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Modeling chlorophyll a fluorescence transient: Relation to photosynthesis

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Abstract

To honor Academician Alexander Abramovitch Krasnovsky, we present here an educational review on the relation of chlorophyll a fluorescence transient to various processes in photosynthesis. The initial event in oxygenic photosynthesis is light absorption by chlorophylls (Chls), carotenoids, and, in some cases, phycobilins; these pigments form the antenna. Most of the energy is transferred to reaction centers where it is used for charge separation. The small part of energy that is not used in photochemistry is dissipated as heat or re-emitted as fluorescence. When a photosynthetic sample is transferred from dark to light, Chl a fluorescence (ChlF) intensity shows characteristic changes in time called fluorescence transient, the OJIPSMT transient, where O (the origin) is for the first measured minimum fluorescence level; J and I for intermediate inflections; P for peak; S for semi-steady state level; M for maximum; and T for terminal steady state level. This transient is a real signature of photosynthesis, since diverse events can be related to it, such as: changes in redox states of components of the linear electron transport flow, involvement of alternative electron routes, the build-up of a transmembrane pH gradient and membrane potential, activation of different nonphotochemical quenching processes, activation of the Calvin-Benson cycle, and other processes. In this review, we present our views on how different segments of the OJIPSMT transient are influenced by various photosynthetic processes, and discuss a number of studies involving mathematical modeling and simulation of the ChlF transient. A special emphasis is given to the slower PSMT phase, for which many studies have been recently published, but they are less known than on the faster OJIP phase.

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References

  1. Croce, R., and van Amerongen, H. (2011) J. Photochem. Photobiol. B, 104, 142–153.

    PubMed  CAS  Google Scholar 

  2. Muh, F., Glockner, C., Hellmich, J., and Zouni, A. (2012) Biochim. Biophys. Acta, 1817, 44–65.

    PubMed  Google Scholar 

  3. Nelson, N., and Yocum, C. F. (2006) Annu. Rev. Plant Biol., 57, 521–565.

    PubMed  CAS  Google Scholar 

  4. Rabinowitch, E., and Govindjee (1969) Photosynthesis, Wiley, N. Y.

    Google Scholar 

  5. Ke, B. (2001) Photosynthesis: Photobiochemistry and Photobiophysics. Advances in Photosynthesis and Respiration (Govindjee, series ed.) Vol. 10, Kluwer Academic, Dordrecht.

    Google Scholar 

  6. Blankenship, R. E. (2002) Molecular Mechanisms of Photosynthesis, Blackwell Science, Oxford.

    Google Scholar 

  7. Shevela, D., Bjorn, L. O., and Govindjee (2013) in Natural and Artificial Photosynthesis: Solar Power as an Energy Source (Razeghifard, R., ed.) John Wiley and Sons, Hoboken, NJ, pp. 13–64 (in press).

  8. Govindjee, Amesz, J., and Fork, D. C. (eds.) (1986) Light Emission by Plants and Bacteria, Academic Press, Orlando.

    Google Scholar 

  9. Papageorgiou, G. C., and Govindjee (eds.) (2004) Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration (Govindjee and Sharkey, T. D., series eds.) Vol. 19, Springer, Dordrecht, The Netherlands.

    Google Scholar 

  10. Latimer, P., Bannister, T. T., and Rabinowitch, E. (1956) Science, 124, 585–586.

    PubMed  CAS  Google Scholar 

  11. Manodori, A., and Melis, A. (1986) Plant Physiol., 82, 185–189.

    PubMed Central  PubMed  CAS  Google Scholar 

  12. Chow, W. S., Fan, D.-Y., Oguchi, R., Jia, H., Losciale, P., Park, Y.-I., He, J., Oquist, G., Shen, Y.-G., and Anderson, J. M. (2012) Photosynth. Res., 113, 63–74.

    PubMed  CAS  Google Scholar 

  13. Kautsky, H., and Hirsch, A. (1931) Naturwissenschaften, 19, 964.

    CAS  Google Scholar 

  14. Govindjee and Papageorgiou, G. C. (1971) Photophysiology, 6, 1–50.

    Google Scholar 

  15. Papageorgiou, G. C. (1975) in Bioenergetics of Photosynthesis (Govindjee, ed.) Academic Press, New York, pp. 319–372.

    Google Scholar 

  16. Govindjee (1995) Aust. J. Plant Physiol., 22, 131–160.

    CAS  Google Scholar 

  17. Klughammer, C., and Schreiber, U. (2008) PAM Appl. Notes, 1, 27–35 (http://www.walz.com/).

    Google Scholar 

  18. Lazar, D. (1999) Biochim. Biophys. Acta, 1412, 1–28.

    PubMed  CAS  Google Scholar 

  19. Lazar, D. (2006) Funct. Plant Biol., 33, 9–30.

    CAS  Google Scholar 

  20. Strasser, R. J., Srivastava, A., and Tsimilli-Michael, M. (2000) in Probing Photosynthesis: Mechanism, Regulation and Adaptation (Yunus, M., Pathre, U., and Mohanty, P., eds.) Taylor and Francis, London, pp. 443–480.

  21. Strasser, R. J., Tsimilli-Michael, M., and Srivastava, A. (2004) in Chlorophyll a Fluorescence: a Signature of Photosynthesis. Advances in Photosynthesis and Respiration (Papageorgiou, G. C., and Govindjee, eds.) Vol. 19, Springer, Dordrecht, pp. 321–362.

  22. Papageorgiou, G. C., Tsimilli-Michael, M., and Stamatakis, K. (2007) Photosynth. Res., 94, 275–290.

    PubMed  CAS  Google Scholar 

  23. Stirbet, A., and Govindjee (2011) J. Photochem. Photobiol. B, 104, 236–257.

    PubMed  CAS  Google Scholar 

  24. Stirbet, A., and Govindjee (2012) Photosynth. Res., 113, 15–61.

    PubMed  CAS  Google Scholar 

  25. Schansker, G., Toth, S. Z., Kovacs, L., Holzwarth, A. R., and Garab, G. (2013) Photosynth. Res., doi: 10.1007/s11120-013-9806-5.

    Google Scholar 

  26. Falkowski, P. G., and Raven, J. A. (2007) Aquatic Photosynthesis, 2nd Edn., Princeton University Press, Princeton, NJ.

    Google Scholar 

  27. Laisk, A., Nedbal, L., and Govindjee (eds.) (2009) Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Advances in Photosynthesis and Respiration (Govindjee and Sharkey, T. D., series eds.) Vol. 29, Springer, Dordrecht.

    Google Scholar 

  28. Eaton-Rye, J. J., Tripathy, B. C., and Sharkey, T. D. (eds.) (2011) Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation, Advances in Photosynthesis and Respiration (Govindjee and Sharkey, T. D., series eds.) Vol. 34, Springer, Dordrecht.

    Google Scholar 

  29. Rottgers, R. (2007) Deep-Sea Res., 54, 437–451.

    Google Scholar 

  30. Serodio, J., Ezequiel, J., Frommlet, J., Laviale, M., and Lavaud, J. (2013) Plant Physiol., 163, 1089–1102.

    PubMed  CAS  Google Scholar 

  31. Adams, W. W., III, and Demmig-Adams, B. (2004) in Advances in Photosynthesis and Respiration (Papageorgiou, G. C., and Govindjee, eds.) Vol. 19, Springer, Berlin, pp. 583–604.

    Google Scholar 

  32. Logan, B. A., Adams, W. W., III, and Demmig-Adams, B. (2007) Funct. Plant Biol., 34, 853–859.

    CAS  Google Scholar 

  33. Kalaji, H. M., Goltsev, V., Bosa, K., Allakhverdiev, S. I., Strasser, R. J., and Govindjee (2012) Photosynth. Res., 114, 69–96.

    PubMed  CAS  Google Scholar 

  34. Mar, T., Govindjee, Singhal, G. S., and Merkelo, H. (1972) Biophys. J., 12, 797–808.

    PubMed Central  PubMed  CAS  Google Scholar 

  35. Briantais, J.-M., Merkelo, H., and Govindjee (1972) Photosynthetica, 6, 133–141.

    CAS  Google Scholar 

  36. Kitajima, M., and Butler, W. L. (1975) Biochim. Biophys. Acta, 408, 297–305.

    PubMed  CAS  Google Scholar 

  37. Itoh, S., and Sugiura, K. (2004) in Chlorophyll a Fluorescence: A Signature of Photosynthesis. Advances in Photosynthesis and Respiration (Papageorgiou, G. C., and Govindjee, eds.) Vol. 19, Springer, Dordrecht, pp. 231–250.

    Google Scholar 

  38. Franck, F., Juneau, P., and Popovic, R. (2002) Biochim. Biophys. Acta, 162, 239–246.

    Google Scholar 

  39. Pfundel, E. (1998) Photosynth. Res., 56, 185–195.

    CAS  Google Scholar 

  40. Gilmore, A. M., Itoh, S., and Govindjee (2000) Philos. Trans. R. Soc. Lond. B, 335, 1–14.

    Google Scholar 

  41. Pfundel, E., Klughammer, C., Meister, A., and Cerovic, Z. G. (2013) Photosynth. Res., 114, 189–206.

    PubMed  Google Scholar 

  42. Tian, L., Dinc, E., and Croce, R. (2013) Poster at 16th Int. Photosynthesis Congr., St. Louis, Mo, USA, August.

    Google Scholar 

  43. Govindjee (2004) in Chlorophyll a Fluorescence: a Signature of Photosynthesis. Advances in Photosynthesis and Respiration (Papageorgiou, G. C., and Govindjee, eds.) Vol. 19, Springer, Dordrecht, pp. 1–41.

    Google Scholar 

  44. Schreiber, U. (1986) Photosynth. Res., 9, 261–272.

    PubMed  CAS  Google Scholar 

  45. Strasser, R. J., and Govindjee (1991) in Regulation of Chloroplast Biogenesis (Argyroudi-Akoyunoglou, J. H., and Akoyunoglou, G., eds.) Plenum Press, New York, pp. 423–426.

  46. Strasser, R. J., and Govindjee (1992) in Research in Photosynthesis (Murata, N., ed.) Vol. 2, Kluwer Academic Publishers, Dordrecht, pp. 29–32.

  47. Papageorgiou, G. C., and Govindjee (1968) Biophys. J., 8, 1299–1315.

    PubMed Central  PubMed  CAS  Google Scholar 

  48. Papageorgiou, G. C., and Govindjee (1968) Biophys. J., 8, 1316–1328.

    PubMed Central  PubMed  CAS  Google Scholar 

  49. Sunil, B., Riazunnisa, K., Krishna, S. T., Schansker, G., Strasser, R. J., Raghavendra, S., and Mohanty, P. (2008) Indian J. Biochem. Biophys., 45, 37–43.

    CAS  Google Scholar 

  50. Guisse, B., Srivastava, A., and Strasser, R. J. (1995) Arch. Sci. Geneve, 48, 147–160.

    CAS  Google Scholar 

  51. Srivastava, A., Guisse, B., Greppin, H., and Strasser, R. J. (1997) Biochim. Biophys. Acta, 1320, 95–106.

    CAS  Google Scholar 

  52. Tsimilli-Michael, M., Pecheux, M., and Strasser, R. J. (1998) Arch. Sci. Geneve, 51, 205–240.

    Google Scholar 

  53. Duysens, L. M. N., and Sweers, H. E. (1963) in Studies on Microalgae and Photosynthetic Bacteria, Japanese Society of Plant Physiologists, University of Tokyo Press, Tokyo, pp. 353–372.

    Google Scholar 

  54. Van Gorkom, H. J., Pulles, M. P. J., and Etienne, A.-L. (1978) in Photosynthetic Oxygen Evolution (Metzner, H., ed.) Academic Press, London, UK, pp. 135–145.

  55. Klimov, V. V. (2003) Photosynth. Res., 76, 247–253.

    PubMed  CAS  Google Scholar 

  56. Schatz, G. H., Brock, H., and Holzwarth, A. R. (1988) Biophys. J., 54, 397–405.

    PubMed Central  PubMed  CAS  Google Scholar 

  57. Dau, H. (1994) J. Photochem. Photobiol. B, 26, 3–27.

    CAS  Google Scholar 

  58. Samson, G., Prasil, O., and Yaakoubd, B. (1999) Photosynthetica, 37, 163–182.

    CAS  Google Scholar 

  59. Laisk, A., Eichelmann, H., and Oja, V. (2006) Photosynth. Res., 90, 45–66.

    PubMed  CAS  Google Scholar 

  60. Laisk, A., Eichelmann H., and Oja, V. (2009) in Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Advances in Photosynthesis and Respiration (Laisk, A., Nedbal, L., and Govindjee, eds.) Vol. 29, Springer, Dordrecht, pp. 295–322.

  61. Papageorgiou, G. C., and Govindjee (2011) J. Photochem. Photobiol. B: Biol., 104, 258–270.

    CAS  Google Scholar 

  62. Zhu, X.-G., Wang, Y., Ort, D. R., and Long, S. P. (2012) Publications from USDA-ARS/UNL Faculty, Paper 1137.

    Google Scholar 

  63. Antal, T. K., Kovalenko, I. B., Rubin, A. B., and Tyystjarvi, E. (2013) Photosynth. Res., 117, 1–30.

    PubMed  CAS  Google Scholar 

  64. Renger, G., and Schulze, A. (1985) Photobiochem. Photobiophys., 9, 79–87.

    CAS  Google Scholar 

  65. Lazar, D., and Schansker, G. (2009) in Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Advances in Photosynthesis and Respiration (Laisk, A., Nedbal, L., and Govindjee, eds.) Vol. 29, Springer, Dordrecht, pp. 85–123.

  66. Bannister, T. T., and Rice, G. (1968) Biochim. Biophys. Acta, 162, 555–580.

    PubMed  CAS  Google Scholar 

  67. Delosme, R. (1967) Biochim. Biophys. Acta, 143, 108–128.

    PubMed  CAS  Google Scholar 

  68. Neubauer, C., and Schreiber, U. (1987) Zeit. Naturforsch., 42c, 1246–1254.

    Google Scholar 

  69. Strasser, R. J., Srivastava, A., and Govindjee (1995) Photochem. Photobiol., 61, 32–42.

    CAS  Google Scholar 

  70. Schansker, G., Toth, S. Z., Kovacs, L., Holzwarth, A. R., and Garab, G. (2011) Biochim. Biophys. Acta, 1807, 1032–1043.

    PubMed  CAS  Google Scholar 

  71. Stirbet, A., Govindjee, Strasser, B. J., and Strasser, R. J. (1998) J. Theor. Biol., 193, 131–151.

    CAS  Google Scholar 

  72. Zhu, X.-G., Govindjee, Baker, N. R., deSturler, E., Ort, D. R., and Long, S. P. (2005) Planta, 223, 114–133.

    PubMed  CAS  Google Scholar 

  73. Lazar, D. (2009) Photosynthetica, 47, 483–498.

    CAS  Google Scholar 

  74. Antal, T. K., and Rubin, A. B. (2008) Photosynth. Res., 96, 217–226.

    PubMed  CAS  Google Scholar 

  75. Makarov, S. S., Grachev, E. A., and Antal, T. K. (2012) Math. Biol. Bioinform., 7, 508–528.

    CAS  Google Scholar 

  76. Okayama, S., and Butler, W. L. (1972) Biochim. Biophys. Acta, 267, 523–527.

    PubMed  CAS  Google Scholar 

  77. Shinkarev, V. P., and Govindjee (1993) Proc. Natl. Acad. Sci. USA, 90, 7466–7469.

    PubMed Central  PubMed  CAS  Google Scholar 

  78. Schreiber, U., and Neubauer, C. (1990) Photosynth. Res., 25, 279–293.

    PubMed  CAS  Google Scholar 

  79. Lazar, D. (2003) J. Theor. Biol., 220, 469–503.

    PubMed  CAS  Google Scholar 

  80. Joliot, A., and Joliot, P. (1964) CR Acad. Sci. Paris, 258, 4622–4625.

    CAS  Google Scholar 

  81. Stirbet, A. (2013) Photosynth. Res., 116, 189–214.

    PubMed  CAS  Google Scholar 

  82. Tsimilli-Michael, M., and Strasser, R. J. (2013) Photosynth. Res., 117, 289–320.

    PubMed  CAS  Google Scholar 

  83. Joliot, P., Bennoun, P., and Joliot, A. (1973) Biochim. Biophys. Acta, 305, 317–328.

    PubMed  CAS  Google Scholar 

  84. Paillotin, G. (1976) J. Theor. Biol., 58, 237–252.

    CAS  Google Scholar 

  85. Lavergne, J., and Trissl, H.-W. (1995) Biophys. J., 68, 2474–2492.

    PubMed Central  PubMed  CAS  Google Scholar 

  86. Laisk, A., and Oja, V. (2013) Photosynth. Res., 117, 431–448.

    PubMed  CAS  Google Scholar 

  87. Moya, I. (1974) Biochim. Biophys. Acta, 368, 214–227.

    PubMed  CAS  Google Scholar 

  88. Lavorel, J., and Etienne, A.-L. (1977) in Topics in Photosynthesis. Primary Processes of Photosynthesis (Barber, J., ed.) Vol. 2, Elsevier/North-Holland Biomed-ical Press, Amsterdam, pp. 203–268.

  89. Holzwarth, A. R. (1987) in The Light Reactions (Barber, J., ed.) Elsevier, Amsterdam, pp. 95–157.

  90. Schmuk, G., and Moya, I. (1994) Remote Sens. Environ., 47, 72–76.

    Google Scholar 

  91. Strasser, R. J. (1978) in Chloroplast Development (Argyroudi-Akoyunoglou, J. H., and Akoyunoglou, G., eds.) Elsevier Biomedical, Amsterdam, pp. 513–538.

  92. Strasser, R. J. (1981) in Proc. Fifth Int. Congr. on Photosynthesis, Halkidiki, Greece, 1980 (Akoyunoglou, G., ed.) Vol. 3, Balaban International Science Services, Philadelphia, pp. 727–737.

  93. Butler, W. L. (1980) Proc. Natl. Acad. Sci. USA, 77, 4697–4701.

    PubMed Central  PubMed  CAS  Google Scholar 

  94. Koblizek, M., Kaftan, D., and Nedbal, L. (2001) Photosynth. Res., 68, 141–152.

    PubMed  CAS  Google Scholar 

  95. Yusuf, M. A., Kumar, D., Rajwanshi, R., Strasser, R. J., Tsimilli-Michael, M., Govindjee, and Sarin, N. M. (2010) Biochim. Biophys. Acta, 1797, 1428–1438.

    PubMed  CAS  Google Scholar 

  96. Strasser, R. J., Tsimilli-Michael, M., and Greppin, H. (1997) in Travelling Shot on Plant Development (Penel, C., Simon, P., and Greppin, H., eds.) Rochat-Baumann, Geneva, pp. 99–129.

  97. Stirbet, A., and Strasser, R. J. (2001) in Proc. 12th Int. Congr. on Photosynthesis, CSIRO Publishing, Colingwood.

    Google Scholar 

  98. Strasser, R. J., and Stirbet, A. (2001) Math. Comput. Simul., 56, 451–461.

    Google Scholar 

  99. Schreiber, U., Klughammer, C., and Kolbowski, J. (2011) PAM Appl. Notes, 1, 1–21 (http://www.walz.com).

    Google Scholar 

  100. Schreiber, U., Klughammer, C., and Kolbowski, J. (2012) Photosynth. Res., 113, 127–144.

    PubMed Central  PubMed  CAS  Google Scholar 

  101. Vredenberg, W. J. (2008) Photosynth. Res., 96, 83–97.

    PubMed  CAS  Google Scholar 

  102. Pospisil, P., and Tyystjarvi, E. (1999) Photosynth. Res., 32, 55–66.

    Google Scholar 

  103. Oukarroum, A., Goltsev, V., and Strasser, R. J. (2013) PLoS ONE, 8, e59433; doi:10.1371/journal.pone.0059433.

    PubMed Central  PubMed  CAS  Google Scholar 

  104. Toth, S. Z., Schansker, G., and Strasser, R. J. (2007) Photosynth. Res., 93, 193–203.

    PubMed  CAS  Google Scholar 

  105. Toth, S. Z., Puthur, J. T., Nagy, V., and Garab, G. (2009) Plant Physiol., 149, 1568–1578.

    PubMed Central  PubMed  CAS  Google Scholar 

  106. Toth, S. Z., Nagy, V., Puthur, J. T., Kovacs, L., and Garab, G. (2011) Plant Physiol., 156, 382–392.

    PubMed Central  PubMed  CAS  Google Scholar 

  107. Strasser, B. J. (1997) Photosynth. Res., 52, 147–155.

    CAS  Google Scholar 

  108. Antal, T. K., Volgusheva, A. A., Kukarskih, G. P., Bulychev, A. A., Krendeleva, T. E., and Rubin, A. B. (2006) Physiol. Plant., 128, 360–367.

    CAS  Google Scholar 

  109. Antal, T. K., Krendeleva, T. E., and Rubin, A. B. (2007) Photosynth. Res., 94, 13–22.

    PubMed  CAS  Google Scholar 

  110. Antal, T. K., Kolacheva, A., Maslakov, A., Riznichenko, G. Yu., Krendeleva, T. E., and Rubin, A. B. (2013) Photosynth. Res., 114, 143–154.

    PubMed  CAS  Google Scholar 

  111. Tsimilli-Michael, M., and Strasser, R. J. (2008) in Mycorrhiza: State of the Art, Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics (Varma, A., ed.) 3rd Edn., Springer, Dordrecht, pp. 679–703.

  112. Govindjee (1990) Photosynth. Res., 25, 151–160.

    PubMed  CAS  Google Scholar 

  113. Lavergne, J., and Briantais, J.-M. (1996) in Oxygenic Photosynthesis: the Light Reactions (Ort, D. R., and Yocum, C. F., eds.) Kluwer Academic Publishers, Dordrecht, pp. 265–287.

  114. Danielsson, R., Suorsa, M., Paakkarinen, V., Albertsson, P. A., Styring, S., Aro, E.-M., and Mamedov, F. (2006) J. Biol. Chem., 281, 14241–14249.

    PubMed  CAS  Google Scholar 

  115. Vass, I., and Aro, E.-M. (2008) in Primary Processes of Photosynthesis: Basic Principles and Apparatus. Comprehensive Series in Photochemical and Photobiological Sciences (Renger, G., ed.) Vol. 8, Royal Society of Chemistry, Cambridge, pp. 393–411.

  116. Melis, A., and Homann, P. (1975) Photochem. Photobiol., 21, 431–437.

    CAS  Google Scholar 

  117. Melis, A., and Homann, P. (1976) Photochem. Photobiol., 23, 343–350.

    PubMed  CAS  Google Scholar 

  118. Melis, A. (1978) FEBS Lett., 95, 202–206.

    PubMed  CAS  Google Scholar 

  119. Melis, A., and Duysens, L. N. M. (1979) Photochem. Photobiol., 29, 373–382.

    CAS  Google Scholar 

  120. Dekker, J. P., and Boekema, E. J. (2005) Biochim. Biophys. Acta, 1706, 12–39.

    PubMed  CAS  Google Scholar 

  121. Albertsson, P.-A., Andreasson, E., and Svensson, P. (1990) FEBS Lett., 273, 36–40.

    PubMed  CAS  Google Scholar 

  122. Lazar, D., Tomek, P., Ilik, P., and Naus, J. (2001) Photosynth. Res., 68, 247–257.

    PubMed  CAS  Google Scholar 

  123. Antal, T. K., Krendeleva, T. E., Pashchenko, V. Z., Rubin, A. B., Stensjo, K., Tyystjarvi, E., Los, D. A., Carpentier, R., Nishihara, H., and Allakhverdiev, S. (2012) in State of the Art and Progress in Production of Biohydrogen (Azbarm, N., and Levin, D., eds.) Bentham Science Publishers, Bussum, pp. 25–54.

  124. Maslakov, A., Antal, T. K., and Riznichenko, G. Yu. (2012) in Materials of the Conf. “Synergetics in Science. 8th Kurdyumov’s Reading” [in Russian], Tver, Tverskoi SU, pp. 167–171.

    Google Scholar 

  125. Tomek, P., Ilik, P., Lazar, D., Stroch, M., and Naus, J. (2003) Plant Sci., 164, 665–670.

    CAS  Google Scholar 

  126. Schansker, G., and Strasser, R. J. (2005) Photosynth. Res., 84, 145–151.

    PubMed  CAS  Google Scholar 

  127. Melis, A. (1985) Biochim. Biophys. Acta, 808, 334–342.

    CAS  Google Scholar 

  128. Graan T., and Ort, D. R. (1986) Biochim. Biophys. Acta, 852, 320–330.

    CAS  Google Scholar 

  129. Hsu, B.-D. (1992) Plant Sci., 81, 169–174.

    CAS  Google Scholar 

  130. Strasser, R. J., and Stirbet, A. (1998) Math. Comput. Simul., 48, 3–9.

    Google Scholar 

  131. Diner, B. (1977) Biochim. Biophys. Acta, 466, 247–258.

    Google Scholar 

  132. Joliot, P., Lavergne, J., and Beal, D. (1992) Biochim. Biophys. Acta, 1101, 1–12.

    CAS  Google Scholar 

  133. Hohmann-Marriott, H. M., Takizawa, K., Eaton-Rye, J. J., Mets, L., and Minagawa, J. (2010) FEBS Lett., 584, 1021–1026.

    PubMed  CAS  Google Scholar 

  134. Groom, Q. J., Kramer, D. M., Crofts, A. R., and Ort, D. R. (1993) Photosynth. Res., 36, 205–215.

    PubMed  CAS  Google Scholar 

  135. Field, T. S., Nedbal, L., and Ort, D. R. (1998) Plant Physiol., 116, 1209–1218.

    Google Scholar 

  136. Haldimann, P., and Tsimilli-Michael, M. (2005) Biochim. Biophys. Acta, 1706, 239–249.

    PubMed  CAS  Google Scholar 

  137. Bennoun, P. (1982) Proc. Natl. Acad. Sci. USA, 79, 4352–4356.

    PubMed Central  PubMed  CAS  Google Scholar 

  138. Garab, G., Lajko, F., Mustardy, L., and Marton, L. (1989) Planta, 179, 349–358.

    PubMed  CAS  Google Scholar 

  139. Cournac, L., Josse, E. M., Joet, T., Rumeau, D., Redding, K., Kuntz, M., and Peltier, G. (2000) Phil. Trans. R. Soc. B, 355, 1447–1454.

    PubMed Central  PubMed  CAS  Google Scholar 

  140. Cournac, L., Latouche, G., Cerovic, Z., Redding, K., Ravenel, J., and Peltier, G. (2002) Plant Physiol., 129, 1921–1928.

    PubMed Central  PubMed  CAS  Google Scholar 

  141. Peltier, G., and Cournac, L. (2002) Annu. Rev. Plant Biol., 53, 523–550.

    PubMed  CAS  Google Scholar 

  142. Houille-Vernes, L., Rappaport, F., Wollman, F.-A., Alric, J., and Johnson, X. (2011) Proc. Natl. Acad. Sci. USA, 108, 20820–20825.

    PubMed Central  PubMed  CAS  Google Scholar 

  143. Harris, G. C., and Heber, U. (1993) Plant Physiol., 101, 1169–1173.

    PubMed Central  PubMed  CAS  Google Scholar 

  144. Haldimann, P., and Strasser, R. J. (1999) Photosynth. Res., 62, 67–83.

    CAS  Google Scholar 

  145. Stirbet, A., and Strasser, J. R. (1995) Arch. Sci. Geneve, 48, 41–60.

    CAS  Google Scholar 

  146. Tsimilli-Michael, M., Stamatakis, K., and Papageorgiou, G. C. (2009) Photosynth. Res., 99, 243–255.

    PubMed  CAS  Google Scholar 

  147. Stirbet, A., and Strasser, R. J. (1996) Math. Comp. Sim., 42, 245–253.

    Google Scholar 

  148. Stirbet, A., Govindjee, Strasser, B. J., and Strasser, R. J. (1995) in Photosynthesis: from Light to Biosphere (Mathis, P., ed.) Vol. 2, Kluwer Academic Publishers, Dordrecht, pp. 919–922.

  149. Lebedeva, G. V., Belyaeva, N. E., Demin, O. V., Riznichenko, G. Y., and Rubin, A. B. (2002) Biophysics, 47, 968–980.

    Google Scholar 

  150. Munday, J. C., and Govindjee (1969) Biophys. J., 9, 1–21.

    PubMed Central  PubMed  CAS  Google Scholar 

  151. Schansker, G., Toth, S. Z., and Strasser, R. J. (2005) Biochim. Biophys. Acta, 1706, 250–261.

    PubMed  CAS  Google Scholar 

  152. Schansker, G., Toth, S. Z., and Strasser, R. J. (2006) Biochim. Biophys. Acta, 1757, 787–797.

    PubMed  CAS  Google Scholar 

  153. Kroon, B. M. A., and Thoms, S. (2006) J. Phycol., 42, 593–609.

    CAS  Google Scholar 

  154. Rubin, A. B., and Riznichenko, G. Yu. (2009) in Photosynthesis in silico: Understanding Complexity from Molecules to Ecosystems. Advances in Photosynthesis and Respiration (Laisk, A., Nedbal, L., and Govindjee, eds.) Vol. 29, Springer, Dordrecht, pp. 151–176.

  155. Xin, C.-P., Yang, J., and Zhu, X.-G. (2013) Photosynth. Res., 117, 339–354.

    PubMed  CAS  Google Scholar 

  156. Harbinson, J., and Woodward, F. I. (1987) Plant Cell Env., 10, 131–140.

    CAS  Google Scholar 

  157. Trebst, A., Hart, E., and Draber, W. (1970) Z. Naturforsch., 25b, 1157–1159.

    Google Scholar 

  158. Joly, D., and Carpentier, R. (2007) J. Photochem. Photobiol. B, 88, 43–50.

    PubMed  CAS  Google Scholar 

  159. Joly, D., and Carpentier, R. (2009) Photochem. Photobiol. Sci., 8, 167–173.

    PubMed  CAS  Google Scholar 

  160. Bohme, H. (1978) Eur. J. Biochem., 83, 137–141.

    PubMed  CAS  Google Scholar 

  161. Schottler, M. A., Kirchhoff, H., and Weis, E. (2004) Plant Physiol., 136, 4265–4274.

    PubMed Central  PubMed  Google Scholar 

  162. Asada, K., Schreiber, U., and Heber, U. (1993) Plant Cell Physiol., 34, 39–50.

    CAS  Google Scholar 

  163. Asada, K. (1999) Annu. Rev. Plant Physiol. Plant Mol. Biol., 50, 601–639.

    PubMed  CAS  Google Scholar 

  164. Munekage, Y., Hojo, M., Meurer, J., Endo, T., Tasaka, M., and Shikanai, T. (2002) Cell, 110, 361–371.

    PubMed  CAS  Google Scholar 

  165. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K.-I., Endo, T., Tasaka, M., and Shikanai, T. (2004) Nature, 429, 579–582.

    PubMed  CAS  Google Scholar 

  166. Cardol, P., Gloire, G., Havaux, M., Remacle, C., Matagne, R., and Franck, F. (2003) Plant Physiol., 133, 2010–2020.

    PubMed Central  PubMed  CAS  Google Scholar 

  167. Bukhov, N., and Carpentier, R. (2004) Photosynth. Res., 82, 17–33.

    PubMed  CAS  Google Scholar 

  168. Miyake, C. (2010) Plant Cell Physiol., 51, 1951–1963.

    PubMed  CAS  Google Scholar 

  169. Kramer, D. M., and Evans, J. R. (2011) Plant Physiol., 155, 70–78.

    PubMed Central  PubMed  CAS  Google Scholar 

  170. Ilik, P., Schansker, G., Kotabova, E., Vaczi, P., Strasser, R. J., and Bartak, M. (2006) Biochim. Biophys. Acta, 1757, 12–20.

    PubMed  CAS  Google Scholar 

  171. Hill, R., Larkum, A. W. D., Frankart, C., Kuhl, M., and Ralph, P. J. (2004) Photosynth. Res., 82, 59–72.

    PubMed  CAS  Google Scholar 

  172. Lazar, D. (2013) J. Theor. Biol., 335, 249–264.

    PubMed  CAS  Google Scholar 

  173. Ikegami, I. (1976) Biochim. Biophys. Acta, 449, 245–258.

    PubMed  CAS  Google Scholar 

  174. Malkin, S., and Kok, B. (1966) Biochim. Biophys. Acta, 126, 413–432.

    PubMed  CAS  Google Scholar 

  175. Murata, N., Nishimura, M., and Takamiya, A. (1966) Biochim. Biophys. Acta, 120, 23–33.

    PubMed  CAS  Google Scholar 

  176. Xu, C., Rogers, S. M. D., Goldstein, C., Widholm, J. M., and Govindjee (1989) Photosynth. Res., 21, 93–106.

    PubMed  CAS  Google Scholar 

  177. Pospisil, P., and Dau, H. (2000) Photosynth. Res., 65, 41–52.

    PubMed  CAS  Google Scholar 

  178. Heredia, P., and De Las Rivas, J. (2003) J. Plant Physiol., 160, 1499–1506.

    PubMed  CAS  Google Scholar 

  179. Toth, S. Z., Schansker, G., Garab, G., and Strasser, R. J. (2007) Biochim. Biophys. Acta, 1767, 295–305.

    PubMed  CAS  Google Scholar 

  180. Lavergne, J., Bouchaud, J.-P., and Joliot, P. (1992) Biochim. Biophys. Acta, 1101, 13–22.

    CAS  Google Scholar 

  181. Hsu, B.-D. (1992) Biochim. Biophys. Acta, 1140, 30–36.

    CAS  Google Scholar 

  182. Vermaas, W. F. J., Renger, G., and Dohnt, G. (1984) Biochim. Biophys. Acta, 764, 194–202.

    CAS  Google Scholar 

  183. Avenson, T. J., Kanazawa, A., Cruz, J. A., Takizawa, K., Ettinger, W. E., and Kramer, D. M. (2005) Plant Cell Env., 28, 97–109.

    CAS  Google Scholar 

  184. Foyer, C. H., Neukermans, J., Queval, G., Noctor, G., and Harbinson, J. (2012) J. Exp. Bot., 63, 1637–1661.

    PubMed  CAS  Google Scholar 

  185. Graan, T., and Ort, D. R. (1983) J. Biol. Chem., 258, 2831–2836.

    PubMed  CAS  Google Scholar 

  186. Riznichenko, G. Yu., Lebedeva, G. V., Demin, O. V., and Rubin, A. B. (1999) Kinetic J. Biol. Phys., 25, 177–192.

    CAS  Google Scholar 

  187. Lebedeva, G. V., Belyaeva, N. E., Riznichenko, G. Yu., Rubin, A. B., and Demin, O. V. (2000) J. Phys. Chem., 74, 1702–1710.

    Google Scholar 

  188. Belyaeva, N. E., Lebedeva, G. V., and Riznichenko, G. Yu. (2003) in Mathematics Computer Education (Riznichenko, G. Yu., ed.) [in Russian], Vol. 10, Progress-Traditsiya, Moscow, pp. 263–276.

  189. Belyaeva, N. E., Pashchenko, V. Z., Renger, G., Riznichenko, G. Yu., and Rubin, A. B. (2006) Biophysics, 51, 860–872.

    Google Scholar 

  190. Belyaeva, N. E., Schmitt, F.-J., Paschenko, V. Z., Renger, G., Riznichenko, G. Yu., and Rubin, A. B. (2008) Photosyn. Res., 98, 105–119.

    PubMed  CAS  Google Scholar 

  191. Belyaeva, N. E., Schmitt, F.-J., Paschenko, V. Z., Riznichenko, G. Y., Rubin, A. B., and Renger, G. (2011) BioSystems, 103, 188–195.

    PubMed  CAS  Google Scholar 

  192. Belyaeva, N. E., Bulychev, A. S., Riznichenko, G. Yu., and Rubin, A. B. (2011) Biophysics, 56, 464–477.

    Google Scholar 

  193. Riznichenko, G. Y., Belyaeva, N. E., Kovalenko, I. B., and Rubin, A. B. (2009) Biophysics, 54, 10–22.

    Google Scholar 

  194. Reynolds, J. A., Johnson, E. A., and Tanford, C. (1985) Proc. Natl. Acad. Sci. USA, 82, 6869–6873.

    PubMed Central  PubMed  CAS  Google Scholar 

  195. Bulychev, A. A., and Vredenberg, W. J. (1999) Physiol. Plant., 105, 577–584.

    CAS  Google Scholar 

  196. Vass, I., and Cser, K. (2009) Trends Plant Sci., 14, 200–205.

    PubMed  CAS  Google Scholar 

  197. Vos, M. H., and Van Gorkom, H. J. (1990) Biophys. J., 58, 1547–1555.

    PubMed Central  PubMed  CAS  Google Scholar 

  198. Govindjee and Jursinic, P. (1979) Photochem. Photobiol. Rev., 4, 125–205.

    CAS  Google Scholar 

  199. Butler, W. L. (1972) Proc. Natl. Acad. Sci. USA, 69, 3420–3422.

    PubMed Central  PubMed  CAS  Google Scholar 

  200. Duysens, L. N. M., van der Schatte-Olivier, T. E., and den Haan, G. A. (1972) in Progress in Photobiology (Schenck, G. O., ed.) Proc. VI Int. Congr. on Photobiology, Bochum, 1972, Abstract No. 277.

  201. Antal, T. K., Osipov, V., Matorin, D. N., and Rubin, A. B. (2011) J. Photochem. Photobiol. B, 102, 169–173.

    PubMed  CAS  Google Scholar 

  202. Papageorgiou, G. C., and Govindjee (1967) Biochim. Biophys. Acta, 131, 173–178.

    Google Scholar 

  203. Mohanty, P., Papageorgiou, G. C., and Govindjee (1971) Photochem. Photobiol., 14, 667–682.

    CAS  Google Scholar 

  204. Mohanty, P., Braun, B. Z., and Govindjee (1973) Biochim. Biophys. Acta, 292, 459–476.

    PubMed  CAS  Google Scholar 

  205. Mohanty, P., and Govindjee (1973) Biochim. Biophys. Acta, 305, 95–104.

    PubMed  CAS  Google Scholar 

  206. Mohanty, P., and Govindjee (1973) Plant Cell Physiol., 14, 611–629.

    CAS  Google Scholar 

  207. Mohanty, P., and Govindjee (1974) Plant Biochem. J., 1, 78–106.

    CAS  Google Scholar 

  208. Walker, D. A., Sivak, M. N., Prinsley, R., and Cheesbrough, J. K. (1983) Plant Physiol., 73, 542–549.

    PubMed Central  PubMed  CAS  Google Scholar 

  209. Govindjee and Satoh, K. (1986) in Light Emission by Plants and Bacteria (Govindjee, Amesz, J., and Fork, D. C., eds.) Academic Press, Orlando, pp. 497–537.

  210. Walker, D. A., and Sivak, M. N. (1985) in Regulation of Carbon Partitioning in Photosynthetic Tissue (Heath, R. L., and Preiss, J., eds.) Proc. 8th Ann. Symp. in Plant Physiology, 11–12 January 1985, University of California, Riverside, American Society of Plant Physiology, Rockville, Maryland, pp. 93–108.

  211. Demmig-Adams, B., Adams, W. W., III, Barker, D. H., Logan, B. A., Bowling, D. R., and Verhoeven, A. S. (1996) Physiol. Plant., 98, 254–264.

    Google Scholar 

  212. Baker, N. R. (2008) Annu. Rev. Plant Biol., 59, 89–113.

    PubMed  CAS  Google Scholar 

  213. Bradbury, M., and Baker, N. R. (1984) Biochim. Biophys. Acta, 765, 275–281.

    CAS  Google Scholar 

  214. Niyogi, K. K., and Truong, T. B. (2013) Curr. Opin. Plant Biol., c16, 1–8.

    Google Scholar 

  215. Papageorgiou, G. C., and Govindjee (2014) in Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria (Demmig-Adams, B., Garab, G., Adams, W. W., III, and Govindjee, eds.) Springer, Dordrecht (in press).

  216. Adams, W. W., III, Muller, O., Cohu, C. M., and Demmig-Adams, B. (2014) in Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria (Demmig-Adams, B., Garab, G., Adams, W. W., III, and Govindjee, eds.) Springer, Dordrecht (in press).

  217. Kalituho, L., Beran, K. C., and Jahns, P. (2007) Plant Physiol., 143, 1861–1870.

    PubMed Central  PubMed  CAS  Google Scholar 

  218. Kana, R., Kotabova, E., Komarek, O., Sediva, B., Papageorgiou, G. C., Govindjee, and Prasil, O. (2012) Biochim. Biophys. Acta, 1817, 1237–1247.

    PubMed  CAS  Google Scholar 

  219. Kodru, S., Nellaepalli, S., Malavath, T., Devadasu, E., Subramanyam, R., and Govindjee (2013) Abstract of Poster #146, 16th Int. Photosynthesis Congr., St. Louis, Mo, USA, August.

    Google Scholar 

  220. Holzwarth, A. R., Lenk, D., and Jahns, P. (2013) Biochim. Biophys. Acta, 1827, 786–792.

    PubMed  CAS  Google Scholar 

  221. Muller, P., Li, X.-P., and Niyogi, K. K. (2001) Plant Physiol., 125, 1558–1566.

    PubMed Central  PubMed  CAS  Google Scholar 

  222. Nilkens, M., Kress, E., Lambrev, P., Miloslavina, Y., Muller, M., Holzwarth, A. R., and Jahns, P. (2010) Biochim. Biophys. Acta, 1797, 466–475.

    PubMed  CAS  Google Scholar 

  223. Minagawa, J. (2011) Biochim. Biophys. Acta, 1807, 897–905.

    PubMed  CAS  Google Scholar 

  224. Matsubara, S., and Chow, W. S. (2004) Proc. Natl. Acad. Sci. USA, 101, 18234–18239.

    PubMed Central  PubMed  CAS  Google Scholar 

  225. Apel, K., and Hirt, H. (2004) Annu. Rev. Plant Biol., 55, 373–399.

    PubMed  CAS  Google Scholar 

  226. Hakala, M., Tuominen, I., Keranen, M., Tyystjarvi, T., and Tyystjarvi, E. (2005) Biochim. Biophys. Acta, 1706, 68–80.

    PubMed  CAS  Google Scholar 

  227. Demmig-Adams, B., and Adams, W. W., III (2006) New Phytol., 172, 11–21.

    PubMed  CAS  Google Scholar 

  228. Vass, I. (2011) Physiol. Plant., 142, 6–16.

    PubMed  CAS  Google Scholar 

  229. Allahverdieva, Y., and Aro, E.-M. (2012) in Photosynthesis: Plastid Biology, Energy Conversion and Carbon Assimilation, Advances in Photosynthesis and Respiration (Eaton-Rye, J. J., Tripathy, B. C., and Sharkey, T. D., eds.) Vol. 34, Springer, Dordrecht, pp. 275–297.

  230. Tyystjarvi, E. (2013) Int. Rev. Cell Mol. Biol., 300, 243–303.

    PubMed  CAS  Google Scholar 

  231. Briantais, J.-M., Vernotte, C., Picaud, M., and Krause, G. H. (1979) Biochim. Biophys. Acta, 548, 128–138.

    PubMed  CAS  Google Scholar 

  232. Krause, G. H., and Jahns, P. (2004) in Chlorophyll Fluorescence: a Signature of Photosynthesis. Advances in Photosynthesis and Respiration (Papageorgiou, G. C., and Govindjee, eds.) Vol. 19, Springer, Dordrecht, The Netherlands, pp. 463–495.

  233. Barber, J. (2004) Photosynth. Res., 80, 137–144.

    PubMed  CAS  Google Scholar 

  234. Murata, N., and Sugahara, K. (1969) Biochim. Biophys. Acta, 189, 182–192.

    PubMed  CAS  Google Scholar 

  235. Wraight, C. A., and Crofts, A. R. (1970) Eur. J. Biochem., 17, 319–327.

    PubMed  CAS  Google Scholar 

  236. Ruban, A. V., Johnson, M. P., and Duffy, C. D. P. (2012) Biochim. Biophys. Acta, 1817, 167–181.

    PubMed  CAS  Google Scholar 

  237. Zaks, J., Amarnath, K., Sylak-Glassman, E. J., and Fleming, G. R. (2013) Photosynth. Res., 116, 389–409.

    PubMed Central  PubMed  CAS  Google Scholar 

  238. Goss, R., Oroszi, S., and Wilhelm, C. (2007) Physiol. Plant., 131, 496–507.

    PubMed  CAS  Google Scholar 

  239. Johnson, M. P., Perez-Bueno, M. L., Zia, A., Horton, P., and Ruban, A. V. (2009) Plant Physiol., 149, 1061–1075.

    PubMed Central  PubMed  CAS  Google Scholar 

  240. Li, X. P., Bjorkman, O., Shih, C., Grossman, A. R., Rosenquist, M., Jansson, S., and Niyogi, K. K. (2000) Nature, 403, 391–395.

    PubMed  CAS  Google Scholar 

  241. Peers, G., Truong, T. B., Ostendorf, E., Busch, A., Elrad, D., Grossman, A. R., Hippler, M., and Niyogi, K. K. (2009) Nature, 462, 518–522.

    PubMed  CAS  Google Scholar 

  242. Bonente, G., Ballottari, M., Truong, T. B., Morosinotto, T., Ahn, T. K., Fleming, G. R., Niyogi, K. K., and Bassi, R. (2010) PLoS Biol., e1000577.

    Google Scholar 

  243. Zhu, S. H., and Green, B. R. (2010) Biochim. Biophys. Acta, 1797, 1449–14457.

    PubMed  CAS  Google Scholar 

  244. Wilson, A., Ajlani, G., Verbavatz, J.-M., Vass, I., Kerfeld, C. A., and Kirilovsky, D. (2006) Plant Cell, 18, 992–107.

    PubMed Central  PubMed  CAS  Google Scholar 

  245. Kirilovsky, D., Kana, R., and Prasil, O. (2014) in Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria (Demmig-Adams, B., Garab, G., Adams, W. W., III., and Govindjee, eds.) Springer, Dordrecht (in press).

  246. Gilmore, A. M., Hazlett, T. L., and Govindjee (1995) Proc. Natl. Acad. Sci. USA, 92, 2273–2277.

    PubMed Central  PubMed  CAS  Google Scholar 

  247. Gilmore, A. M. (1997) Physiol. Plant., 99, 197–209.

    CAS  Google Scholar 

  248. Sivak, M. N., Heber, U., and Walker, D. A. (1985) Planta, 163, 419–423.

    PubMed  CAS  Google Scholar 

  249. Anderson, J. M., Chow, W. S., and De Las Rivas, J. (2008) Photosynth. Res., 98, 575–587.

    PubMed  CAS  Google Scholar 

  250. Johnson, M. P., Brain, A. P. R., and Ruban, A. V. (2011) Plant Sign. Behav., 6, 1386–1390.

    CAS  Google Scholar 

  251. Mullineaux, C. W., Ruban, A. V., and Horton, P. (1994) Biochim. Biophys. Acta, 1185, 119–123.

    CAS  Google Scholar 

  252. Holzwarth, A. R., Miloslavina, Y., Nilkens, M., and Jahns, P. (2009) Chem. Phys. Lett., 483, 262–267.

    CAS  Google Scholar 

  253. Demmig-Adams, B., Adams, W. W., III, Heber, U., Neimanis, S., Winter, K., Kruger, A., Czygan, F.-C., Bilger, W., and Bjorkman, O. (1990) Plant Physiol., 92, 293–301.

    PubMed Central  PubMed  CAS  Google Scholar 

  254. Jahns, P., Latowski, D., and Strzalka, K. (2009) Biochim. Biophys. Acta, 1787, 3–14.

    PubMed  CAS  Google Scholar 

  255. Bassi, R., Pineau, B., Dainese, P., and Marquardt, J. (1993) Eur. J. Biochem., 212, 297–303.

    PubMed  CAS  Google Scholar 

  256. Gilmore, A. M., Hazlett, T. L., Debrunner, P. G., and Govindjee (1996) Photosynth. Res., 48, 171–187.

    PubMed  CAS  Google Scholar 

  257. Niyogi, K. K., Grossman, A. R., and Bjorkman, O. (1998) Plant Cell, 10, 1121–1134.

    PubMed Central  PubMed  CAS  Google Scholar 

  258. Holub, O., Seufferheld, M. J., Gohlke, C., Govindjee, Heiss, G. J., and Clegg, R. M. (2007) J. Microsc., 225, 90–120.

    Google Scholar 

  259. Johnson, M. P., and Ruban, A. V. (2011) J. Biol. Chem., 286, 19973–19981.

    PubMed Central  PubMed  CAS  Google Scholar 

  260. Ahn, T. K., Avenson, T. J., Ballottari, M., Cheng, Y. C., Niyogi, K. K., Bassi, R., and Fleming, G. R. (2008) Science, 320, 794–797.

    PubMed  CAS  Google Scholar 

  261. Duffy, C. D. P., Chmeliov, J., Macernis, M., Sulskus, J., Valkunas, L., and Ruban, A. V. (2013) J. Phys. Chem. B, 117, 10974–10986.

    PubMed  CAS  Google Scholar 

  262. Muller, M. G., Lambrev, P., Reus, M., Wientjes, E., Croce, R., and Holzwarth, A. R. (2010) Chemphyschem., 11, 1289–1296.

    PubMed  Google Scholar 

  263. Huner, N. P. A., Ivanov, A. G., Sane, P. V., Pocock, T., Krol, M., Balseris, A., Rosso, D., Savitch, L. V., Hurry, V. M., and Oquist, G. (2008) in Photoprotection, Photoinhibition, Gene Regulation, and Environment (Demmig-Adams, B., Adams, W. W., III and Mattoo, A. K., eds.) Springer, pp. 155–173.

  264. Ruban, A. V., Young, A. J., and Horton, P. (1993) Plant Physiol., 102, 741–750.

    PubMed Central  PubMed  CAS  Google Scholar 

  265. Tikkanen, M., Suorsa, M., Gollan, P. J., and Aro, E.-M. (2012) FEBS Lett., 586, 2911–2916.

    PubMed  CAS  Google Scholar 

  266. Malkin, S., Wong, D., Govindjee, and Merkelo, H. (1980) Photobiochem. Photobiophys., 1, 83–89.

    CAS  Google Scholar 

  267. Takizawa, K., Cruz, J. A., Kanazawa, A., and Kramer, D. M. (2007) Biochim. Biophys. Acta, 1767, 1233–1244.

    PubMed  CAS  Google Scholar 

  268. Johnson, M. P., Zia, A., and Ruban, A. V. (2012) Planta, 235, 193–204.

    PubMed  CAS  Google Scholar 

  269. Hill, A. V. (1910) J. Physiol., 40, iv–vii.

    Google Scholar 

  270. Laisk, A., Oja, V., Rasulov, B., Eichelmann, H., and Sumberg, A. (1997) Plant Physiol., 115, 803–815.

    PubMed Central  PubMed  CAS  Google Scholar 

  271. Laisk, A., Eichelmann, H., Oja, V., Eatherall, A., and Walker, D. A. (1989) Proc. R. Soc. Lond. B, 237, 389–415.

    CAS  Google Scholar 

  272. Laisk, A. (1993) Proc. R. Soc. Lond. B, 251, 243–251.

    CAS  Google Scholar 

  273. Cramer, W. A., Yamashita, E., and Hasan, S. S. (2013) in Encyclopedia of Biological Chemistry (Lane, M. D., and Lennarz, W. J., eds.) 2nd Edn., Vol. 4, Academic Press, Waltham MA, pp. 167–171.

  274. Usuda, H., Ku, M. S. B., and Edwards, G. E. (1984) Plant Physiol., 76, 238–243.

    PubMed Central  PubMed  CAS  Google Scholar 

  275. Lambrev, P. H., Miloslavina, Y., Jahns, P., and Holzwarth, A. R. (2012) Biochim. Biophys. Acta, 1817, 760–769.

    PubMed  CAS  Google Scholar 

  276. Serodio, J., and Lavaud, J. (2011) Photosynth. Res., 108, 61–76.

    PubMed  CAS  Google Scholar 

  277. Ebenhoh, O., Houwaart, T., Lokstein, H., Schleded, S., and Tirok, K. (2011) Biosystems, 103, 196–204.

    PubMed  Google Scholar 

  278. Pfundel, E., and Dilley, R. A. (1993) Plant Physiol., 101, 65–71.

    PubMed Central  PubMed  CAS  Google Scholar 

  279. Seelert, H., Poetsch, A., Dencher, N. A., Engel, A., Stahlberg, H., and Muller, D. J. (2000) Nature, 405, 418–419.

    PubMed  CAS  Google Scholar 

  280. Zhu, X.-G., De Sturler, E., and Long, S. P. (2007) Plant Physiol., 145, 513–526.

    PubMed Central  PubMed  CAS  Google Scholar 

  281. Vollmar, M., Schilieper, D., Winn, M., and Buechner, C. (2009) J. Biol. Chem., 284, 18228–18235.

    PubMed Central  PubMed  CAS  Google Scholar 

  282. Zaks, J., Amarnath, K., Kramer, D. M., Niyogi, K. K., and Fleming, G. R. (2012) Proc. Natl. Acad. Sci. USA, 109, 15757–15762.

    PubMed Central  PubMed  CAS  Google Scholar 

  283. Li, X.-P., Muller-Moule, P., Gilmore, A. M., and Niyogi, K. K. (2002) Proc. Natl. Acad. Sci. USA, 99, 15222–15227.

    PubMed Central  PubMed  CAS  Google Scholar 

  284. Cruz, J. A., Sacksteder, C. A., Kanazawa, A., and Kramer, D. M. (2001) Biochemistry, 40, 1226–1237.

    PubMed  CAS  Google Scholar 

  285. Kramer, D. M., Avenson, T. J., and Edwards, G. E. (2004) Trends Plant Sci., 9, 349–357.

    PubMed  CAS  Google Scholar 

  286. El-Bissati, K., Delphin, E., Murata, N., Etienne, A.-L., and Kirilovsky, D. (2000) Biochim. Biophys. Acta, 1457, 229–242.

    PubMed  CAS  Google Scholar 

  287. Kirilovsky, D. (2007) Photosynth. Res., 93, 7–16.

    PubMed  CAS  Google Scholar 

  288. Stadnichuk, I. N., Yanyushin, M. F., Zharmukhamedov, S. K., Maksimov, E. G., Muronets, E. M., and Pashchenko, V. Z. (2011) Dokl. Biochem. Biophys., 439, 167–170.

    PubMed  CAS  Google Scholar 

  289. Kirilovsky, D., and Kerfeld, C. A. (2012) Biochim. Biophys. Acta, 1817, 158–166.

    PubMed  CAS  Google Scholar 

  290. Kirilovsky, D., and Kerfeld, C. A. (2013) Photochem. Photobiol. Sci., 12, 1135–1143.

    PubMed  CAS  Google Scholar 

  291. Campbell, D., Hurry, V., Clarke, A., Gustafsson, P., and Oquist, G. (1998) Microbiol. Mol. Biol. Rev., 6, 667–683.

    Google Scholar 

  292. Boulay, C., Abasova, L., Six, C., Vass, I., and Kirilovsky, D. (2008) Biochim. Biophys. Acta, 1777, 1344–1354.

    PubMed  CAS  Google Scholar 

  293. Gorbunov, M. Y., Kuzminov, F. I., Fadeev, V. V., Kim, J. D., and Falkowski, P. G. (2011) Biochim. Biophys. Acta, 1807, 1591–1599.

    PubMed  CAS  Google Scholar 

  294. Weis, E., and Berry, J. A. (1987) Biochim. Biophys. Acta, 894, 198–208.

    CAS  Google Scholar 

  295. Krause, G. H., and Weis, E. (1991) Ann. Rev. Plant Physiol. Plant Mol. Biol., 42, 313–349.

    CAS  Google Scholar 

  296. Vass, I., Styring, S., Hundal, T., Koivuniemi, A., Aro, E.-M., and Andersson, B. (1992) Proc. Natl. Acad. Sci. USA, 89, 1408–1412.

    PubMed Central  PubMed  CAS  Google Scholar 

  297. Walters, R. G., and Horton, P. (1993) Photosynth. Res., 36, 119–139.

    PubMed  CAS  Google Scholar 

  298. Bukhov, N. G., Heber, U., Wiese, C., and Shuvalov, V. A. (2001) Planta, 212, 749–758.

    PubMed  CAS  Google Scholar 

  299. Ivanov, A. G., Sane, P. V., Zeinalov, Y., Malmberg, G., Gardestrom, P., Huner, N. P. A., and Oquist, G. (2001) Planta, 213, 575–585.

    PubMed  CAS  Google Scholar 

  300. Ivanov, A. G., Sane, P. V., Zeinalov, Y., Simidjiev, I., Huner, N. P. A., and Oquist, G. (2002) Planta, 215, 457–465.

    PubMed  CAS  Google Scholar 

  301. Sane, P. V., Ivanov, A. G., Sveshnikov, D., Huner, N. P. A., and Oquist, G. (2002) J. Biol. Chem., 277, 32739–32745.

    PubMed  CAS  Google Scholar 

  302. Sane, P. V., Ivanov, A. G., Hurry, V. M., Huner, N. P. A., and Oquist, G. (2003) Plant Physiol., 132, 2144–2151.

    PubMed Central  PubMed  CAS  Google Scholar 

  303. Ivanov, A. G., Hurry, V., Sane, P. V., Oquist, G., and Huner, N. P. A. (2008) J. Plant Biol., 51, 85–96.

    CAS  Google Scholar 

  304. Oquist, G., and Huner, N. P. A. (2003) Annu. Rev. Plant Biol., 54, 329–355.

    PubMed  Google Scholar 

  305. Huner, N. P. A., Oquist, G., and Sarhan, F. (1998) Trends Plant Sci., 3, 224–230.

    Google Scholar 

  306. Klimov, V. V., Klevanik, A. V., Shuvalov, V. A., and Krasnovsky, A. A. (1977) FEBS Lett., 82, 183–186.

    PubMed  CAS  Google Scholar 

  307. Holzwarth, A. R. (1991) in Chlorophylls (Scheer, H., ed.) CRC Press, Boca Raton, pp. 1125–1151.

  308. Dau, H., and Sauer, K. (1992) Biochim. Biophys. Acta, 1102, 91–106.

    CAS  Google Scholar 

  309. Leibl, W., Breton, J., Deprez, J., and Trissl, H.-W. (1989) Photosynth. Res., 22, 257–275.

    PubMed  CAS  Google Scholar 

  310. Murata, N. (1969) Biochim. Biophys. Acta, 172, 242–251.

    PubMed  CAS  Google Scholar 

  311. Murata, N. (2009) Photosynth. Res., 99, 155–160.

    PubMed  CAS  Google Scholar 

  312. Bonaventura, C., and Myers, J. (1969) Biochim. Biophys. Acta, 189, 366–383.

    PubMed  CAS  Google Scholar 

  313. Allen, J. F. (1992) Biochim. Biophys. Acta, 1098, 275–335.

    PubMed  CAS  Google Scholar 

  314. Allen, J. F. (2003) Science, 299, 1530–1532.

    PubMed  CAS  Google Scholar 

  315. Kargul, J., and Barber, J. (2008) FEBS Lett., 275, 1056–1068.

    CAS  Google Scholar 

  316. Lemeille, S., and Rochaix, J. D. (2010) Photosynth. Res., 106, 33–46.

    PubMed  CAS  Google Scholar 

  317. Bennett, J., Steinback, K. E., and Arntzen, C. J. (1980) Proc. Natl. Acad. Sci. USA, 77, 5253–5257.

    PubMed Central  PubMed  CAS  Google Scholar 

  318. Allen, J. F., Bennett, J., Steinback, K. E., and Arntzen, C. J. (1981) Nature, 291, 25–29.

    CAS  Google Scholar 

  319. Wollman, F.-A., and Lemaire, C. (1988) Biochim. Biophys. Acta, 933, 85–94.

    CAS  Google Scholar 

  320. Iwai, M., Takizawa, K., Tokutsu, R., Okamuro A., Takahashi, Y., and Minagawa, J. (2010) Nature, 464, 1210–1213.

    PubMed  CAS  Google Scholar 

  321. Galka, P., Santabarbara, S., Khuong, T. T. H., Degand, H., Morsomme, P., Jennings, R. C., Boekema, E. J., and Caffarri, S. (2012) Plant Cell, 24, 2963–2978.

    PubMed Central  PubMed  CAS  Google Scholar 

  322. Takahashi, H., Clowez, S., Wollman, F.-A., Vallon, O., and Rappaport, F. (2013) Nature Commun., DOI: 10.1038/ncomms2954.

    Google Scholar 

  323. Mullineaux, C. W., Tobin, M. J., and Jones, G. R. (1997) Nature, 390, 421–424.

    CAS  Google Scholar 

  324. Allen, J. F., and Mullineaux, C. W. (2004) in Chlorophyll a Fluorescence: a Signature of Photosynthesis. Advances in Photosynthesis and Respiration (Papageorgiou, G. C., and Govindjee, eds.) Vol. 19, Springer, Dordrecht, pp. 447–461.

  325. Papageorgiou, G. C., and Stamatakis, K. (2004) in Chlorophyll a Fluorescence: a Signature of Photosynthesis. Advances in Photosynthesis and Respiration (Papageorgiou, G. C., and Govindjee, eds.) Vol. 19, Springer, Dordrecht, pp. 663–678.

  326. Allen, J. F., Sanders, C. E., and Holmes, N. G. (1985) FEBS Lett., 193, 271–275.

    CAS  Google Scholar 

  327. Yang, S., Su, Z., Li, H., Feng, J., Xie, J., Xia, A., Gong, Y., and Zhao, J. (2007) Biochim. Biophys. Acta, 1767, 15–21.

    PubMed  CAS  Google Scholar 

  328. Kana, R. (2013) Photosynth. Res., 116, 465–479.

    PubMed  CAS  Google Scholar 

  329. Li, D., Xie, J., Zhao, J., Xia, A., Li, D., and Gong, Y. (2004) Biochim. Biophys. Acta, 1608, 114–121.

    PubMed  CAS  Google Scholar 

  330. Murata, N., Mohanty, P. S., Hayashi, H., and Papageorgiou, G. C. (1992) FEBS Lett., 296, 187–189.

    PubMed  CAS  Google Scholar 

  331. Mullineaux, C. W., and Allen, J. F. (1986) FEBS Lett., 205, 155–160.

    CAS  Google Scholar 

  332. Mao, H.-B., Li, G.-F., Ruan, X., Wu, Q.-Y., Gong, Y.-D., Zhang, X.-F., and Zhao, N.-M. (2002) FEBS Lett., 519, 82–86.

    PubMed  CAS  Google Scholar 

  333. Bulte, L., and Wollman, F. A. (1990) Biochim. Biophys. Acta, 1016, 253–258.

    CAS  Google Scholar 

  334. Bulte, L., Gans, P., Rebeille, F., and Wollman, F. A. (1990) Biochim. Biophys. Acta, 1020, 72–80.

    CAS  Google Scholar 

  335. Volgusheva, A. A., Zagidullin, V. E., Antal, T. K., Korvatovsky, B. N., Krendeleva, T. E., Paschenko, V. Z., and Rubin, A. B. (2007) Biochim. Biophys. Acta, 1767, 559–564.

    PubMed  CAS  Google Scholar 

  336. Volgusheva, A. A., Kukarskikh, G. P., Antal, T. K., Lavrukhina, O. G., Krendeleva, T. E., and Rubin, A. B. (2008) Biofizika, 53, 787–796.

    PubMed  CAS  Google Scholar 

  337. Nellaepalli, S., Mekala, N. R., Zsiros, O., Mohanty, P., and Subramanyam, R. (2011) Biochim. Biophys. Acta, 1807, 1177–1184.

    PubMed  CAS  Google Scholar 

  338. Nellaepalli, S., Kodru, S., Tirupathi, M., and Subramanyam, R. (2012) PLoS ONE, 7, e49839; doi:10.1371/journal.pone.004983.

    PubMed Central  PubMed  CAS  Google Scholar 

  339. Gordienko, T. V., and Karavaev, V. A. (2003) Biol. Bull., 30, 34–39.

    CAS  Google Scholar 

  340. Jablonsky, J., Bauwe, H., and Wolkenhauer, O. (2011) BMC Sys. Biol., 5, 185.

    Google Scholar 

  341. Farquhar, G. D., von Caemmerer, S., and Berry, J. A. (1980) Planta, 149, 78–90.

    PubMed  CAS  Google Scholar 

  342. Zhu, X.-G., Long, S. P., and Ort, D. R. (2010) Annu. Rev. Plant Biol., 61, 235–261.

    PubMed  CAS  Google Scholar 

  343. Van der Veen, R. (1949) Physiol. Plant., 2, 217–234.

    Google Scholar 

  344. Van der Veen, R. (1949) Physiol. Plant., 2, 287–296.

    Google Scholar 

  345. Walker, D. A. (1992) Photosynth. Res., 34, 387–395.

    PubMed  CAS  Google Scholar 

  346. Siebke, K., and Weis, E. (1995) Photosynth. Res., 45, 225–237.

    PubMed  CAS  Google Scholar 

  347. Ferimazova, N., Kupper, H., Nedbal, L., and Trtilek, M. (2002) Photochem. Photobiol., 76, 501–508.

    PubMed  CAS  Google Scholar 

  348. Ogawa, T. (1982) Biochim. Biophys. Acta, 681, 103–109.

    CAS  Google Scholar 

  349. Fridlyand, L. E. (1998) J. Theor. Biol., 193, 739–741.

    PubMed  CAS  Google Scholar 

  350. Buschmann, P., and Gradmann, D. (1997) J. Theor. Biol., 188, 323–332.

    CAS  Google Scholar 

  351. Laisk, A. (1977) Kinetics of Photosynthesis and Photorespiration in C3 Plants [in Russian], Nauka, Moscow, p. 196.

    Google Scholar 

  352. Giersch, C. (1986) Arch. Biochem. Biophys., 245, 263–270.

    PubMed  CAS  Google Scholar 

  353. Laisk, A., and Walker, D. A. (1986) Proc. R. Soc. Lond. B, 227, 281–302.

    CAS  Google Scholar 

  354. Laisk, A., Siebke, K., Gerst, U., Eichelmann, H., Oja, V., and Heber, U. (1991) Planta, 185, 554–562.

    PubMed  CAS  Google Scholar 

  355. Ryde-Pettersson, U. (1991) Eur. J. Biochem., 198, 613–619.

    PubMed  CAS  Google Scholar 

  356. Kukushkin, A. K. (1997) Biofizika, 42, 1224–1234.

    CAS  Google Scholar 

  357. Karavaev, V. A., and Kukushkin, A. K. (1993) Biofizika, 38, 958–975.

    CAS  Google Scholar 

  358. Rovers, W., and Giersch, C. (1995) Biosystems, 35, 63–73.

    PubMed  CAS  Google Scholar 

  359. Khuznetsova, S. A., and Kukushkin, A. K. (1999) Biofizika, 44, 448–454.

    CAS  Google Scholar 

  360. Lazar, D., Kana, R., Klinkovsky, T., and Naus, J. (2005) Photosynthetica, 43, 13–27.

    CAS  Google Scholar 

  361. Giersch, C., Sivak, M. N., and Walker, D. A. (1991) Proc. R. Soc. Lond. B, 245, 77–83.

    CAS  Google Scholar 

  362. Demmig-Adams, B., Garab, G., Adams, W. W., III, and Govindjee (eds.) (2014) Non-Photochemical Quenching and Energy Dissipation in Plants, Algae and Cyanobacteria, Springer, Dordrecht (in press).

    Google Scholar 

  363. Steffen, R., Christen, G., and Renger, G. (2001) Biochemistry, 40, 173–180.

    PubMed  CAS  Google Scholar 

  364. Steffen, R., Eckert, H.-J., Kelly, A. A., Dormann, P., and Renger, G. (2005) Biochemistry, 44, 3123–3133.

    PubMed  CAS  Google Scholar 

  365. Belyaeva, N. E. (2004) PhD thesis [in Russian], Moscow.

  366. Baniulis, D., Yamashita, E., Zhang, H., Hasan, S. S., and Cramer, W. A. (2008) Photochem. Photobiol., 84, 1349–1358.

    PubMed  CAS  Google Scholar 

  367. Hasan, S. S., Yamashita, E., Baniulis, D., and Cramer, W. A. (2013) Proc. Natl. Acad. Sci. USA, 110, 4297–4302.

    PubMed Central  PubMed  CAS  Google Scholar 

  368. Papageorgiou, G. C., Garcia-Mendoza, E., Matsubara, S., and Govindjee (2013) Paper presented at Int. Conf. on “Photosynthesis Research for Sustainability, June 5–9, 2013 (for information on the conference, see Allakhverdiev, S. I., Huseynova, I. M., and Govindjee (2013) Photosynth. Res., 118, 297–307).

    Google Scholar 

  369. Ferrante, P., Ballottari, M., Bonente, G., Giuliano, G., and Bassi, R. (2012) J. Biol. Chem., 287, 16276–16288.

    PubMed Central  PubMed  CAS  Google Scholar 

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Published in Russian in Biokhimiya, 2014, Vol. 79, No. 4, pp. 379–412.

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Stirbet, A., Riznichenko, G.Y., Rubin, A.B. et al. Modeling chlorophyll a fluorescence transient: Relation to photosynthesis. Biochemistry Moscow 79, 291–323 (2014). https://doi.org/10.1134/S0006297914040014

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