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Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity

  • Original Papers
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Photosynthetica

Abstract

In order to examine the possible role of unsaturated fatty acids in photosynthesis of halophytes under high salinity, the effect of salinity on plant growth, chlorophyll (Chl) content, photochemical efficiency of PSII, membrane lipid content and fatty acids composition of a C3 euhalophyte Suaeda salsa L. was investigated. Salt stress induced a slight increase of the maximal photochemical efficiency of PSII (Fv/Fm), actual PSII efficiency (ΦPSII), Chl a content and Chl a/b ratio. The unsaturated fatty acid content also increased under salt stress. The proportion of MGDG, DGDG, SQDG, and PC decreased, while the proportion of PG increased from 10.9% to 26.9% under salt stress. These results suggest that S. salsa displays high resistance to photoinhibition under salt stress and that increased concentration of unsaturated fatty acids in membrane lipids of S. salsa enhances the tolerance of photosystem II to salt stress.

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Abbreviations

16:0:

palmitic acid; 16:1(3t)

Δ3:

trans-hexadecenoic

18:0:

stearic acid

18:1:

oleic acid

18:2:

linoleic acid

18:3:

linolenic acid

Chl:

chlorophyll

DGDG:

digalactosyldiacylglycerols

Fo :

initial fluorescence of the dark-adapted state

Fv :

variable fluorescence

Fm :

maximal fluorescence of the dark-adapted state

Fs :

the steady-state fluorescence

Fm′:

maximal fluorescence in the light-adapted state

Fv/Fm :

maximal photochemical efficiency of PSII

DBI:

double bond index

MGDG:

monogalactosyldiacylglycerols

PC:

phosphatidylcholines

PG:

phosphatidylglycerols

ΦPSII :

the quantum yield of PSII electron transport

SQDG:

sulphoquinovosyldiacylglycerols

References

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • 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. Nat. Acad. Sci. 96: 5862–5867, 1999.

    Article  CAS  PubMed  Google Scholar 

  • Anderson, J.M.: Photoregulation of the composition, function, and structure of thylakoid membranes. — Annu. Rev. Plant Physiol. 37: 93–136, 1986.

    Article  CAS  Google Scholar 

  • Aro, E.M., Virgin, I., Andersson, B.: Photoinhibition of Photosystem II. Inactivation, protein damage and turnover. — Biochim. Biophys. Acta 1143: 113–134, 1993.

    Article  CAS  PubMed  Google Scholar 

  • Baker, N.R.: A possible role for photosystem II in environmental perturbations of photosynthesis. — Physiol. Plant. 81: 563–570, 1991.

    Article  CAS  Google Scholar 

  • Ben Hamed, K., Ben Youssef, N., Ranieri, A., Zarrouk, M., Abdelly, C.: Changes in content and fatty acid profiles of total lipids and sulfolipids in the halophyte Crithmum maritimum under salt stress. — J. Plant Physiol. 162: 599–602, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Berberich, T., Harada, M., Sugawara, K., Kodama, H., Iba, K., Kusano, T.: Two maize genes encoding ω-3 fatty acid desaturase and their differential expression to temperature. — Plant Mol. Biol. 36: 297–306, 1998.

    Article  CAS  PubMed  Google Scholar 

  • Berry, J.A., Björkman, O.: Photosynthetic response and adaptation to temperature in higher plants. — Anna. Rev. Plant Physiol. 31: 491–543, 1980.

    Article  Google Scholar 

  • Carter, D.R., Cheeseman, J.M.: The effects of external NaCI on thylakoid stacking in lettuce plants. — Plant Cell Environ. 16: 215–222, 1993.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Cooke, D.T., Burden, R.S.: Lipid modulation of plasma memrane-bound ATPases. — Physiol. Plant. 78: 152–159, 1990.

    Article  Google Scholar 

  • Dakhma, W.S., Zarrouk, M., Cherif, A.: Effects of drought-stress on lipids in rape leaves. — Phytochemistry 40: 1383–1386, 1995.

    Article  CAS  Google Scholar 

  • Deuticke, B., Haest, C.W.M.: Lipid modulation of transport proteins in vertebrate cell-membranes. — Annu. Rev. Physiol. 49: 221–235, 1987.

    Article  CAS  PubMed  Google Scholar 

  • Domonkos, I., Laczkó-Dobos, H., Gombos, Z.: Lipid-assisted protein-protein interactions that support photosynthetic and other cellular activities. — Prog. Lipid. Res. 47: 422–435, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Gigon, A., Matos, A.R., Laffray, D., Zuily-Fodil, Y., Pham-Thi, A.T.: Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). — Ann. Bot. 94: 345–351, 2004.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Inaba, M., Sakamoto, A., Murata, N.: Functional expression in Escherichia coli of low-affinity and high-affinity Na+(Li+)/H+ antiporters of Synechocystis. — J. Bacteriol. 183: 1376–1384, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Liu, X.-Y., Li, B., Yang, J.-H., Sui, N., Yang, X.-M., Meng, Q.-W.: Overexpression of tomato chloroplast omega-3 fatty acid desaturase gene alleviates the photoinhibition of photosystems 2 and 1 under chilling stress. — Photosynthetica 46: 185–192, 2008.

    Article  CAS  Google Scholar 

  • Lu, C.M., Qiu, N.M., Lu, Q.T., Wang, B.S., Kuang, T.Y.: Does salt stress lead to increased susceptibility of photosystem II to photoinhibition and changes in photosynthetic pigment composition in halophyte Suaeda salsa grown outdoors? — Plant Sci. 163: 1063–1068, 2002.

    Article  CAS  Google Scholar 

  • Lu, C.M., Qiu, N.W., Wang, B.S., Zhang, J.H.: Salinity treatment shows no effects on photosystem II photochemistry, but increases the resistance of photosystem II to heat stress in halophyte Suaeda salsa. — J. Exp. Bot. 54: 851–860, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Matos, M.C., Campos, P.S., Ramalho, J.C., Medeira, M.C., Maia, M.I., Semedo, J.M., Marques, N.M., Matos, A.: Photosynthetic activity and cellular integrity of the Andean legume Pachyrhizus ahipa (Wedd.) Parodi under heat and water stress. — Photosynthetica 40: 493–501, 2002.

    Article  CAS  Google Scholar 

  • Mikami, K., Murata, N.: Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. — Prog. Lipid. Res. 42: 527–543, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Muller, M., Santarius, K.A.: Changes in chloroplast membrane lipids during adaptation of barley to extreme salinity. — Plant Physiol. 62: 326–329, 1978.

    Article  CAS  PubMed  Google Scholar 

  • Munns, R., Tester, M.: Mechanisms of saline tolerance. — Annu. Rev. Plant Biol. 59: 651–681, 2008.

    Article  CAS  PubMed  Google Scholar 

  • Olsson, M.: Alteration in lipid-composition, lipid-peroxidation and antioxidative protection during senescence in drought-stressed plants of Pisum sativum. — Plant Physiol. Biochem. 33: 547–553, 1995.

    CAS  Google Scholar 

  • Qiu, N., Chen, M., Yang, H., Wang, B.: [Comparative studies on the mechanisms of salt-tolerance and drought-tolerance of Kalanchoë daigremontiana and Suaeda salsa.] — Shandong Sci. China 14: 5–10, 2001. [In Chin.]

    Google Scholar 

  • Ramani, B., Zorn, H., Papentsrock, J.: Quantification and fatty acid profiles of sulfolipids of two halophytes and glycophytes grown under different salt concentrations. — Z. Naturforsch. 59: 835–842, 2004.

    CAS  Google Scholar 

  • Rodríguez-Vargas, S., Sánchez-García, A., Martínez-Rivas, J.M., Prieto, J.A., Randez-Gil, F.: Fluidization of membrane lipids enhances the tolerance of Saccharomyces cerevisiae to freezing and salt stress. — Appl. Environ. Microbiol. 73: 110–116, 2007.

    Article  PubMed  Google Scholar 

  • Schuler, I., Milon, A., Nakatani, Y., Ourisson, G., Albrecht, A.M., Benveniste, P., Hartmann, M.A.: Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers. — Proc. Nat. Acad. Sci. USA 88: 6926–6930, 1991.

    Article  CAS  PubMed  Google Scholar 

  • Siegenthaler, P.-A.: Molecular organization of acyl lipids in photosynthetic membranes of higher plants. — In: Siegenthaler, P.-A., Murata, N. (ed.): Lipids in Photosynthesis. Pp. 119–144. Kluwer Acad. Publ., Dordrecht — Boston — London 1998.

    Google Scholar 

  • Siegenthaler, P.-A., Eichenberger, W.: Structure, function and metabolism of plant lipids. — In: Plant Lipids-Metabolism- Congresses. Pp. 485–488. Elsevier Science Publ., Amsterdam 1984.

    Google Scholar 

  • Staehelin, L.A.: Chloroplast structure: from chlorophyll granules to supra-molecular architecture of thylakoid membranes. — Photosynth. Res. 76: 185–196, 2003.

    Article  CAS  PubMed  Google Scholar 

  • Sui, N., Li, M., Shu, D.F., Zhao, S.J., Meng, Q.W.: Antisense-mediated depletion of tomato chloroplast glycerol-3-phosphate acyltransferase affects male fertility and increases thermal tolerance. — Physiol. Plant. 130: 301–314, 2007b.

    Article  CAS  Google Scholar 

  • 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, 2007a.

    Article  CAS  PubMed  Google Scholar 

  • Upchurch, R.G.: Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. — Biotechnol. Lett. 30: 967–977, 2008.

    Article  CAS  PubMed  Google Scholar 

  • van Kooten, O., Snel, J.F.H.: The use of chlorophyll fluorescence nomenclature in plant stress physiology. — Photosynth. Res. 25: 147–150, 1990.

    Article  Google Scholar 

  • Wang, B.S., Lüttge, U., Ratajczak, R.: Effects of salt treatment and osmotic stress on V-ATPase and V-PPase in leaves of the halophyte Suaeda salsa. — J. Exp. Bot. 52: 2355–2365, 2001.

    Article  CAS  PubMed  Google Scholar 

  • Xu, Y.N., Siegenthaler, P.A.: Low temperature treatments induce an increase in the relative content of both linolenic and Δ3-transhexadecenoic acids in thylakoid membrane phosphatidylglycerol of squash cotyledons. — Plant Cell Physiol. 38: 611–618, 1997.

    CAS  Google Scholar 

  • Zhang, M., Barg, R., Yin, M.G., Gueta-Dahan, Y., Leikin-Frenkel, A., Salts, Y., Shabtai, S., Ben-Hayyim, G.: Modulated fatty acid desaturation via overexpression of two distinct x-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. — Plant J. 44: 361–371, 2005.

    Article  CAS  PubMed  Google Scholar 

  • Zhao, S.J., Shi, G.A., Dong, X.C.: [Techniques of Plant Physiological Experiment.] — China Agr. Sci. Tech. Press, Beijing 2002. [In Chin.]

    Google Scholar 

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Acknowledgements

We are grateful for financial support from the NSFC (National Natural Science Research Foundation of China, project No. 30870138), the China Postdoctoral Science Foundation (20090450155), the Doctoral Foundation of Shandong Province (2009BSB02023), the Postdoctoral Innovative Foundation of Shandong Province (200802009), and the Opening Foundation of the State Key Laboratory of Crop Biology, China (2008KF03).

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Sui, N., Li, M., Li, K. et al. Increase in unsaturated fatty acids in membrane lipids of Suaeda salsa L. enhances protection of photosystem II under high salinity. Photosynthetica 48, 623–629 (2010). https://doi.org/10.1007/s11099-010-0080-x

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  • DOI: https://doi.org/10.1007/s11099-010-0080-x

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