Biologia Plantarum

, Volume 57, Issue 1, pp 149–153 | Cite as

Lipid profiling and tolerance to low-temperature stress in Thellungiella salsuginea in comparison with Arabidopsis thaliana

  • X. D. Zhang
  • R. P. Wang
  • F. J. Zhang
  • F. Q. Tao
  • W. Q. Li
Brief Communication


Changes in membrane lipid composition is a fundamental strategy for plants to resist low-temperature stress. We compared members of 11 membrane glycerolipid classes in Thellungiella salsuginea and its close relative Arabidopsis thaliana at normal growth temperature, and during cold acclimation (CA), freezing (FR), and post-freezing recovery (PFR). The results showed several properties of T. salsuginea distinct from that in A. thaliana, which included: 1) low relative content of phosphatidic acid (PA) and a rapid increase and decrease of PA during FR and PFR respectively; 2) insensitivity of lyso-phospholipids to freezing; and 3) high ratio of phosphatidylcholine to phosphatidylethanolamine. All these properties were in favour of maintaining membrane integrity and stability and therefore enable T. salsuginea to be more tolerant to freezing than A. thaliana.

Additional key words

cold acclimation freezing membrane glycerolipids post-freezing recovery 



cold acclimation


C-repeat binding factor
















phosphatidic acid






post-freezing recovery








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  1. Atici, O., Demir, Y., Kocacaliskan, I.: Effects of low temperature on winter wheat and cabbage leaves. — Biol. Plant. 46: 603–606, 2003.CrossRefGoogle Scholar
  2. Boyer, J.S.: Plant productivity and environment. — Science 218: 443–448, 1982.PubMedCrossRefGoogle Scholar
  3. Cullis, P.R., Dekruijff, B.: Lipid polymorphism and the functional roles of lipids in biological membranes. — Biochim. biophys. Acta 559: 399–420, 1979.PubMedCrossRefGoogle Scholar
  4. Du, J., Huang, Y.P., Xi, J., Cao, M.J., Ni, W.S., Chen, X., Zhu, J.K., Oliver, D.J., Xiang, C.B.: Functional gene-mining for salt-tolerance genes with the power of Arabidopsis. — Plant J. 56: 653–664, 2008.PubMedCrossRefGoogle Scholar
  5. Gao, F., Zhou, Y.J., Huang, L.Y., He, D.C., Zhang, G.F.: Proteomic analysis of long-term salinity stress-responsive proteins in Thellungiella halophila leaves. — Chinese Sci. Bull. 53: 3530–3537, 2008.CrossRefGoogle Scholar
  6. Gao, F., Zhou, Y.J., Zhu, W.P., Li, X.F., Fan, L.M., Zhang, G.F.: Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. — Planta 230: 1033–1046, 2009.PubMedCrossRefGoogle Scholar
  7. Gong, Q., Li, P., Ma, S., Indu Rupassara, S., Bohnert, H.J.: Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. — Plant J. 44: 826–839, 2005.PubMedCrossRefGoogle Scholar
  8. Griffith, M., Timonin, M., Wong, A.C.E., Gray, G.R., Akhter, S.R., Saldanha, M., Rogers, M.A., Weretilnyk, E.A., Moffatt, B.: Thellungiella: an Arabidopsis-related model plant adapted to cold temperatures. — Plant Cell Environ. 30: 529–538, 2007.PubMedCrossRefGoogle Scholar
  9. Harwood, J.L. (ed): Plant Lipid Biosynthesis: Fundamentals and Agricultural Applications. Pp. 155–184. Cambridge University Press, Cambridge 1998.Google Scholar
  10. Hong, Y., Devaiah, S.P., Bahn, S.C., Thamasandra, B.N., Li, M., Welti, R., Wang, X.: Phospholipase Dɛ and phosphatidic acid enhance Arabidopsis nitrogen signaling and growth. — Plant J. 58: 376–387, 2009.PubMedCrossRefGoogle Scholar
  11. Inan, G., Zhang, Q., Li, P., Wang, Z., Cao, Z., Zhang, H., Zhang, C., Quist, T.M., Goodwin, S.M., Zhu, J., Shi, H., Damsz, B., Charbaji, T., Gong, Q., Ma, S., Fredricksen, M., Galbraith, D.W., Jenks, M.A., Rhodes, D., Hasegawa, P.M., Bohnert, H.J., Joly, R.J., Bressan, R.A., Zhu, J.K.: Salt stress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. — Plant Physiol. 135: 1718–1737, 2004.PubMedCrossRefGoogle Scholar
  12. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., Thomashow, M.F..: Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. — Science 280: 104–106, 1998.PubMedCrossRefGoogle Scholar
  13. Kant, S., Bi, Y.M., Weretilnyk, E., Barak, S., Rothstein, S.J.: The Arabidopsis halophytic relative Thellungiella halophila tolerates nitrogen-limiting conditions by maintaining growth, nitrogen uptake, and assimilation. — Plant Physiol. 147: 1168–1180, 2008.PubMedCrossRefGoogle Scholar
  14. Levitt, J. (ed.): Responses of Plants to Environmental Stresses: Chilling, Freezing, and High Temperature Stresses. 2nd Revised Ed. — Academic Press, New York 1980.Google Scholar
  15. Li, L., Li, W.: Profiling the changes of molecular species in membrane lipids during cold-acclimationin winter and spring cultivars of rapeseed (Brassicanapus). — Acta bot. yunnan. 32: 347–354, 2010.Google Scholar
  16. Li, P.H., Mane, S.P., Sioson, A.A., Robinet, C.V., Heath, L.S., Bohnert, H.J., Grene, R.: Effects of chronic ozone exposure on gene expression in Arabidopsis thaliana ecotypes and in Thellungielia halophila. — Plant Cell Environ. 29: 854–868, 2006.PubMedCrossRefGoogle Scholar
  17. Li, W., Li, M., Zhang, W., Welti, R., Wang, X.: The plasma membrane-bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana. — Nat. Biotechnol. 22: 427–433, 2004.PubMedCrossRefGoogle Scholar
  18. Li, W., Wang, R., Li, M., Li, L., Wang, C., Welti, R., Wang, X.: Differential degradation of extraplastidic and plastidic lipids during freezing and post-freezing recovery in Arabidopsis thaliana. — J. biol. Chem. 283: 461–468, 2008.PubMedCrossRefGoogle Scholar
  19. Rahman, L.N., Bamm, V.V., Voyer, J.A., Smith, G.S., Chen, L., Yaish, M.W., Moffatt, B.A., Dutcher, J.R., Harauz, G.: Zinc induces disorder-to-order transitions in free and membraneassociated Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2: a solution CD and solid-state ATR-FTIR study. — Amino Acids 40: 1485–1502, 2010.PubMedCrossRefGoogle Scholar
  20. Sang, Y., Zheng, S., Li, W., Huang, B., Wang, X.: Regulation of plant water loss by manipulating the expression of phospholipase Dα. — Plant J. 28: 135–144, 2001.PubMedCrossRefGoogle Scholar
  21. Stepien, P., Johnson, G.N.: Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and the halophyte Thellungiella: role of the plastid terminal oxidase as an alternative electron sink. — Plant Physiol. 149: 1154–1165, 2009.PubMedCrossRefGoogle Scholar
  22. Steponkus, P.L., Uemura, M., Webb, M.A.: A contrast of the cryostability of the plasma membrane of winter rye and spring oat — two species that differ widely in their freezing tolerance and plasma membrane lipid composition. — In: Steponkus, P.L. (ed): Advances in Low-Temperature Biology. Pp. 211–312. JAI Press, Greenwich 1993.Google Scholar
  23. Steponkus, P.L., Uemura, M., Joseph, R.A., Gilmour, S.J., Thomashow, M.F.: Mode of action of the COR15a gene on the freezing tolerance of Arabidopsis thaliana. — Proc. nat. Acad. Sci. USA 95: 14570–14575, 1998.PubMedCrossRefGoogle Scholar
  24. Taji, T., Seki, M., Satou, M., Sakurai, T., Kobayashi, M., Ishiyama, K., Narusaka, Y., Narusaka, M., Zhu, J.K., Shinozaki, K.: Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. — Plant Physiol. 135: 1697–1709, 2004.PubMedCrossRefGoogle Scholar
  25. Tocquin, P., Corbesier, L., Havelange, A., Pieltain, A., Kurtem, E., Bernier, G., Perilleux, C.: A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. — BMC Plant Biol. 3: 2–--, 2003.PubMedCrossRefGoogle Scholar
  26. Uemura, M., Joseph, R.A., Steponkus, P.L.: Cold-acclimation of Arabidopsis thaliana — effect on plasma-membrane lipidcomposition and freeze-induced lesions. — Plant Physiol. 109: 15–30, 1995.PubMedGoogle Scholar
  27. Uemura, M., Steponkus, P.L.: Cold acclimation in plants: relationship between the lipid composition and the cryostability of the plasma membrane. — J. Plant Res. 112: 245–254, 1999.CrossRefGoogle Scholar
  28. Upchurch, R.G.: Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. — Biotechnol. Lett. 30: 967–977, 2008.PubMedCrossRefGoogle Scholar
  29. Verkleij, A.J., De Maagd, R., Leunissen-Bijvelt, J., De Kruijff, B.: Divalent cations and chlorpromazine can induce nonbilayer structures in phosphatidic acid-containing model membranes. — Biochim. biophys. Acta 684: 255–262, 1982.PubMedCrossRefGoogle Scholar
  30. Wang, C., Zien, C.A., Afitlhile, M., Welti, R., Hildebrand, D.F., Wang, X.: Involvement of phospholipase D in woundinduced accumulation of jasmonic acid in Arabidopsis. — Plant Cell 12: 2237–2246, 2000.PubMedGoogle Scholar
  31. Welti, R., Li, W.Q., Li, M.Y., Sang, Y.M., Biesiada, H., Zhou, H.E., Rajashekar, C.B., Williams, T.D., Wang, X.M.: Profiling membrane lipids in plant stress responses — Role of phospholipase Dα in freezing-induced lipid changes in Arabidopsis. — J. biol. Chem. 277: 31994–32002, 2002.PubMedCrossRefGoogle Scholar
  32. Wong, C.E., Li, Y., Labbe, A., Guevara, D., Nuin, P., Whitty, B., Diaz, C., Golding, G.B., Gray, G.R., Weretilnyk, E.A., Griffith, M., Moffatt, B.A.: Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. — Plant Physiol. 140: 1437–1450, 2006.PubMedCrossRefGoogle Scholar
  33. Zhang, X.Y., Liang, C., Wang, G.P., Luo, Y., Wang, W.: The protection of wheat plasma membrane under cold stress by glycine betaine overproduction. — Biol. Plant. 54: 83–88, 2010.CrossRefGoogle Scholar
  34. Zhang, Y., Zhu, H., Zhang, Q., Li, M., Yan, M., Wang, R., Wang, L., Welti, R., Zhang, W., Wang, X.: Phospholipase D alpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. — Plant Cell 21: 2357–2377, 2009.PubMedCrossRefGoogle Scholar
  35. Zhu, J.K.: Plant salt tolerance. — Trends Plant Sci. 6: 66–71, 2001.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • X. D. Zhang
    • 1
    • 3
  • R. P. Wang
    • 2
  • F. J. Zhang
    • 2
  • F. Q. Tao
    • 2
  • W. Q. Li
    • 1
    • 2
  1. 1.Key Laboratory of Biodiversity and Biogeography, Kunming Institute of BotanyChinese Academy of SciencesKunming YunnanChina
  2. 2.Germplasm Bank of Wild Species, Kunming Institute of BotanyChinese Academy of SciencesKunming YunnanChina
  3. 3.Graduate School of the Chinese Academy of SciencesBeijingChina

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