Photosynthetic responses of sun- and shade-grown barley leaves to high light: Is the lower PSII connectivity in shade leaves associated with protection against excess of light?

Photosynthesis Research

Volumn 119, Issue 3, 2014, Pages 339-354

  Zivcak, Marek ^a   Brestic, Marian ^a   Kalaji, Hazem M ^b   Govindjee, ^c  

^a SLOVAK UNIVERSITY OF AGRICULTURE IN NITRA   (Slovakia)

^b WARSAW UNIVERSITY OF LIFE SCIENCES   (Poland)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Barley; Chlorophyll a fluorescence; Electron transport; Photoinhibition; PSII excitonic connectivity; Sun and shade leaves

Indexed keywords

CAROTENOID; CHLOROPHYLL; CHLOROPHYLL A; CHLOROPHYLL B;

ARTICLE; FLUORESCENCE; GROWTH, DEVELOPMENT AND AGING; HORDEUM; LIGHT; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGY; PLANT LEAF;

CAROTENOIDS; CHLOROPHYLL; FLUORESCENCE; HORDEUM; LIGHT; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES;

EID: 84894439357     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-014-9969-8     Document Type: Article

References (127)

1. Adir N, Zer H, Shokhat S, Ohad I (2003) Photoinhibition - a historical perspective. Photosynth Res 76:343-370
2. Anderson JM, Park YI, Chow WS (1997) Photoinactivation and photoprotection of photosystem II in nature. Physiol Plant 100:214-223
3. + from stromal components via the intersystem chain. Plant Cell Physiol 33:927-932
4. Bailey S, Walters RG, Jansson S, Horton P (2001) Acclimation of Arabidopsis thaliana to the light environment: the existence of separate low light and high light responses. Planta 213:794-801
5. Bailey S, Horton P, Walters RG (2004) Acclimation of Arabidopsis thaliana to the light environment: the relationship between photosynthetic function and chloroplast composition. Planta 218:793-802
6. Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173-185
7. 2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plant of diverse origins. Planta 170:489-504
8. Bradbury M, Baker NR (1981) Analysis of the slow phases of the in vivo chlorophyll fluorescence induction curve. Biochim Biophys Acta 63:542-551
9. Bradbury M, Baker NR (1984) A quantitative determination of photochemical and non-photochemical quenching during the slow phase of the chlorophyll fluorescence induction curve of bean leaves. Biochim Biophys Acta 765:275-281
10. Brestic M, Zivcak M (2013) PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In: Rout GR, Das AB (eds) Molecular stress physiology of plants. Springer, Berlin
11. Brestic M, Cornic G, Fryer M, Baker N (1995) Does photorespiration protect the photosynthetic apparatus in French bean leaves from photoinhibition during drought stress? Planta 196:450-457
12. Brestic M, Zivcak M, Kalaji MH, Allakhverdiev SI, Carpentier R (2012) Photosystem II thermo-stability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiol Biochem 57:93-105
13. Briantais JM, Merkelo H, Govindjee (1972) Lifetime of the excited state τ in vivo. III. Chlorophyll during fluorescence induction in Chlorella pyrenoidosa. Photosynthetica 6:133-141
14. Bussotti F, Desotgiu R, Cascio C, Pollastrini M, Gravano E, Gerosa G, Marzuoli R, Nali C, Lorenzini G, Salvatori E, Manes F et al (2011) Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environ Exp Bot 73:19-30
15. Butler WL (1978) Energy distribution in the photochemical apparatus of photosynthesis. Annu Rev Plant Physiol 29:345-378
16. Cascio C, Schaub M, Novak K, Desotgui R, Bussotti F, Strasser RJ (2010) Foliar responses to ozone of Fagus sylvatica L. seedlings grown in shaded and in full sunlight conditions. Environ Exp Bot 68:188-197
17. Chow WS, Anderson JM (1987) Photosynthetic responses of Pisum sativum to an increase in irradiance during growth. 2. Thylakoid membrane components. Aust J Plant Physiol 14:9-19
18. Demmig-Adams B, Adams WW (1992) Photoprotection and other responses of plants to high light stress. Annu Rev Plant Physiol Plant Mol Biol 43:599-626
19. Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11-21
20. Demmig-Adams B, Moeller DL, Logan BA, Adams WW (1998) Positive correlation between levels of retained zeaxanthin + anthrexanthin and degree of photoinhibition in shade leaves of Schefflera arboricola. Planta 205:367-374
21. Desotgiu R, Bussotti F, Faoro F, Iriti M, Agati G, Marzuoli R, Gerosa G, Tani C (2010) Early events in Populus hybrid and Fagus sylvatica leaves exposed to ozone. Sci World J 10:512-527
22. Duysens LMN, Sweers HT (1963) Mechanism of the two photochemical reactions in algae as studied by means of fluorescence. In: Japanese Society of Plant Physiologists (ed) Studies on microalgae and photosynthetic bacteria. University of Tokyo Press, Tokyo, pp 353-372
23. 2 uptake and transmittance at 800 nm. Plant Cell Physiol 41:432-439
24. Evans JR (1993) Photosynthesis acclimation and nitrogen partitioning within a lucerne canopy. Stability through time and comparison with a theoretical optimum. Aust J Plant Physiol 20:69-82
25. Evans JR (1996) Developmental constraints on photosynthesis: effects of light and nutrition. In: Baker NR (ed) Photosythesis and the environment. Kluwer, Dordrecht, pp 281-304
26. Falbel TG, Meehl JB, Staehelin LA (1996) Severity of mutant phenotype in a series of chlorophyll-deficient wheat mutants depends on light intensity and the severity of the block in chlorophyll synthesis. Plant Physiol 112:821-832
27. Force L, Critchley C, van Rensen JJS (2003) New fluorescence parameters for monitoring photosynthesis in plants. 1. The effect of illumination on the fluorescence parameters of the JIP-test. Photosynth Res 78:17-33
28. Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signaling. New Phytol 146:359-388
29. Genty B, Briantais JM, Baker NR (1989) The relationship between quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87-92
30. Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63-92
31. Golding AJ, Johnson GN (2003) Down-regulation of linear and activation of cyclic electron transport during drought. Planta 218:107-114
32. Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji MH, Yordanov I, Krasteva V, Alexandrov V, Stefanov D, Allakverdiev S, Strasser RJ (2012) Drought-induced modifications of photosynthetic electron transport in intact leaves: analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta 1817:1490-1498
33. Gray RG, Savith LV, Ivanov AG, Huner NPA (1996) Photosystem II excitation pressure and development of resistance to photoinhibition. Plant Physiol 110:61-71
34. Haehnel W (1984) Photosynthetic electron transport in higher plants. Annu Rev Plant Physiol Plant Mol Biol 35:659-693
35. Havaux M, Strasser RJ, Greppin H (1991) A theoritical and experimental analysis of qP and qN coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27:41-55
36. B-protein, the cytochrome-f cytochrome-B6 complex and other components of the photosynthetic apparatus. Planta 173:267-274
37. Jiang HX, Chen LS, Zheng JG, Han S, Tang N, Smith BR (2008) Aluminum-induced effects on Photosystem II photochemistry in Citrus leaves assessed by the chlorophyll a fluorescence transient. Tree Physiol 28:1863-1871
38. Joliot A, Joliot P (1964) Etude cinétique de la réaction photochimique libérant l'oxygène au cours de la photosynthèse. Comptes Rendus de l'Académie des Sciences, Paris 258:4622-4625
39. Joliot P, Joliot A (2003) Excitation transfer between photosynthetic units: the 1964 experiment. Photosynth Res 76:241-245
40. 2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64-72
41. Kalaji MH, Carpentier R, Allakhverdiev SI, Bosa K (2012) Fluorescence parameters as an early indicator of light stress in barley. J Photochem Photobiol B Biol 112:1-6
42. Kirchhoff H, Borinski M, Lenhert S, Chi LF, Buchel C (2004) Transversal and lateral exciton energy transfer in grana thylakoids of spinach. Biochemistry 43(45):14508-14516
43. Kitajima M, Butler WL (1975) Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochim Biophys Acta 376:105-115
44. Kornyeyev D, Logan BA, Holaday AS (2010) Excitation pressure as a measure of the sensitivity of photosystem II to photoinactivation. Funct Plant Biol 37:943-951
45. A redox state and excitation energy fluxes. Photosynth Res 79:209-218
46. Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Ann Rev Plant Physiol Plant Mol Biol 42:313-349
47. Krause GH, Briantais JM, Vernotte C (1982) Photoinduced quenching of chlorophyll fluorescence in intact chloroplasts and algae: resolution into two components. Biochim Biophys Acta 679:116-124
48. Krol M, Ivanov AG, Jansson S, Kloppstech K, Huner NP (1999) Greening under high light or cold temperature affects the level of xanthophyll-cycle pigments, early light-inducible proteins, and light-harvesting polypeptides in the wild-type barley and the chlorina f2 mutant. Plant Physiol 120:193-204
49. Kroon BMA (1994) Variability of Photosystem II quantum yield and related processes in Chlorella pyrenoidosa (Chlorophyta) acclimated to an oscillating light regime simulating a mixed photic zone. J Phycol 30:841-852
50. 2 concentration and different growth irradiance. Photosynthetica 41:209-219
51. Kyle DJ, Ohad I, Arntzen CJ (1984) Membrane protein damage and repair: selective loss of a quinone-protein function in chloroplast membranes. Proc Nat Acad Sci USA 81:4070-4074
52. Laisk A, Oja V (2013) Thermal phase and excitonic connectivity in fluorescence induction. Photosynth Res 117:431-448
53. Lambrev PH, Schmitt FJ, Kussin S, Schoengen M, Varkonyi Z, Eichler HJ, Garab G, Renger G (2011) Functional domain size in aggregates of light-harvesting complex II and thylakoid membranes. Biochim Biophys Acta 9:1022-1031
54. Lavergne J, Trissl HW (1995) Theory of fluorescence induction in photosystem-II - derivation of analytical expressions in a model including exciton-radical-pair equilibrium and restricted energy transfer between photosynthetic units. Biophys J 68:2474-2492
55. Lazar D (1999) Chlorophyll a fluorescence induction. Biochim Biophys Acta 1412:1-28
56. Lazar D (2006) The polyphasic chlorophyll a fluorescence risemeasured under high intensity of exciting light. Funct Plant Biol 33:9-30
57. Leong TY, Anderson JM (1984a) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. I. Study on the distribution of chlorophyll-protein complexes. Photosynth Res 5:105-115
58. Leong TY, Anderson JM (1984b) Adaptation of the thylakoid membranes of pea chloroplasts to light intensities. II. Regulation of electron transport capacities, electron carriers, coupling factor (CF1) activity and rates of photosynthesis. Photosynth Res 5:117-128
59. Leong TY, Anderson JM (1986) Light-quality and irradiance adaptation of the composition and function of pea thylakoid membranes. Biochim Biophys Acta 850:57-63
60. Lichtenthaler HK (1985) Differences in morphology and chemical composition of leaves grown at different light intensities and qualities. In: Baker NR, Davies WJ, Ong CK (eds) Control of leaf growth. Cambridge University Press, Cambridge, pp 201-221
61. Lichtenthaler HL (1987) Chlorophyll and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350-382
62. Lichtenthaler HK, Buschmann C, Doll M, Fietz HJ, Bach T, Kozel U, Meier D, Rahmsdorf U (1981) Photosynthetic activity, chloroplast ultrastructure, and leaf characteristics of high-light and low-light plants and of sun and shade leaves. Photosynth Res 2:115-141
63. Lichtenthaler HK, Ač A, Marek MV, Kalina J, Urban O (2007) Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiol Biochem 45:577-588
64. Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Plant Mol Biol 45:633-662
65. Malkin S, Kok B (1966) Fluorescence induction studies in isolated chloroplasts. I. Number of components involved in the reaction and quantum yields. Biochim Biophys Acta 126:413-432
66. Malkin S, Wong D, Govindjee, Merkelo H (1980) Parallel measurements on fluorescence lifetime and intensity from leaves during fluorescence induction. Photobiochem Photobiophys 1:83-89
67. Mehta P, Allakhverdiev SI, Jajoo A (2010) Characterization of photosystem II heterogeneity in response to high salt stress in wheat leaves (Triticum aestivum). Photosynth Res 105:249-255
68. Mehta P, Kraslavsky V, Bharti S, Allakhverdiev SI, Jajoo A (2011) Analysis of salt stress induced changes in photosystem II heterogeneity by prompt fluorescence and delayed fluorescence in wheat (Triticum aestivum) leaves. J Photochem Photobiol B 104:308-313
69. Melis A (1999) Photosystem-II damage and repair cycle in chloroplasts: what modulates the rate of photodamage in vivo? Trends Plant Sci 4:130-135
70. Melis A, Homann PH (1976) Heterogeneity of the photochemical centers in system II of chloroplasts. Photochem Photobiol 23:343-350
71. Moya I, Govindjee, Vernotte C, Briantais JM (1977) Antogonistic effect of mono-and divalent cations on lifetime τ and quantum yield of fluorescence (φ) in isolated chloroplasts. FEBS Lett 75:13-18
72. Munday JC, Govindjee (1969) Light-induced changes in the fluorescence yield of chlorophyll a in vivo: IV. The effect of preillumination on the fluorescence transient of Chlorella pyrenoidosa. Biophys J 9:22-35
73. Muraoka H, Tang YH, Terashima I, Koizumi H, Washitani I (2000) Contribution of diffusional limitation, photo inhibition and photorespiration to midday depression of photosynthesis in Arisaema heterophyllum in natural high light. Plant Cell Environ 23:235-250
74. Murchie EH, 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 20:438-448
75. Neubauer C, Schreiber U (1987) The polyphasic rise of chlorophyll fluorescence upon onset of strong continuous illumination: I. Saturation characteristics and partial control by the photosystem II acceptor side. Z Naturforsch 42c:1246-1254
76. Niinemets Ü, Kull O (2001) Sensitivity of photosynthetic electron transport to photoinhibition in a temperate deciduous forest canopy: photosystem II center openness, non-radiative energy dissipation and excess irradiance under field conditions. Tree Physiol 21:899-914
77. Ögren E (1991) Prediction of photoinhibition of photosynthesis from measurements of fluorescence quenching components. Planta 184:538-544
78. Ögren E, Rosenqvist E (1992) On the significance of photoinhibition of photosynthesis in the field and its generality among species. Photosynth Res 33:63-71
79. Oguchi R, Hikosaka K, Hirose T (2003) Does the photosynthetic light-acclimation need change in leaf anatomy? Plant Cell Environ 26:505-512
80. 2 evolution and chlorophyll fluorescence in sunflower leaves. Photosynth Res 114:15-28
81. Osmond CB (1994) What is photoinhibition? Some insights from the comparison of sun and shade plants. In: Baker NR, Bowyer JR (eds) Photoinhibition: molecular mechanisms to the field. Bios Scientific, Oxford, pp 189-258
82. Oukarroum A, El Madidi S, Schansker G, Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ Exp Bot 60:438-446
83. Oxborough K, Baker NR (1997) Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components - calculation of qP and Fv′/Fm′ without measuring Fo. Photosynth Res 54:135-142
84. Paillotin G (1976) Movement of excitations in the photosynthesis domain of photosystem II. J Theor Biol 58:237-252
85. Papageorgiou G, Govindjee (eds) (2004) Chlorophyll a fluorescence: a signature of photosynthesis. Kluwer (now Springer), Dordrecht
86. Powles SB (1984) Photoinhibition of photosynthesis induced by visible light. Annu Rev Plant Physiol 35:15-44
87. Quick W, Horton P (1984) Studies on the induction of chlorophyll fluorescence in barley protoplasts. II Resolution of fluorescence quenching by redox state and the transthylakoid pH gradient. Proc R Soc Lond B 220:371-382
88. Quick WP, Stitt M (1989) An explanation of factors contributing to non-photochemical quenching of fluorescence in barley leaves. Biochim Biophys Acta 977:287-296
89. Redillas MC, Kim YS, Jeong JS, Strasser RJ, Kim JK (2011) The use of JIP test to evaluate drought-tolerance of transgenic rice overexpressing OsNAC10. Plant Biotechnol Rep 5:169-176
90. Repkova J, Brestic M, Zivcak M (2008) Bioindication of barley leaves vulnerability in conditions of water deficit. Cereal Res Commun 36:1747-1750
91. A within a narrow range over a broad range of light intensities. Photosynth Res 70:299-310
92. Schansker G, Srivastava A, Govindjee, Strasser RJ (2003) Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol 30:785-796
93. Schansker G, Tóth SZ, Strasser RJ (2005) Methylviologen and dibromothymoquinone treat-ments of pea leaves reveal the role of photosystem I in the chlorophyll a fluorescence rise OJIP. Biochim Biophys Acta 1706:250-261
94. Schansker G, Toth S, Kovacs L, Holzwarth AR, Garab G (2011) Evidence for a fluorescence yield change driven by a lightinduced conformational change within photosystem II during the fast chlorophyll a fluorescence rise. Biochim Biophys Acta 1807:1032-1043
95. A model. Photosynth Res. doi: 10.1007/s11120-013-9806-5
96. Schreiber U (1986) Detection of rapid induction kinetics with a new type of high frequency modulated chlorophyll fluorescence. Photosynth Res 9:261-272
97. Schreiber U, Bilger W (1987) Rapid assessment of stress effects on plant leaves by chlorophyll fluorescence measurements. In: Tenhunen JD, Catarino FM, Lange OL, Oechel WC (eds) Plant response to stress. Springer, Berlin-Heidelberg, pp 27-53
98. Schreiber U, Schliwa U, Bilger W (1986) Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer. Photosynth Res 10:51-62
99. Schreiber U, Bilger W, Klughammer C, Neubauer C (1988) Application of the PAM fluorometer in stress detection. In: Lichtenthaler HK (ed) Applications of chlorophyll fluorescence. Kluwer, Dordrecht, pp 151-155
100. Schreiber U, Hormann H, Neubauer C, Klughammer C (1995) Assessment of photosystem II photochemical quantum yield by chlorophyll fluorescence quenching analysis. Aust J Plant Physiol 22:209-220
101. Setlik I, Allakhverdiev SI, Nedbal L, Setlikova E, Klimov VV (1990) Three types of Photosystem II photoinactivation. I. Damaging processes on the acceptor side. Photosynth Res 23:39-48
102. Srivastava A, Strasser RJ, Govindjee (1999) Greening of peas: parallel measurements of 77K emission spectra, OJIP chlorophyll a fluorescence transient, period four oscillation of the initial fluorescence level, delayed light emission, and P700. Photosynthetica 37:365-392
103. Stiehl HH, Witt HT (1969) Quantitative treatment of the function of plastoquinone in photosynthesis. Z Naturforsch B 24:1588-1598
104. Stirbet A (2013) Excitonic connectivity between photosystem II units: what is it and how to measure it? Photosynth Res 116:189-214
105. Stirbet A, Govindjee (2011) On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B Biol 104:236-257
106. Stirbet A, Govindjee (2012) Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J-I-P rise. Photosynth Res 113:15-61
107. 0 and the O-J-I-P fluorescence rise in higher plants and algae. In: Argyroudi-Akoyunoglou JH (ed) Regulation of chloroplast biogenesis. Plenum Press, New York, pp 423-426
108. Strasser RJ, Stirbet AD (2001) Estimation of the energetic connectivity of PSII centres in plants using the fluorescence rise O-J-I-P. Fitting of experimental data to three different PSII models. Math Comp Simul 56:451-461
109. Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: The JIP-test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer, Dordrecht, pp 977-980
110. Strasser RJ, Srivastava A, Govindjee (1995) Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. Photochem Photobiol 61:32-42
111. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterise and screen photosynthetic samples. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor and Francis, London, pp 445-483
112. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll fluorescence: a signature of photosynthesis, Advances in photosynthesis and respiration, vol 19. Springer, Dordrecht, pp 321-362
113. Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V (2010) Simultaneous in vivo recording of prompt and delayed fluorescence and 820 nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta Bioenerg 1797:1313-1326
114. Tanaka R, Tanaka A (2000) Chlorophyll b is not just an accessory pigment but a regulator of the photosynthetic antenna. Porphyrins 9:240-245
115. Terashima I, Araya T, Miyazava KS, Yano S (2005) Construction and maintenance of the optimal photosynthetic systems of the leaf, herbaceous plant and tree: an eco-developmental treatise. Ann Bot 95:507-519
116. Timperio AM, Gevi F, Ceci LR, Zolla L (2012) Acclimation to intense light implies changes at the level of trimeric subunits involved in the structural organization of the main light-harvesting complex of photosystem II (LHCII) and their isoforms. Plant Physiol Biochem 50:8-14
117. Toth SZ, Schansker G, Strasser RJ (2007) A non-invasive assay of the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193-203
118. Trissl H-W, Lavergne J (1995) Fluorescence induction from photosystem II: analytical equations for the yields of photochemistry and fluorescence derived from analysis of a model including exciton radical pair equilibrium and restricted energy transfer between photosynthetic units. Aust J Plant Physiol 22:183-193
119. Tsimilli-Michael M, Strasser RJ (2013) The energy flux theory 35 years later: formulations and applications. Photosynth Res 117:289-320
120. Tyystjärvi E, Ali-Yrkko K, Kettunen R, Aro EM (1992) Slow degradation of the Dl protein is related to the susceptibility of low-light-grown pumpkin plants to photoinhibition. Plant Physiol 100:1310-1317
121. Tyystjärvi E, Rantamäki S, Tyystjärvi J (2009) Connectivity of photosystem II is the physical basis of retrapping in photosynthetic thermoluminescence. Biophys J 96:3735-3743
122. Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta 1817:209-217
123. Vredenberg WJ (2008) Analysis of initial chlorophyll fluorescence induction kinetics in chloroplasts in terms of rate constants of donor side quenching release and electron trapping in photosystem II. Photosynth Res 96:83-97
124. Walters R, Horton GP (1991) Resolution of components of non-photochemical chlorophyll fluorescence quenching in barley leaves. Photosynth Res 27:121-133
125. Weis E, Ball JR, Berry J (1987) Photosynthetic control of electron transport in leaves of Phaseolus vulgaris. Evidence for regulation of PSII by the proton gradient. In: Biggins J (ed) Progress in photosynthesis research. Kluwer, Dordrecht, pp 553-556
126. White AJ, Critchley C (1999) Rapid light curves: a new fluorescence method to assess the state of the photosynthetic apparatus. Photosynth Res 9:63-72
127. Zivcak M, Brestic M, Olsovska K, Slamka P (2008) Performance index as a sensitive indicator of water stress in Triticum aestivum L. Plant Soil Environ 54:133-139