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Current views on the function of the violaxanthin cycle (development of ideas put forward by D.I. Sapozhnikov)

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Abstract

David Iosifovich Sapozhnikov (17.06.1911–23.11.1983), a well-known plant physiologist and evolutionist would have been 100 this year. Sapozhnikov investigated the role of carotenoids in plant life and acquired worldwide recognition for his discovery of the violaxanthin cycle. This review considers the most important Sapozhnikov’s results and hypotheses elaborated by subsequent research, as well as the modern concepts in this area of investigation.

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Abbreviations

Ax:

antheraxanthin

NPQ:

non-photochemical quenching of chlorophyll fluorescence

PSII:

photosystem II

VC:

violaxanthin cycle

VDE:

violaxanthin deepoxidase

Vx:

violaxanthin

ZE:

zeaxanthin epoxidase

Zx:

zeaxanthin

References

  1. Sapozhnikov, D.I., Evolution of Photosynthesis, Sov. Bot., 1939, no. 5, pp. 100–112.

  2. Sapozhnikov, D.I., Mechanism of Photosynthesis and Its Evolution, Tr. Bot. Inst. Akad. Nauk SSSR, Ser. 4, Experimental Botany, 1951, no. 8, pp. 106–139.

  3. Dorough, C.D. and Calvin, M., The Path of Oxygen in Photosynthesis, J. Am. Chem. Soc., 1951, vol. 73, pp. 2362–2365.

    Article  CAS  Google Scholar 

  4. Sapozhnikov, D.I., Bronshtein, I.A., and Krasovskaya, T.A., Usage of Paper Chromatography Method for Pigment Analysis in Green Leaf Plastids, Biokhimiya, 1955, vol. 20, no. 3, pp. 286–291.

    CAS  Google Scholar 

  5. Sapozhnikov, D.I., Krasovskaya, T.A., and Maevskaya, A.N., Changes in the Ratio of Main Carotenoids in Green Leaf Plastids under Light Action, Dokl. Akad. Nauk SSSR, 1957, vol. 113, no. 2, pp. 465–467.

    CAS  Google Scholar 

  6. Sapozhnikov, D.I., Eidelman, Z.M., and Bazhanova, N.V., The Role of Carotenoids in Photosynthesis, Tr. Bot. Inst. Akad. Nauk SSSR, Ser. 4, Experimental Botany, 1962, no. 15, pp. 43–52.

  7. Hager, A. and Perz, H., Veranderung der Lichtabsorbtion eines Carotinoids im Enzym (De-Epoxidase)-Substrate (Violaxanthin)-Komplex, Planta, 1970, vol. 93, pp. 314–322.

    Article  CAS  Google Scholar 

  8. Siefermann, D. and Yamamoto, H.Y., Light Induced De-Epoxidation of Violaxanthin in Lettuce Chloroplasts: 3. Reaction Kinetics and Effect of Light Intensity on De-Epoxidase Activity and Substrate Availability, Biochim. Biophys. Acta, 1974, vol. 357, pp. 144–150.

    Article  PubMed  CAS  Google Scholar 

  9. Pfundel, E.E. and Bilger, W., Regulation and Possible Function of Violaxanthin Cycle, Photosynth. Res., 1994, vol. 42, pp. 89–109.

    Article  Google Scholar 

  10. Eskling, M., Arvidsson, P.O., and Akerlund, H.E., The Xanthophyll Cycle, Its Regulation and Components, Physiol. Plant., 1997, vol. 100, pp. 806–816.

    Article  CAS  Google Scholar 

  11. Latowski, D., Kostecka-Gugała, A., and Strzałka, K., Effect of the Temperature on Violaxanthin De-Epoxidation: Comparison of the In Vivo and Model Systems, Russ. J. Plant Physiol., 2003, vol. 50, pp. 173–177.

    Article  CAS  Google Scholar 

  12. Popova, I.A., Ryzhova, E.F., and Sapozhnikov, D.I., Some Properties of the Reaction of Violaxanthin De-Epoxidation, Dokl. Akad. Nauk SSSR, 1971, vol. 201, no. 2, pp. 494–496.

    CAS  Google Scholar 

  13. Siefermann, D., Über den Zusammenhang von Xanthophyll-Cyclus und Photosynthese bei Lemna gibba L., PhD Diss. Tübingen: Eberhard Karls Universität, 1973.

    Google Scholar 

  14. Sapozhnikov, D.I., Gabr, M.A., and Maslova, T.G., Position of the Light Threshold of the De-Epoxidation Reaction of Violaxanthin in Leaves of Protophilous and Shade Tolerant Plants, Bot. Zh. (Leningrad), 1973, vol. 58, pp. 1205–1209.

    CAS  Google Scholar 

  15. Sapozhnikov, D.I., Popova, I.A., and Ryzhova, E.F., Effect of Salicylaldoxim on Light Relations in the Violaxanthin Cycle, Dokl. Akad. Nauk SSSR, 1973, vol. 207, no. 6, pp. 1290–1292.

    Google Scholar 

  16. Maslova, T.G., Koroleva, O.Ya., Zelenskii, M.I., Gabr, M.A., and Sapozhnikov, D.I., Inhibition of Oxygen Evolution in the Process of Photosynthesis after Violaxanthin Cycle Damage, Sov. Plant Physiol., 1978, vol. 25, pp. 91–96.

    CAS  Google Scholar 

  17. Sapozhnikov, D.I., Investigation of the Violaxanthin Cycle, Pure Appl. Chem., 1973, vol. 35, pp. 47–61.

    Article  PubMed  CAS  Google Scholar 

  18. Sapozhnikov, D.I., Gabr, M.A., and Maslova, T.G., Effect of Anaerobiosis and Some Metabolites on the Violaxanthin Cycle in Plant Leaves, Sov. Plant Physiol., 1976, vol. 23, pp. 31–35.

    CAS  Google Scholar 

  19. Siefermann-Harms, D., Carotenoids in Photosynthesis: 1. Location in Photosynthetic Membranes and Light-Harvesting Function, Biochim. Biophys. Acta, 1985, vol. 811, pp. 325–355.

    CAS  Google Scholar 

  20. Stransky, H. and Hager, A., Carotenoid Pattern and Occurrence of Light Induced Xanthophyll Cycle in Various Classes of Algae, Arch. Mikrobiol., 1970, vol. 73, pp. 315–323.

    Article  PubMed  CAS  Google Scholar 

  21. García-Plazaola, J.I., Matsubara, S., and Osmond, C.B., The Lutein-Epoxide Cycle in Higher Plants: Its Relationships to Other Xanthophyll Cycles and Possible Functions, Funct. Plant Biol., 2007, vol. 34, pp. 759–773.

    Article  Google Scholar 

  22. Demmig, B. and Bjorkman, O., Comparison of the Effect of Excessive Light on Chlorophyll Fluorescence (77K) and Photon Yield of O2 Evolution in Leaves of Higher Plants, Planta, 1987, vol. 171, pp. 171–184.

    Article  CAS  Google Scholar 

  23. Sapozhnikov, D.I. and Sakharova, O.V., Role of Manganese in Light Reaction of Xanthophyll Conversion, Dokl. Akad. Nauk SSSR, 1964, vol. 157, no. 6, pp. 1480–1482.

    CAS  Google Scholar 

  24. Radunz, A. and Schmid, G., On the Localization of the Xanthophylls in the Thylakoid Membrane, Ber. Dtsch. Bot. Ges., 1979, vol. 92, pp. 437–443.

    Google Scholar 

  25. Sapozhnikov, D.I., Ivantsova, L.V., and Maslova, T.G., Existence of Two Types of Photochemical Reaction of Violaxanthin De-Epoxidation in Green Plant Leaves, Dokl. Akad. Nauk SSSR, 1969, vol. 189, no. 5, pp. 1135–1138.

    CAS  Google Scholar 

  26. Sapozhnikov, D.I., Kutyurin, V.M., Maslova, T.G., Ulubekova, M.V., Nazarov, N.M., Artamkina, I.Yu., and Semenyuk, K.G., Xanthophyll Oxygen Exchange as Related to Their Role in Plant Photosynthesis, Dokl. Akad. Nauk SSSR, 1967, no. 5, pp. 1182–1185.

  27. Hager, A., Reversible, Light-Induced Conversion of Xanthophylls in Chloroplasts, Ber. Dtsch. Bot. Ges., 1975, vol. 88, pp. 27–44.

    CAS  Google Scholar 

  28. Krinsky, N.I., Carotenoid Protection against Oxidation, Pure Appl. Chem., 1979, vol. 51, pp. 649–660.

    Article  CAS  Google Scholar 

  29. Demmig-Adams, B. and Adams, W.W., Photoprotection and Other Responses of Plants to High Light Stress, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1992, vol. 43, pp. 599–626.

    Article  CAS  Google Scholar 

  30. Gilmore, A.M., Mechanistic Aspects of Xanthophyll Cycle-Dependent Photoprotection in Higher Plant Chloroplasts and Leaves, Physiol. Plant., 1997, vol. 99, pp. 197–209.

    Article  CAS  Google Scholar 

  31. Ladygin, V.G. and Shirshikova, G.N., Current Ideas about the Functional Role of Carotenoids in Chloroplasts of Eukaryotes, Zh. Obshch. Biol., 2006, vol. 67, pp. 163–189.

    PubMed  CAS  Google Scholar 

  32. Wolf, Ch. and Witt, H.T., On Metastable States of Carotenoids in Primary Events of Photosynthesis, Z. Naturforsch., 1969, vol. 24, pp. 1031–1037.

    Google Scholar 

  33. Mathis, P. and Kleo, J., The Triplet State of β-Carotene and of Analog Polyenes of Different Length, Photochem. Photobiol., 1973, vol. 18, pp. 343–346.

    Article  CAS  Google Scholar 

  34. Havaux, M. and Niyogi, K.K., The Violaxanthin Cycle Protects Plants from Photooxidative Damage by More than One Mechanism, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 8762–8767.

    Article  PubMed  CAS  Google Scholar 

  35. Havaux, M., Dall’Osto, L., and Bassi, R., Zeaxanthin Has Enhanced Antioxidant Capacity with Respect to All Other Xanthophylls in Arabidopsis Leaves and Functions in Dependent of Binding to PSII Antennae, Plant Physiol., 2007, vol. 145, pp. 1506–1520.

    Article  PubMed  CAS  Google Scholar 

  36. Johnson, M.P., Havaux, M., Triantaphyllides, C., Ksas, B., Pascal, A.A., Robert, B., Davison, P.A., Ruban, A.V., and Horton, P., Elevated Zeaxanthin Bound to Oligomeric LHCII Enhances the Resistance of Arabidopsis to Photooxidative Stress by a Lipidprotective, Antioxidant Mechanism, J. Biol. Chem., 2007, vol. 282, pp. 22 605–22 618.

    CAS  Google Scholar 

  37. Horton, P., Ruban, A.V., and Wentworth, M., Allosteric Regulation of the Light-Harvesting System of Photosystem II, Trans. R. Soc. London, 2000, vol. 355, pp. 1361–1370.

    Article  CAS  Google Scholar 

  38. Horton, P., Wentworth, M., and Ruban, A., Control of the Light Harvesting Function of Chloroplast Membranes: The LHC II-Aggregation Model for Non-Photochemical Quenching, FEBS Lett., 2005, vol. 579, pp. 4201–4206.

    Article  PubMed  CAS  Google Scholar 

  39. Niogi, K.K., Grossman, A.R., and Bjorkman, O., Arabidopsis Mutants Define a Central Role for the Xanthophyll Cycle in the Regulation of Photosynthetic Energy Conversion, Plant Cell, 1998, vol. 10, pp. 1121–1134.

    Article  Google Scholar 

  40. Gruszecki, W.I. and Strzałka, K., Carotenoids as Modulators of Lipid Membrane Physical Properties, Biochim. Biophys. Acta, 2005, vol. 1740, pp. 108–115.

    PubMed  CAS  Google Scholar 

  41. Kostecka-Gugała, A., Latowski, D., and Strzałka, K., Termotropic Phase Behaviour of α-Dipalmitoylphosphatitylcholine Multibilayers Is Influenced to Various Extents by Carotenoids Containing Different Structural Features — Evidence from Differential Scanning Calorimetry, Biochim. Biophys. Acta, 2003, vol. 1609, pp. 193–202.

    Article  PubMed  Google Scholar 

  42. Lyubimenko, V.N., Relations between Chlorophyll and Proteins, Dnevnik I Vseros. S’ezda Russkikh Botanikov V Petrograde, 1921.

  43. Lyubimenko, V.N., Investigation of Plastid Pigments. The relation of Chlorophyll and Plastid Proteins, Izv. Akad. Nauk SSSR, Ser. 6, Biologiya, 1923, vol. 17, pp. 129–148.

    Google Scholar 

  44. Sapozhnikov, D.I., Maslova, T.G., and Bazhanova, N.V., The State of Pigments in Leaves, Tr. Bot. Inst. Akad. Nauk SSSR, Ser. 4, Experimental Botany, 1962, no. 15, pp. 53–64.

  45. Liu, Z., Yan, H., Wang, K., Kuang, T., Zhang, J., Gui, L., An, X., and Chang, W., Crystal Structure of Spinach Major Light-Harvesting Complex at 2.72Å Resolution, Nature, 2004, vol. 428, pp. 287–292.

    Article  PubMed  CAS  Google Scholar 

  46. Standfuss, R., van Scheltinga, A.C.T., Lamborghini, M., and Kuhlbrandt, W., Mechanisms of Photoprotection and Nonphotochemical Quenching in Pea Light-Harvesting Complex at 2.5Å Resolution, EMBO J., 2005, vol. 24, pp. 919–928.

    Article  PubMed  CAS  Google Scholar 

  47. Jahns, P., Latowski, D., and Strzałka, K., Mechanism and Regulation of the Violaxanthin Cycle: The Role of Antenna Proteins and Membrane Lipids, Biochim. Biophys. Acta, 2009, vol. 1787, pp. 3–14.

    Article  PubMed  CAS  Google Scholar 

  48. Szilagyi, A., Sommarin, M., and Åkerlund, H.E., Membrane Curvature Stress Controls the Maximal Conversion of Violaxanthin to Zeaxanthin in the Violaxanthin Cycle — Influence of Tocopherol, Cetylethers, Linolenic Acid, and Temperature, Biochim. Biophys. Acta, 2007, vol. 1768, pp. 2310–2318.

    Article  PubMed  CAS  Google Scholar 

  49. Andersson, U., Heddad, M., and Adamska, I., Light Stress-Induced One-Helix Protein of the Chlorophyll a/b-Binding Family Associated with Photosystem I, Plant Physiol., 2003, vol. 132, pp. 811–820.

    Article  PubMed  CAS  Google Scholar 

  50. Simidjiev, I., Stoylova, S., Amenitsch, H., Javorfi, T., Mustardy, L., Laggner, P., Holzenburg, A., and Garab, G., Self-Assembly of Large Ordered Lamellae from Non-Bilayer Lipids and Integral Membrane Proteins In Vitro, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 1473–1476.

    Article  PubMed  CAS  Google Scholar 

  51. Grudzinski, W., Matula, M., Sielewiesiuk, J., Kernen, P., Krupa, Z., and Gruszecki, W.I., Effect of 13-cis Violaxanthin on Organization of Light Harvesting Complex II in Monomolecular Layers, Biochim. Biophys. Acta, 2001, vol. 1503, pp. 291–302.

    Article  PubMed  CAS  Google Scholar 

  52. Deroche, M.E. and Costes, C., Heterogenity of Carotenoids in Chloroplasts, Prog. Photosynth. Res., 1969, vol. 11, pp. 681–693.

    Google Scholar 

  53. Sapozhnikov, D.I. and Kornyushenko, G.A., Heterogeneity of Violaxanthins in Pea Plants, Sov. Plant Physiol., 1969, vol. 16, pp. 1038–1041.

    CAS  Google Scholar 

  54. Maslova, T.G., Popova, I.A., Kornyushenko, G.A., and Koroleva, O.Ya., Violaxanthin Cycle in Photosynthesis: History and Current Concept, Russ. J. Plant Physiol., 1996, vol. 43, pp. 383–393.

    CAS  Google Scholar 

  55. Gilmore, A.M., Mohanty, N., and Yamamoto, H.Y., Epoxidation of Zeaxanthin and Antheraxanthin Reverses Non-Photochemical Quenching of Photosystem II Chlorophyll a Fluorescence in the Presence of Trans-Thylakoid pH, FEBS Lett., 1994, vol. 350, pp. 271–274.

    Article  PubMed  CAS  Google Scholar 

  56. Ruban, A.V., Pascal, A., Lee, P.J., Robert, B., and Horton, P., Molecular Configuration of Xanthophyll Cycle Carotenoids in Photosystem II Antenna Complexes, Biol. Chem., 2002, vol. 77, pp. 42 937–42 942.

    Google Scholar 

  57. Latowski, D., Åkerlund, H.E., and Strzałka, K., Violaxanthin De-Epoxidase, the Xanthophyll Cycle Enzyme, Requires Lipid Hexagonal Structures for Its Activity, Biochemistry, 2004, vol. 43, pp. 4417–4420.

    Article  PubMed  CAS  Google Scholar 

  58. Maslova, T.G., Mamushina, N.S., Sherstneva, O.A., Bubolo, L.S., and Zubkova, E.K., Seasonal Structural and Functional Changes in the Photosynthetic Apparatus of Evergreen Conifers, Russ. J. Plant Physiol., 2009, vol. 56, pp. 607–615.

    Article  CAS  Google Scholar 

  59. Sapozhnikov, D.I. and Bazhanova, N.V., Characteristics of Light Reactions in Isolated Chloroplasts, Dokl. Akad. Nauk SSSR, 1958, vol. 120, no. 5, pp. 1141–1143.

    CAS  Google Scholar 

  60. Hieber, A.D., Bugos, R.C., and Yamamoto, H.Y., Plant Lipocalins: Violaxanthin De-Epoxidase and Zeaxanthin-Epoxidase, Biochim. Biophys. Acta, 2000, vol. 1482, pp. 84–91.

    Article  PubMed  CAS  Google Scholar 

  61. Jahns, P. and Heyde, S., Dicyclohexylcarbodiimide Alters the pH Dependence of Violaxanthin De-Epoxidation, Planta, 1999, vol. 207, pp. 393–400.

    Article  CAS  Google Scholar 

  62. Bratt, C.E., Arvidsson, P.O., Carlsson, M., and Åkerlund, H.E., Regulation of Violaxanthin Deepoxidase Activity by pH and Ascorbate Concentration, Photosynth. Res., 1995, vol. 45, pp. 169–175.

    Article  CAS  Google Scholar 

  63. Yamamoto, H.Y., Biochemistry of the Violaxanthin Cycle in Higher Plants, Pure Appl. Chem., 1979, vol. 51, pp. 639–648.

    Article  CAS  Google Scholar 

  64. Härtel, H., Lokstein, H., Grimm, B., and Rank, B., Kinetic Studies on the Xanthophyll Cycle in Barley Leaves (Influence of Antenna Size and Relations to Nonphotochemical Chlorophyll Fluorescence Quenching), Plant Physiol., 1996, vol. 110, pp. 471–482.

    PubMed  Google Scholar 

  65. Reinhold, C., Niczyporuk, S., Beran, K.C., and Jahns, P., Short-Term Down-Regulation of Zeaxanthin Epoxidation in Arabodopsis thaliana in Response to Photo-Oxidative Stress Conditions, Biochim. Biophys. Acta, 2008, vol. 1777, pp. 462–469.

    Article  PubMed  CAS  Google Scholar 

  66. Yatsko, Ya.N., Dymova, O.V., and Golovko, T.K., Violaxanthin Cycle Pigment De-Epoxidation and Thermal Dissipation of Light Energy in Three Boreal Species of Evergreen Conifer Plants, Russ. J. Plant Physiol., 2011, vol. 58, pp. 169–173.

    Article  CAS  Google Scholar 

  67. Maslova, T.G., Mamushina, N.S., Zubkova, E.K., and Voitsekhovskaya, O.V., Specific Features of Plastid Pigment Apparatus and Photosynthesis in the Leaves of Ephemeroid and Summer Plants as Related to Photoinhibition, Russ. J. Plant Physiol., 2003, vol. 50, pp. 52–56.

    Article  CAS  Google Scholar 

  68. Streb, P., Shang, W., Feierabent, J., and Bligny, R., Divergent Strategies of Photoprotection in High Mountain Plants, Planta, 1998, vol. 207, pp. 313–324.

    Article  CAS  Google Scholar 

  69. Lu, C., Jiang, G., Wang, B., and Kuang, T., Photosystem II Photochemistry and Photosynthetic Pigment Composition in Salt-Adapted Halophyte Artemisia anethifolia Grown under Outdoor Conditions, J. Plant Physiol., 2003, vol. 160, pp. 403–408.

    Article  PubMed  CAS  Google Scholar 

  70. Larcher, W., Wagner, J., and Thammathaworn, A., Effects of Superimposed Temperature Stress on In Vivo Chlorophyll Fluorescence of Vigna unguiculata under Saline Stress, J. Plant Physiol., 1990, vol. 136, pp. 92–102.

    Article  CAS  Google Scholar 

  71. Ralph, P.J., Polk, S.M., Moore, K.A., Orth, R.J., and Smith, W.O., Jr., Operation of the Xanthophyll Cycle in the Seagrass Zostera marina in Response to Variable Irradiance, J. Exp. Mar. Biol. Ecol., 2002, vol. 71, pp. 189–207.

    Article  Google Scholar 

  72. Popova, O.F., Development of Dark Reaction of Xanthophyll Conversion during Greening of Etiolated Maize Seedlings, Bot. Zh. (Leningrad), 1968, vol. 53, pp. 978–982.

    Google Scholar 

  73. Popova, O.V. and Eidelman, Z.M., Xanthophyll Conversion during Plastid Greening, Dokl. Akad. Nauk SSSR, 1976, vol. 175, no. 6, pp. 1407–1409.

    Google Scholar 

  74. Nelson, N. and Yocum, Ch., Structure and Function of Photosystems I and II, Annu. Rev. Plant Biol., 2006, vol. 57, pp. 521–565.

    Article  PubMed  CAS  Google Scholar 

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Correspondence to T. G. Maslova.

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Original Russian Text © T.G. Maslova, E.F. Markovskaya, 2012, published in Fiziologiya Rastenii, 2012, Vol. 59, No. 3, pp. 472–480.

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Maslova, T.G., Markovskaya, E.F. Current views on the function of the violaxanthin cycle (development of ideas put forward by D.I. Sapozhnikov). Russ J Plant Physiol 59, 434–441 (2012). https://doi.org/10.1134/S1021443712030120

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