, Volume 48, Issue 3, pp 400–408 | Cite as

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

  • Y. L. Sun
  • F. Li
  • N. Su
  • X. L. Sun
  • S. J. Zhao
  • Q. W. Meng
Original Papers


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.

Additional key words

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



ascorbate peroxidase


ascorbic acid




the maximal photochemical efficiency of PSII


Lycopersicon esculentum glycerol-3-phosphate acyltransferase gene




net photosynthetic rate




photosynthetic photon flux density


photosystem I (II)


polyvinylidene fluoride


reactive oxygen species


sodium dodecyl sulfate polyacrylamide gel electrophoresis




superoxide dismutase




palmitic acid


3-trans-hexadecenoic acid


stearic acid


oleic acid


linoleic acid


linolenic acids


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We thank professor Lixin Zhang, Institute of Botany, Chinese Academy of Sciences, for the D1-specific antibodies. This research was supported by the State Key Basic Research and Development Plan of China (2009CB118500), the Natural Science Foundation of China (30871458), Program for Changjiang Scholars and Innovative Research Team in University (Grant IRT0635) and the Natural Science Foundation of Shandong province (Y2007D50).


  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.CrossRefPubMedGoogle Scholar
  2. Allakhverdiev, S.I., Murata, N.: Salt stress inhibits photosystems II and I in cyanobacteria. — Photosynth. Res. 98: 529–539, 2008.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.Google Scholar
  6. Arnon, D.I.: Copper enzymes in isolated chloroplasts — polyphenoloxidase in Beta vulgaris. — Plant Physiol. 24: 1–15, 1949.CrossRefPubMedGoogle Scholar
  7. Aro, E.M., Virgin, I., Andersson, B.: Photoinhibition of photosystem II: Inactivation, protein damage and turnover. — Biochim. Biophys. Acta 1143: 113–134, 1993.CrossRefPubMedGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  10. Giannopolitis, C.N., Ries, S.K.: Superoxide dismutases. I. Occurrence in higher plants. — Plant Physiol. 59: 309–314, 1977.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.Google Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  16. Mahajan, S., Tuteja, N.: Cold, salinity and drought stresses: An overview. — Arch. Biochem. Biophys. 444: 139–158, 2005.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  19. Murashige, T., Skoog, F.: A revised medium for rapid growth and bioassays with tobacco tissue cultures. — Plant Physiol. 15: 473–497, 1962.CrossRefGoogle Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  25. Roughan, P.G., Slack, C.R.: Cellular organization of glycerolipid metabolism. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 33: 97–132, 1982.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.Google Scholar
  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.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefPubMedGoogle Scholar
  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.CrossRefGoogle Scholar
  34. Van Kooten, O., Snel, J.P.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. — Photosynth. Res. 25: 147–150, 1990.CrossRefGoogle Scholar
  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.Google Scholar
  36. Wada, H., Murata, N.: The essential role of phosphatidylglycerol in photosynthesis. — Photosynth. Res. 92: 205–215, 2007.CrossRefPubMedGoogle Scholar
  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.Google Scholar
  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.Google Scholar
  39. Yeo, A.: Molecular biology of salt tolerance in the context of whole plant physiology. — J. Exp. Bot. 49: 915–929, 1998.CrossRefGoogle Scholar
  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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Y. L. Sun
    • 1
  • F. Li
    • 1
  • N. Su
    • 2
  • X. L. Sun
    • 1
  • S. J. Zhao
    • 1
  • Q. W. Meng
    • 1
  1. 1.College of Life Science, State Key Laboratory of Crop BiologyShandong Agricultural UniversityTai’anP.R. China
  2. 2.College of Life ScienceShandong Normal UniversityJi’nanP.R. China

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