Photosynthetica 2010, 48(3):400-408 | DOI: 10.1007/s11099-010-0052-1

The increase in unsaturation of fatty acids of phosphatidylglycerol in thylakoid membrane enhanced salt tolerance in tomato

Y. L. Sun1, F. Li1, N. Su2, X. L. Sun1, S. J. Zhao1, Q. W. Meng1,*
1 College of Life Science, State Key Laboratory of Crop Biology, Shandong Agricultural University, Tai'an, P.R. China
2 College of Life Science, Shandong Normal University, Ji'nan, P.R. China

Overexpression of chloroplastic glycerol-3-phosphate acyltransferase gene (LeGPAT) in tomato increased cis-unsaturated fatty acid content in phosphatidylglycerol (PG) of thylakoid membrane. By contrast, suppressing the expression of LeGPAT decreased the content of cis-unsaturated fatty acid in PG. Under salt stress, sense transgenic plants exhibited higher activities of chloroplastic antioxidant enzymes, lower content of reactive oxygen species (ROS) and less ion leakage compared with the wild type (WT) plants. The net photosynthetic rate (P N) and the maximal photochemical efficiency (Fv/Fm) of photosystem II (PSII) decreased more slightly in sense lines but more markedly in the antisense ones, compared to WT. D1 protein, located in the reactive center of the PSII, is the primary target of photodamage and has the highest turnover rate in the chloroplast. Under salt stress, compared with WT, the content of D1 protein decreased slightly in sense lines and significantly in the antisense ones. In the presence of streptomycin (SM), the net degradation of the damaged D1 protein was faster in sense lines than in other plants. These results suggested that, under salt-stress conditions, increasing cis-unsaturated fatty acids in PG by overexpression of LeGPAT can alleviate PSII photoinhibition by accelerating the repair of D1 protein and improving the activity of antioxidant enzymes in chloroplasts.

Keywords: ascorbate peroxidase; D1 protein; glycerol-3-phosphate acyltransferase; phosphatidylglycerol; salt stress

Received: September 21, 2009; Accepted: May 13, 2010; Published: September 1, 2010Show citation

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Sun, Y.L., Li, F., Su, N., Sun, X.L., Zhao, S.J., & Meng, Q.W. (2010). The increase in unsaturation of fatty acids of phosphatidylglycerol in thylakoid membrane enhanced salt tolerance in tomato. Photosynthetica48(3), 400-408. doi: 10.1007/s11099-010-0052-1.
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References

  1. Allakhverdiev, S.I., Kinoshita, M., Inaba, M., Suzuki, I., Murata, N.: Unsaturated fatty acids in membrane lipids protect the photosynthetic machinery against salt-induced damage in Synechococcus. - Plant Physiol. 125: 1842-1853, 2001.
  2. Allakhverdiev, S.I., Murata, N.: Salt stress inhibits photosystems II and I in cyanobacteria. - Photosynth. Res. 98: 529-539, 2008. Go to original source...
  3. Allakhverdiev, S.I., Nishiyama, Y., Miyairi, S., Yamamoto, H., Inagaki, N., Kanesaki, Y., Murata, N.: Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. - Plant Physiol. 130: 1443-1453, 2002. Go to original source...
  4. Allakhverdiev, S.I., Nishiyama, Y., Suzuki, I., Tasaka, Y., Murata, N.: Genetic engineering of the unsaturation of fatty acids in membrane lipids alters the tolerance of Synechocystis to salt stress. - Proc. Natl. Acad. Sci. USA. 96: 5862-5867, 1999. Go to original source...
  5. Andersson, B., Aro, E.M.: Photodamage and D1 protein turnover in photosystem II. - In: Aro, E.M., Andersson, B. (ed.): Regulation of Photosynthesis. Kluwer Academic Publishers, Pp. 377-393, Dordrecht 2001. Go to original source...
  6. Arnon, D.I.: Copper enzymes in isolated chloroplasts - polyphenoloxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
  7. Aro, E.M., Virgin, I., Andersson, B.: Photoinhibition of photosystem II: Inactivation, protein damage and turnover. - Biochim. Biophys. Acta 1143: 113-134, 1993. Go to original source...
  8. Chen, Z.Q., Xu, C.H., Chen, M.J., Xu, L., Wang, K.F., Lin, S.Q., Kuang, T.Y.: Effect of chilling acclimation on thylakoid membrane protein of wheat. - Acta Bot. Sin. 36: 423-429, 1994.
  9. Foyer, C.H., Halliwell, B.: The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. - Planta 133: 21-25, 1976. Go to original source...
  10. Giannopolitis, C.N., Ries, S.K.: Superoxide dismutases. I. Occurrence in higher plants. - Plant Physiol. 59: 309-314, 1977. Go to original source...
  11. 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...
  12. Huflejt, M.E., Tremolieres, A., Pineau, B., Lang, J.K., Hatheway, J., Packer, L.: Changes in membrane lipid composition during saline growth of the fresh water cyanobacterium Synechococcus 6311. - Plant Physiol. 94: 1512-1521, 1990. Go to original source...
  13. Jimenez, A., Hernandez, J.A., del Rio, L.A., Sevilla, F.: Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves. - Plant Physiol. 114: 272-284, 1997. Go to original source...
  14. Jordan, P., Fromme, P., Witt, H.T, Klukas, O., Saenger, W., Krauss, N.: Three-dimensional structure of cyanobacterial photosystem I at 2.5 A resolution. - Nature 411: 909-917, 2001. Go to original source...
  15. Loll, B., Kern, J., Seanger, W., Zouni, A., Biesiadka, J.: Lipids in photosystem II: Interactions with protein and cofactors. - Biochim. Biophys. Acta. 1767: 509-519, 2007. Go to original source...
  16. Mahajan, S., Tuteja, N.: Cold, salinity and drought stresses: An overview. - Arch. Biochem. Biophys. 444: 139-158, 2005. Go to original source...
  17. Mattoo, A., Giardi, M.T., Raskind, A., Edelman, M.: Dynamic metabolism of photosystem II reaction center proteins and pigments. - Plant Physiol. 107: 454-461, 1999. Go to original source...
  18. Moon, B.Y., Higashi, S., Gombos, Z., Murata, N.: Unsaturation of the membrane lipids of chloroplasts stabilizes the photosynthetic machinery against low-temperature photoinhibition in transgenic tobacco plants. - Proc. Natl. Acad. Sci. USA 92: 6219-6223, 1995. Go to original source...
  19. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures. - Plant Physiol. 15: 473-497, 1962. Go to original source...
  20. Murata, N., Ishizaki-Nishizawa, O., Higashi, S., Hayashi, H., Tasaka, Y., Nishida, I.: Genetically engineered alteration in the chilling sensitivity of plants. - Nature 356: 710-713, 1992. Go to original source...
  21. Nishida, I., Murata, N.: Chilling sensitivity in plants and cyanobacteria: The crucial contribution of membrane lipids. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 47: 541-568, 1996. Go to original source...
  22. Noctor, G., Foyer, C.H.: Ascorbate and glutathione: Keeping active oxygen under control. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249-279, 1998. Go to original source...
  23. Ohnishi, N., Murata, N.: Glycinebetaine counteracts the inhibitory effects of salt stress on the degradation and synthesis of the D1 protein during photoinhibition in Synechococcus sp. PCC 7942. - Plant Physiol. 141: 758-765, 2006. Go to original source...
  24. Robinson, S.P., Downton, W.J.S., Millhouse, J.A.: Photosynthesis and ion content of leaves and isolated chloroplasts of salt-stressed spinach. - Plant Physiol. 73: 238-242, 1983. Go to original source...
  25. Roughan, P.G., Slack, C.R.: Cellular organization of glycerolipid metabolism. - Annu. Rev. Plant Physiol. Plant Mol. Biol. 33: 97-132, 1982. Go to original source...
  26. Sairam, R.K., Srivastava, G.C.: Changes in antioxidant activity in sub-cellular fractions of tolerant and susceptible wheat genotypes in response to long term salt stress. - Plant Sci. 162: 897-904, 2002. Go to original source...
  27. Sakurai, I., Hagio, M., Gombos, Z., Tyystjarvi, T., Paakkarinen, V., Aro, E.M., Wada, H.: Requirement of phosphatidylglycerol for maintenance of photosynthetic machinery. - Plant Physiol. 133: 1376-1384, 2003. Go to original source...
  28. Sakurai, I., Mizusawa, N., Ohashi, S., Kobayashi, M., Wada, H.: Effects of the lack of phosphatidylglycerol on the donor side of photosystem II. - Plant Physiol. 144: 1336-1346, 2007. Go to original source...
  29. Siegenthaler, P.-A., Eichenberger, W.: Structure, function and metabolism of plant lipids. - In: Siegenthaler, P.-A., Eichenberger, W. (ed.): Plant Lipids-Metabolism-Congresses. Pp. 485-488, Elsevier Science Publishers, Amsterdam 1984.
  30. Sui, N., Li, M., Liu, X.-Y., Wang, N., Fang, W., Meng, Q.-W.: Response of xanthophyll cycle and chloroplastic antioxidant enzymes to chilling stress in tomato over-expressing glycerol-3-phosphate acyltransferase gene. - Photosynthetica 45: 447-454, 2007a. Go to original source...
  31. Sui, N., Li, M., Zhao, S.J., Li, F., Liang, H., Meng, Q.W.: Overexpression of glycerol-3-phosphate acyltransferase gene improves chilling tolerance in tomato. - Planta 226: 1097-1108, 2007b. Go to original source...
  32. Takahashi, S., Murata, N.: Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. - Biochim. Biophys. Acta 1757: 198-205, 2006. Go to original source...
  33. Tanaka, Y., Hibino, T., Hayashi, Y. Tanaka, A., Kishitani, S., Takabe, T., Yokota, S., Takabe, T.: Salt tolerance of transgenic rice overexpressing yeast mitochondrial Mn-SOD in chloroplasts. - Plant Sci. 148: 131-138, 1999. Go to original source...
  34. Van Kooten, O., Snel, J.P.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. - Photosynth. Res. 25: 147-150, 1990. Go to original source...
  35. Wada, H., Murata, N.: Membrane lipids in cyanobacteria. - In: Siegenthaler, P.-A., Murata, N. (ed.): Lipids in Photosynthesis: Structure, Function and Genetics. Pp. 65-81. Kluwer Academic Publishers, Dordrecht - Boston - London 1998. Go to original source...
  36. Wada, H., Murata, N.: The essential role of phosphatidylglycerol in photosynthesis. - Photosynth. Res. 92: 205-215, 2007. Go to original source...
  37. Wang, A.G., Luo, G.H.: Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants. - Plant Physiol. 6: 55-57, 1990.
  38. Xu, Y.N., Siegenthaler, P.A.: Low temperature treatments induce an increase in the relative content of both linolenic and Δ3-trans-hexadecenoic acids in thylakoid membrane phosphatidylglycerol of squash cotyledons. - Plant Cell Physiol. 38: 611-618, 1997. Go to original source...
  39. Yeo, A.: Molecular biology of salt tolerance in the context of whole plant physiology. - J. Exp. Bot. 49: 915-929, 1998. Go to original source...
  40. Zhang, L.X., Paakkarinen, V., van Wijk, K.J., Aro, E.M.: Cotranslational assembly of the D1 protein into photosystem II. - J. Biol. Chem. 274: 16062-16067, 1999. Go to original source...