Biologia plantarum 2013, 57:149-153 | DOI: 10.1007/s10535-012-0137-8

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

X. D. Zhang1,3, R. P. Wang2, F. J. Zhang2, F. Q. Tao2, W. Q. Li1,2,*
1 Key Laboratory of Biodiversity and Biogeography, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming Yunnan, China
2 Germplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming Yunnan, China
3 Graduate School of the Chinese Academy of Sciences, Beijing, China

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.

Keywords: cold acclimation; freezing; membrane glycerolipids; post-freezing recovery
Subjects: lipids; temperature low; cold acclimation; freezing; membrane glycerolipids; post-freezing recovery
Species: Arabidopsis thaliana; Thellungiella salsuginea

Received: September 8, 2011; Accepted: December 21, 2011; Published: March 1, 2013Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Zhang, X.D., Wang, R.P., Zhang, F.J., Tao, F.Q., & Li, W.Q. (2013). Lipid profiling and tolerance to low-temperature stress in Thellungiella salsuginea in comparison with Arabidopsis thaliana. Biologia plantarum57(1), 149-153. doi: 10.1007/s10535-012-0137-8.
Download citation

References

  1. Atici, O., Demir, Y., Kocacaliskan, I.: Effects of low temperature on winter wheat and cabbage leaves. - Biol. Plant. 46: 603-606, 2003. Go to original source...
  2. Boyer, J.S.: Plant productivity and environment. - Science 218: 443-448, 1982. Go to original source...
  3. Cullis, P.R., Dekruijff, B.: Lipid polymorphism and the functional roles of lipids in biological membranes. - Biochim. biophys. Acta 559: 399-420, 1979. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  9. Harwood, J.L. (ed): Plant Lipid Biosynthesis: Fundamentals and Agricultural Applications. Pp. 155-184. Cambridge University Press, Cambridge 1998.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  14. Levitt, J. (ed.): Responses of Plants to Environmental Stresses: Chilling, Freezing, and High Temperature Stresses. 2nd Revised Ed. - Academic Press, New York 1980.
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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.
  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. Go to original source...
  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.
  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.
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  28. Upchurch, R.G.: Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. - Biotechnol. Lett. 30: 967-977, 2008. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  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. Go to original source...
  35. Zhu, J.K.: Plant salt tolerance. - Trends Plant Sci. 6: 66-71, 2001. Go to original source...