Photosynthetica 2010, 48(1):30-41 | DOI: 10.1007/s11099-010-0006-7

Overaccumulation of glycine betaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat

G. P. Wang1, F. Li1, J. Zhang1, M. R. Zhao1, Z. Hui1, W. Wang1,*
1 College of Life Science/State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai'an, Shandong, China

To investigate the role of glycine betaine in photosynthesis under stress, a transgenic wheat (Triticum aestivum L.) line T6 overaccumulating glycine betaine and its wild type Shi4185 were used. Seedlings were exposed to conditions of drought (30%, PEG-6000), heat (40°C) and their combination. The results revealed ultrastructural damage to the chloroplast and thylakoid lamellae with the withered phenotype by both drought and heat stress, and the damage was exacerbated by the combination of drought and heat. The appearance of a K step in the typical O-J-I-P curve and the decrease of Hill activity indicated a reduction of oxygen evolving complex function caused by stress. The greater damage was found in wild type than T6. Overaccumulation of glycine betaine in T6 could protect lipids in the thylakoid membrane from damage and stabilize the index of unsaturated fatty acids under stress. A lower ratio of monogalactosyl diacylglycerol/digalactosyl diacylglycerol and higher phosphatidylglycerol content in the thylakoid membrane of T6 were also observed under stress. These effects can promote stability of the thylakoid membrane. Otherwise, glycine betaine overaccumulation decreased photoinhibition of PSII under stress. The results also suggest that xanthophyll cycle-dependent non-radiative energy dissipation may be involved in the GB-mediated effects on PSII function under stress conditions.

Additional key words: chloroplast ultrastructure; fatty acids; Hill activity; lipids; nonradiative energy dissipation; oxygen-evolving complex; thylakoid membrane

Received: March 16, 2009; Accepted: January 15, 2010; Published: March 1, 2010  Show citation

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Wang, G.P., Li, F., Zhang, J., Zhao, M.R., Hui, Z., & Wang, W. (2010). Overaccumulation of glycine betaine enhances tolerance of the photosynthetic apparatus to drought and heat stress in wheat. Photosynthetica, 48(1), 30-41. doi: 10.1007/s11099-010-0006-7
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    References

    1. Arnon, D. I.: Copper enzymes in isolated chloroplasts: polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: l-15, 1949. Go to original source...
    2. Bruce, B.D.: The role of lipids in plastid protein transport. - Plant Mol. Biol. 38: 223-246, 1998. Go to original source...
    3. Demiral, T., Türkan, I.: Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment? - J. Plant Physiol. 161: 1089-1100, 2004. Go to original source...
    4. Demmig, B., Winter, K.: Characterization of 3 components of non-photochemical fluorescence quenching and their response to photoinhibition. - Aust. J. Plant Physiol. 15:163-177, 1988. Go to original source...
    5. Demmig-Adams, B.: Carotenoids and photoprotection in plants: A role for the xanthophyll zeaxanthin. - Biochim. Biophys. Acta 1020: 1-24, 1990. Go to original source...
    6. Deng, L.Y., Wang, H.C.: [Cold hardiness of crape in relation to membrane lipid composition.] - Acta Phytophysiol. Sin. 8: 273-283, 1982. [In Chin.]
    7. Ding, Z.S., Zhang, Y.M., Zhang, G.R., Wen, Z.Y., Guo, B.H.: [The effect of foreign betaine aldehyde dehydrogenase gene on the synthesis of betaine in wheat.] - Acta Agricult. Boreali-Sin. 18: 40-42, 2003. [In Chin.]
    8. Domonkos, I., Malec, P., Sallai, A., Kovács, L., Itoh, K., Shen, G., Ughy, B., Bogos, B., Sakurai, I., Kis, M., Strzalka, K., Wada, H., Itoh, S., Farkas, T., Gombos, Z.: Phosphatidylglycerol is essential for oligomerization of photosystem I reaction center. - Plant Physiol. 134: 1471-1478, 2004. Go to original source...
    9. Dorne, A.J., Joyard, J., Douce, R.: Do thylakoids realy contain phosphatidylcholine? - Proc. Nat. Acad. Sci. USA 87:71-74, 1990. Go to original source...
    10. Droppa, M., Masojidek, J., Rózsa, Z., Wolak, A., Horváth, L., Farkas, T., Horváth, G.: Characteristics of Cu deficiency-induced inhibition of photosynthetic electron transport in spinach chloroplasts. - Biochim. Biophys. Acta 891: 75-84, 1987. Go to original source...
    11. Garab, G., Lohner, K., Laggner, P., Farlas, T.: Self-regulation of the lipid content of membranes by non-bilarer lipids: a hypothesis. - Trends Plant Sci. 5: 489-494, 2000. Go to original source...
    12. Gilmore A.M.: Mechanistic aspects of xanthophylls cycledependent photoprotection in higher plant chloroplasts and leaves. - Physiol. Plant. 99: 197-209, 1997. Go to original source...
    13. Gisselsson, A., Szilágyi, A., Åkerlund, H.E.: Role of histidines in the binding of violaxanthin de-epoxidase to thylakoid membrane as studied by site-directed mutagenesis. - Physiol. Plant 122: 337-343, 2004. Go to original source...
    14. Gounaris, K., Mannock, D.A., Sen, A., Brain, A.P.R., Williams W.P., Quinn, P.J.: Poly-unsaturated fatty acyl residues of galactopipids are involved in the control of bilayer/nonbilayer lipid transition in higher-plant chloroplasts. - Biochim. Biophys. Acta 732: 229-242, 1983. Go to original source...
    15. Gounaris, K., Brain, A.R.P., Quinn, P.J., Williams, W.P.: Structural reorganisation of chloroplast thylakoid membranes in response to heat-stress. - Biochim. Biophys. Acta 766:198-208, 1984. Go to original source...
    16. Guissé, B., Srivastava, A., Strasser, R.J.: The polyphasic rise of the chlorophyll a fluorescence (O-K-J-I-P) in heat stressed leaves. - Arch. Sci. Genève 48: 147-160, 1995.
    17. Guo, B.H., Zhang, Y.M., Li, H.J., Du, L.Q., Li, Y.X., Zhang, J.S., Chen, S.Y., Zhu, Z.Q.: Transformation of wheat with a gene encoding for the betaine aldehyde dehydrogenase (BADH). - Acta Bot. Sin. 42: 279-283, 2000. [In Chin.]
    18. Hagio, M., Sakurai, I., Sato, S., Kato, T., Tabata, S., Wada, H.: Phosphatidylglycerol is essential for the development of thylakoid membranes in Arabidopsis thaliana. - Plant Cell Physiol. 43: 1456-1464, 2002. Go to original source...
    19. Han, X., Li, R., Wang, J.: Cellular structural comparison between different thermo-resistant cultivars of Raphanus sativus L. under heat stress. - J. W. Bot. Res. 15: 173-178, 1997.
    20. Havaux, M., Bonfils, J.P., Lütz, C., Niyogi, K.K.: Photodamage of the photosynthetic apparatus and its dependence on the leaf developmental stage in the npq1 Arabidopsis mutant deficient in the xanthophyll cycle enzyme violaxanthin de-epoxidase. - Plant Physiol. 124: 273-284, 2000. Go to original source...
    21. Horton, P., Ruban, A.V., Walters, R.G.: Regulation of light harvesting in green plants. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 655-684, 1996. Go to original source...
    22. Huseynova, I.M., Suleymanov, S.Y., Aliyev, J.A.: Structuralfunctional state of thylakoid membranes of wheat genotypes under water stress. - Biochim. Biophys. Acta 1767: 869-875, 2007. Go to original source...
    23. Jiang, C.D., Gao, H.Y., Zou, Q.: Changes of donor and acceptor in photosystem 2 complex induced by iron deficiency in attached soybean and maize leaves. - Photosynthetica 41: 267-271, 2003. Go to original source...
    24. Johnson, G.N., Young, A.J., Scholes, J.D., Horton, P.: The dissipation of excess excitation-energy in British plantspecies. - Plant Cell Environ. 16: 673-679, 1993. Go to original source...
    25. Kanervo, E., Tasaka, Y., Murata, N., Aro, E.M.: Membrane lipid unsaturation modulates processnig of the photosystem II reaction center protein D1 at low temperatures. - Plant Physiol. 114: 841-849, 1997. Go to original source...
    26. Karim, M.A., Fracheboud, Y., Stamp, P.: Photosynthetic activity of developing leaves of Zea mays is less affected by heat stress than that of developed leaves. - Physiol. Plant. 105: 685-693, 1999. Go to original source...
    27. Krause, G.H., Jahns, P.: Pulse amplitude modulated chlorophyll fluorometry and its application in plant science. - In: Green, B.R., Parson, W.W. (ed.): Light-harvesting antennas in photosynthesis. Pp. 373-399. Kluwer Academic Publ., Dordrecht - Boston - London 2003. Go to original source...
    28. Krieger, A., Moya, I., Weis, E.: Energy-dependent quenching chlorophyll a fluorescence: effect of pH on stationary fluorescence and picosecond-relaxation kinetics in thylakoid membranes and Photosystem II preparations. - Biochim. Biophys. Acta 1102: 167-176, 1992. Go to original source...
    29. Larkindale, J., Huang, B.: Thermotolerance and antioxidant systems in Agrostis stolonifera: Involvement of salicylic acid, abscisic acid, calcium, hydrogen peroxide, and ethylene. - J. Plant Physiol. 161: 405-413, 2004. Go to original source...
    30. Ma, X.L., Wang, Y.J., Xie, S.L., Wang, C., Wang W.: Glycinebetaine application ameliorates negative effects of drought stress in tobacco. - Russ. J. Plant Physiol. 54: 472-479, 2007. Go to original source...
    31. Mittler, R.: Abiotic stress, the field environment and stress combination. - Trends Plant Sci. 11: 15-19, 2006. Go to original source...
    32. Noctor, G., Rees, D., Young, A.J. and Horton, P.: The relationship between zeaxanthin, energy-dependent quenching of chlorophyll fluorescence and trans-thylakoid pH gradient in isolated chloroplasts. - Biochim. Biophys. Acta 1057: 320-330, 1991. Go to original source...
    33. Pick, U., Gounaris, K., Weiss, M., Barber, J.: Tightly bound sulpholipids in chloroplast CF0-CF1. - Biochim. Biophys. Acta 808: 415-420, 1985. Go to original source...
    34. Ristic, Z., Cass, D.D.: Chloroplast structure after water and high-temperature stress in two lines of maize that differ in endogenous levels of abscisic acid. - Int. J. Plant Sci. 153: 186-196, 1992. Go to original source...
    35. Rizhsky, L., Liang, H.J., Mittler, R.: The combined effect of drought stress and heat shock on gene expression in tobacco. - Plant Physiol. 130: 1143-1151, 2002. Go to original source...
    36. Sakamoto, A., Murata N.: The role of glycine betaine in the protection of plants from stress: clues from transgenic plants. - Plant Cell Environ. 25: 163-171, 2002. Go to original source...
    37. Schansker, G., Tóth, S.Z., Strasser, R.J.: Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. - Biochim. Biophys. Acta 1706: 250-261, 2005. Go to original source...
    38. Shah, N.H., Paulsen, G.M.: Interaction of drought and high temperature on photosynthesis and grain-filling of wheat. - Plant Soil 257: 219-226, 2003. Go to original source...
    39. Shulaev, V., Cortes, D., Miller, G., Mittler, R.: Metabolomics for plant stress response. - Physiol. Plant 132: 199-208, 2008. Go to original source...
    40. Siegenthaler, P.A., Rawyler A., Smutny, J..: The phospholipid population which sustains the uncoulpled non-cyclic electron flow activity is located in the inner monolayer of the thylakoid membrane. - Biochim. Biophys. Acta 975: 104-111, 1989. Go to original source...
    41. Sigrist, M., Zwilliengerg, C., Giroud, C.H., Eichenberger, W., Boschetti, A.: Sulfolipid associated with the light-harvesting complex associated with photosystem II apoproteins of Chlamydomonas reinhardtii. - Plant Sci. 58: 15-23, 1988. Go to original source...
    42. Strasser, R.J., Govindjee: On the O-J-I-P fluorescence transient in leaves and D1 mutants of Chlamydomonas reinhardtii. - In: Murata, N. (ed) Research in Photosynthesis. Vol. II. Pp. 29-32. Kluwer Academic Publ., Dordrecht - Boston - London 1992.
    43. Tang, Y.L., Wen, X.G., Lu, Q.T., Yang, Z.P., Cheng, Z.K., Lu, C.M.: Heat stress induces an aggregation of the light-harvesting complex of Photosystem II in spinach plants. - Plant Physiol. 143: 629-638, 2007. Go to original source...
    44. Thomas, P.G., Dominy P.J., Vigh L., Mansourian A.R., Quinn P.J., Williams W.P.: Increased thermal stability of pigment-protein complexes of pea thylakoids following catalytic hydrogenation of membrane lipids. - Biochem. Biophys. Acta 849: 131-140, 1986. Go to original source...
    45. Tremolieres, A., Garnier, J., Guyon, D., Maroc, J., Wu, B.: Role of phosphatidyglycerol in photosynthetic membranes: study with mutants of Chlamydomonas reinharatii. - In: Biacs, P.A., Gruiz, K., Kremmer, T. (ed.): Biological Role of Plant Lipids. Pp. 203-206. Akademial Klado, Budapest and Plenum Publ. Press, New York - London 1989. Go to original source...
    46. Vijayan, P., Browse, J.: Photoinhibition in mutants of Arabidopsis deficient in thylakoid unsaturation. - Plant Physiol. 129: 876-885, 2002. Go to original source...
    47. Wada, H., Murata, N.: Membrane lipids in cyanobacteria. - In: Siegenthaler, P. A., Murata, N. (ed.): Lipids in Photosynthesis: Structure, Function and Genetics. Advances in Photosynthesis. Vol. 6. Pp.65-81. Kluwer Academic Publ., Dordrecht - Boston - London 1998. Go to original source...
    48. Wang, C., Ma, X.L., Hui, Z., Wang, W.: Glycine betaine improves thylakoid membrane function of tobacco leaves under low-temperature stress. - Photosynthetica 46: 400-409, 2008. Go to original source...
    49. Webb, M.S., Green, B.R.: Biochemical and biophysical properties of thylakoid acyl lipids. - Biochim. Biophys. Acta 1060: 133-158, 1991. Go to original source...
    50. Wen, X.G., Qiu, N.W., Lu, Q.T., Lu, C.M.: Enhanced thermotolerance of photosystem II in salt-adapted plants of the halophyte Artemisia anethifolia. - Planta 220: 486-497, 2005. Go to original source...
    51. Williams, W.P., Brain, A.P.R., Dominy, P.J.: Induction of nonbilayer lipid phase separations in chloroplast thylakoid membranes by compatible co-solutes and its relation to the thermal stability of Photosystem II. - Biochim. Biophys. Acta 1099: 137-144, 1992. Go to original source...
    52. Williams, W.P.: The physical properties of thylakoid membrane lipids and their relation to photosynthesis. - In: Siegenthaler, P.A., Murata, N. (ed.): Lipids in Photosynthesis: Structure, Function and Genetics. Advances in Photosynthesis. Vol. 6. Pp. 103-118. Kluwer Academic Publ., Dordrecht - Boston - London 1998. Go to original source...
    53. Xu, C., Hartel, H., Wada, H., Hagio, M., Yu, B., Eakin, C., Benning, C.: The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. - Plant Physiol. 129: 594-604, 2002. Go to original source...
    54. Yang, X.H., Wen, X.G., Gong, H.M., Lu, Q.T., Yang, Z.P., Tang, Y.L., Liang, Z., Lu, C.M.: Genetic engineering of the biosynthesis of glycinebetaine enhances thermotolerance of photosystem II in tobacco plants. - Planta 225: 719-733, 2007. Go to original source...
    55. Zhao, X.-X., Ma, Q.-Q., Liang, C., Fang, Y., Wang, Y.-Q., Wang, W.: Effect of glycinebetaine on function of thylakoid membranes in wheat flag leaves under drought stress. - Biol. Plant. 51: 584-588, 2007. Go to original source...
    56. Ye, J.Y., Qian, Y.Q. (ed.): [Techniques of Plant Physiological Experiments.] - Shanghai Scientific & Technical Publ., Shanghai 1985. [In Chin.]
    57. Yu, B., Benning, C.: Anionic lipids are required for chloroplast structure and function in Arabidopsis. - Plant J. 36: 762-770, 2003. Go to original source...

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