestic M, Zivcak M, Olsovska K, Shao H-B, Kalaji HM, Allakhverdiev SI (2014) Reduced glutamine synthetase activity plays a role in control of photosynthetic responses to high light in barley leaves. Plant Physiol Biochem 81:74–83Google Scholar
  12. Brestic M, Zivcak M, Kunderlikova K, Sytar O, Shao H, Kalaji H, Allakhverdiev SI (2015) Low PSI content limits the photoprotection of PSI and PSII in early growth stages of chlorophyll b-deficient wheat mutant lines. Photosynth Res 125:151–166Google Scholar
  13. Bruce D, Samson G, Carpenter C (1997) The origins of non-photochemical quenching of chlorophyll in photosynthesis. Direct quenching by P680(+) in photosystem II enriched membranes at low pH. Biochemistry 36:749–755Google Scholar
  14. Bukhov N, Egorova E, Carpentier R (2002) Electron flow to photosystem I from stromal reductants in vivo: the size of the pool of stromal reductants controls the rate of electron donation to both rapidly and slowly reducing photosystem I units. Planta 215:812–820Google Scholar
  15. Dall’Osto L, Lico C, Alric J, Giuliano G, Havaux M, Bassi R (2006) Lutein is needed for efficient chlorophyll triplet quenching in the major LHCII antenna complex of higher plants and effective photoprotection in vivo under strong light. MBC Plant Biol 6:32Google Scholar
  16. Dall’Osto L, Fiore A, Cazzaniga S, Giuliano G, Bassi R (2007) Different roles of α- and β-branch xanthophylls in photosystem assembly and photoprotection. J Biol Chem 282:35056–35068Google Scholar
  17. Dall’Osto L, Ünlü C, Cazzaniga S, van Amerongen H (2014) Disturbed excitation energy transfer in Arabidopsis thaliana mutants lacking antenna complexes of photosystem II. Biochim Biophys Acta 1837:1981–1988Google Scholar
  18. Dekker JP, Boekema EJ (2005) Supramolecular organization of thylakoid membrane proteins in green plants. Biochim Biophys Acta 1706:12–39Google Scholar
  19. Delrieu MJ (1998) Regulation of thermal dissipation of absorbed excitation energy and violaxanthin deepoxidation in the thylakoids of Lactuca sativa. Photoprotective mechanism of a population of photosystem II centers. Biochim Biophys Acta 1363:157–173Google Scholar
  20. Demming-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599–626Google Scholar
  21. Derks A, Schaven K, Bruce D (2015) Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. Biochim Biophys Acta 1847:468–485Google Scholar
  22. Dobrev K, Stanoeva D, Velitchkova M, Popova AV (2016) The lack of lutein accelerates the extent of light-induced bleaching of photosynthetic pigments in thylakoid membranes of Arabidopsis thaliana. Photochem Photobiol 92:436–445Google Scholar
  23. Endo T, Shikanai T, Takabayashi A, Asada K, Sato F (1999) The role of chloroplastic NAD(P)H dehydrogenase in photoprotection. FEBS Lett 457:5–8Google Scholar
  24. Fan D-Y, Hope AB, Jia H, Chow WS (2008) Separation of light-induced linear, cyclic and stroma-sourced electron fluxes to P700+ in cucumber leaf discs after pre-illumination at low temperature. Plant Cell Physiol 49:901–911Google Scholar
  25. Frank HA, Cogdell RJ (1996) Carotenoids in photosynthesis. Photochem Photobiol 63:257–264Google Scholar
  26. Genty B, Briantais J-M, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92Google Scholar
  27. Giersch C, Krause GH (1991) A simple model relating photoinhibitory fluorescence quenching in chloroplasts to a population of altered photosystem II reaction centers. Photosynth Res 30:115–121Google Scholar
  28. Gilmore AM (1997) Mechanistic aspects of xanthophylls cycle-dependent photoprotection in higher plant chloroplasts and leaves. Physiol Plant 99:197–209Google Scholar
  29. Gray GR, Savitch LV, Ivanov AG, Hüner 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 110:61–71Google Scholar
  30. Groce R, Weiss S, Bassi R (1999) Carotenoid-binding sites of the major light-harvesting complex II of higher plants. J Biol Chem 274:29613–29623Google Scholar
  31. Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E (2005) Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochim Biophys Acta 1706:68–80Google Scholar
  32. Haldrup A, Jensen PE, Lunde C, Scheller HV (2001) Balance of power: a view of the mechanism of photosynthetic state transitions. Trends Plant Sci 6:301–305Google Scholar
  33. Havaux M, Niyogi K (1999) The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 96:8762–8767Google Scholar
  34. Havaux M, DallÓsto L, Cuine S, Giuliano G, 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(14):13878–13888Google Scholar
  35. Hendrickson L, Furbank RT, Show WS (2004) A simple alternative approach to assessing the fate of absorbed light energy using chlorophyll fluorescence. Photosynth Res 82:73–81Google Scholar
  36. Horton P, Ruban A (1992) Regulation of photosystem II. Photosynth Res 34:375–385Google Scholar
  37. Horton P, Ruban AV, Walters RG (1996) Regulation of light harvesting in green plants. Annu Rev Plant Physiol Plant Mol Biol 47:655–684Google Scholar
  38. Huang H-Y, Zhang Q, Zhao LP, Feng J-N, Peng C-L (2010) Does lutein plays a key role in the protection of photosynthetic apparatus in Arabidopsis under severe oxidative stress? Pak J Bot 42:2765–2774Google Scholar
  39. Huang W, Yang YJ, Zhang SB (2017) Specific roles of cyclic electron flow around photosystem I in photosynthetic regulation in immature and mature leave. J Plant Physiol 209:76–83Google Scholar
  40. Hundal T, Virgin I, Stryng S, Andersson B (1990) Changes of the organization of photosystem II following light-induced D1-protein degradation. Biochim Biophys Acta 1017:235–241Google Scholar
  41. Huner NPA, Maxwell DP, Gray GR, Savich LV, Krol M, Ivanov AG, Falk S (1996) Sensing environmental change: PSII excitation pressure and redox signaling. Physiol Plant 98:358–364Google Scholar
  42. Huner NPA, Oquist G, Sarhan F (1998) Energy balance and acclimation to light and cold. Trends Plant Sci 3:224–230Google Scholar
  43. Ilioaia C, Johnson MP, Liao P-N, Pascal AA, van Grondelle R, Walla PJ, Ruban AV, Robert B (2011) Photoprotection in plants involves a change in lutein1 binding domain in the major light-harvesting complex of photosystem II. J Biol Chem 286:27247–27254Google Scholar
  44. Ivanov AG, Morgan R, Gray GR, Velitchkova MY, Huner NPA (1998) Temperature/light dependent development of selective resistance of photoinhibition of photosystem I. FEBS Lett 430:288–292Google Scholar
  45. 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 119:376–383Google Scholar
  46. Ivanov AG, Sane PV, Hurry V, Öquist G, Huner NPA (2008) Photosystem II reaction centre quenching: mechanisms and physiological role. Photosynth Res 98:565–574Google Scholar
  47. Ivanov AG, Rosso D, Savitch LV, Stachula P, Rosembert M, Oquist G, Hurry V, Huner NPA (2012) Implications of alternative electron sinks in increased resistance of PSII and PSI photochemistry to high light stress in cold-acclimated Arabidopsis thaliana. Photosynth Res 113:191–206Google Scholar
  48. Jahns P, Holzwarth AR (2012) The role of xanthophylls cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193Google Scholar
  49. Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochem Biophys Acta 1807:384–389Google Scholar
  50. Kalituho L, Rech J, Jahns P (2007) The roles of specific xanthophylls in light utilization. Planta 225:423–439Google Scholar
  51. 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
  52. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basis. Annu Rev Plant Physiol Plant Mol Biol 42:313–349Google Scholar
  53. Krieger-Liszkay A (2005) Singlet oxygen production in photosynthesis. J Exp Bot 56:337–346Google Scholar
  54. Laasch H (1987) Non-photochemical quenching of chlorophyll a fluorescence in isolated chloroplasts under conditions of stressed photosynthesis. Planta 171:220–225Google Scholar
  55. Laemmli U (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685Google Scholar
  56. Laisk A, Talts E, Oja V, Eichelmann H, Peterson RB (2010) Fast cyclic electron transport around photosystem I in leaves under far-red light: a proton-uncoupled pathway? Photosynth Res 103:79–95Google Scholar
  57. Lazarova D, Stanoeva D, Popova A, Vasilev D, Velitchkova M (2014) UV-B induced alteration of oxygen evolving reactions in pea thylakoid membranes as affected by scavengers of reactive oxygen species. Biol Plant 58:319–327Google Scholar
  58. Lee HY, Hong YN, Chow WS (2001) Photoinactivation of photosystem II complexes and photoprotection by non-functional neighbours in Capsicum annuum L. leaves. Planta 212:332–342Google Scholar
  59. Li Z, Ahn TK, Avenson TJ, Ballottari M, Cruz JA, Kramer DM, Bassi R, Fleming GR, Keasling JD, Niyogi KK (2009) Lutein accumulation in the absence of zeaxanthin restores nonphotochemical quenching in the Arabidopsis thaliana npq1 mutant. Plant Cell 21:1798–1812Google Scholar
  60. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382Google Scholar
  61. Lokstein H, Tian L, Polle J, DellaPenna D (2002) Xanthophyll biosynthetic mutants of Arabidopsis thaliana: altered nonphotochemical quenching of chlorophyll fluorescence is due to changes in photosystem II antenna size and stability. Biochim Biophys Acta 1553:309–319Google Scholar
  62. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–642Google Scholar
  63. Matsubara S, Chow W-S (2004) Populations of photoinactivated photosystem II reaction centers characterized by chlorophyll a fluorescence lifetime in vivo. Proc Natl Acad Sci USA 101:18234–18239Google Scholar
  64. Maxwell PC, Biggins J (1976) Role of cyclic electron transport in photosynthesis as measured by turnover of P700 in vivo. Biochemistry 15:3975–3981Google Scholar
  65. Melis A (1985) Functional properties of photosystem IIβ in spinach chloroplasts. Biochim Biophys Acta 808:334–342Google Scholar
  66. Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23:343–350Google Scholar
  67. Millaleo R, Reyes-Diaz M, Alberdi M, Ivanov AG, Krol M, Hunner NPA (2013) Excess manganese differentially inhibits photosystem I versus II in Arabidopsis thaliana. J Ex Bot 64(1):343–354Google Scholar
  68. 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 51:1951–1963Google Scholar
  69. Miyake C, Horiguchi S, Makino A, Shinzaki Y, Yamamoto H, Tomizawa K (2005) Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. Plant Cell Physiol 46:1819–1830Google Scholar
  70. Morosinotto T, Caffari S, DallOsto L, Bassi R (2003) Mechanistic aspects of the xanthophylls dynamics of higher plant thylakoids. Physiol Plant 119:347–354Google Scholar
  71. Moskalenko AA, Karapetyan NV (1996) Structural role of carotenoids in photosynthetic membranes. Z Naturforsch 51c:763–771Google Scholar
  72. Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T (2002) PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell 110:361–371Google Scholar
  73. Munekage Y, Hashimoto M, Miyake C, Tomizawa K, Endo T, Tasaka M, Shikanai T (2004) Cyclic electron flow around photosystem I is essential for photosynthesis. Nature 429:579–582Google Scholar
  74. Neale PJ, Melis A (1991) Dynamics of photosystem II heterogeneity during photoinhibition: depletion of PSIIβ from non-appressed thylakoids during strong irradiance exposure of Chlamydomonas reinhardtii. Biochim Biophys Acta 1056:195–203Google Scholar
  75. Niyogi KK (1999) Photoprotection revisited: genetic and molecular approaches. Rev Plant Physiol Plant Mol Biol 50:333–359Google Scholar
  76. Niyogi KK, Bjorkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 94:14162–14167Google Scholar
  77. Niyogi KK, Shih C, Chow WS, Pogson BJ, DellaPenna D, Bjoerkman O (2001) Photoprotection in a zeaxanthin- and lutein-deficient double mutant of Arabidopsis. Photosynth Res 67:139–145Google Scholar
  78. Öguist G, Huner NPA (2003) Photosynthesis of overwintering evergreen plants. Annu Rev Plant Biol 54:329–355Google Scholar
  79. Ohnishi N, Allakhverdiev SI, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, 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 44:8494–8499Google Scholar
  80. Ort DR (2001) When there is too much light. Plant Physiol 125:29–32Google Scholar
  81. Peng CL, Gilmore AM (2003) Contrasting changes of photosystem efficiency in Arabidopsis xanthophyll mutants at room or low temperature under high irradiance stress. Photosynthetica 41(2):233–239Google Scholar
  82. Peng CL, Lin Z-F, Su Y-Z, Lin G-Z, Dou H-Y, Zhao C-X (2006) The antioxidative function of lutein: electron spin resonance studies and chemical detection. Funct Plant Biol 33:839–846Google Scholar
  83. Peter GF, Thornber JP (1991) Biochemical composition and organization of higher plant photosystem II light-harvesting pigment-proteins. J Biol Chem 266:16745–16754Google Scholar
  84. Peterman ELG, Dukker FM, van Grondelle R, von Amerongen H (1995) Chlorophyll a and carotenoid triplet states in light-harvesting complex II of higher plants. Biophys J 69:2670–2678Google Scholar
  85. Plumley FG, Schmidt DW (1987) Reconstitution of chlorophyll a/b light-harvesting complexes: xanthophyll-dependent assembly and energy transfer. Proc Natl Acad Sci USA 84:146–150Google Scholar
  86. Pogson B, McDonald KA, Truong M, Britton G, DellaPenna D (1996) Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants. Plant Cell 8:1627–1639Google Scholar
  87. Popova AV, Velitchkova M, Zeinalov Y (2007) Effect of membrane fluidity on photosynthetic oxygen production reactions. Z Naturforsch 62c:253–260Google Scholar
  88. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15–44Google Scholar
  89. 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 193:251–259Google Scholar
  90. Rochaix J-D (2004) Genetics of the biogenesis and dynamics of the photosynthetic machinery in eukaryotes. Plant Cell 16:1650–1660Google Scholar
  91. 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 132:2144–2151Google Scholar
  92. 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 52:1042–1054Google Scholar
  93. Siefermann-Harms D (1985) Carotenoids in photosynthesis. I. Location in photosynthetic membranes and light-harvesting function. Biochim Biophys Acta 811:325–335Google Scholar
  94. Sonoike K (1998) Various aspects of inhibition of photosynthesis under light/chilling stress: “photoinhibition at chilling temperatures” versus “chilling damage in the light”. J Plant Res 111:121–129Google Scholar
  95. 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 center subunits of photosystem I, upon photoinhibition. Photosynth Res 53:55–63Google Scholar
  96. Szyszka B, Ivanov AG, Huner NPA (2007) Psychrophily is associated with differential energy partitioning, photosystem stoichiometry and polypeptide phosphorylation in Chlamidomonas taudensis. Biochim Biophys Acta 1757:789–800Google Scholar
  97. 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(2):300–306Google Scholar
  98. Tjus SE, Andersson B (1993) Loss of the trans-thylakoid proton gradient is an early event during photoinhibitory illumination of chloroplast preparations. Biochim Biophys Acta 1183:315–322Google Scholar
  99. Triantaphylides C, Havaux M (2009) Singlet oxygen in plants: production, detoxification and signaling. Trends Plant Sci 14:219–228Google Scholar
  100. van Kooten O, Snell JFH (1990) The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynth Res 25:147–150Google Scholar
  101. Velichkova M, Popova A (2005) High light-induced changes of 77K fluorescence spectral characteristics of thylakoid membranes with modified fluidity. Bioelectrochemistry 67:81–90Google Scholar
  102. Ware MA, Dall’Osto L, Ruban AV (2016) An in vivo quantitative comparison of photoprotection in Arabidopsis xanthophyll mutants. Front Plant Sci 7:841Google Scholar
  103. Wei H, Yang Y-J, Zhang S-B (2017) Specific roles of cyclic electron flow around photosystem I in photosynthetic regulation in immature and mature leaves. J Plant Physiol 209:76–83Google Scholar
  104. Wientjes E, van Amerongen H, Croce R (2013) LHCII is an antenna for both photosystems after long-term acclimation. Biochim Biophys Acta 1827:420–426Google Scholar
  105. Yamori W, Makino A, Shikanai T (2016) A physiological role of cyclic electron transport around photosystem I in sustaining photosynthesis under fluctuating light in rice. Sci Rep 6:20147Google Scholar
  106. Yruela I, Tomás R, Sanjuán ML, Torrado E, Aured M, Picorel R (1998) The configuration of β-carotene in the photosystem II reaction center. Photochem Photobiol 68:729–737Google Scholar
  107. Zeinalov Y (2002) An equipment for investigations of photosynthetic oxygen production reactions. Bulg J Plant Physiol 28:57–67Google Scholar

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Authors and Affiliations

  • Antoaneta V. Popova
    • 1
    Email author
  • Konstantin Dobrev
    • 1
  • Maya Velitchkova
    • 1
  • Alexander G. Ivanov
    • 1
    • 2
  1. 1.Institute of Biophysics and Biomedical EngineeringBulgarian Academy of SciencesSofiaBulgaria
  2. 2.Department of BiologyUniversity of Western OntarioLondonCanada

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