Metabolome and water homeostasis analysis of Thellungiella salsuginea suggests that dehydration tolerance is a key response to osmotic stress in this halophyte

Plant Journal

Volumn 64, Issue 2, 2010, Pages 215-229

  Lugan, Raphaël ^a   Niogret, Marie Françoise ^a   Leport, Laurent ^a   Guégan, Jean Paul ^b   Larher, François Robert ^a   Savouré, Arnould ^c   Kopka, Joachim ^d   Bouchereau, Alain ^a  

^a AGROCAMPUS OUEST   (France)

^b UNIV RENNES   (France)

^c SORBONNE UNIVERSITÉ   (France)

^d MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

Author keywords

Arabidopsis relative halophyte; Compatible solutes; Metabolic profiling; Osmo adaptation; Osmotic stress tolerance; Plant metabolomics

Indexed keywords

ARABIDOPSIS; COMPATIBLE SOLUTES; METABOLIC PROFILING; OSMO-ADAPTATION; OSMOTIC STRESS; PLANT METABOLOMICS;

BIOMOLECULES; BODY FLUIDS; DEHYDRATION; DEWATERING; METABOLISM; METABOLITES; PLANTS (BOTANY);

OSMOSIS;

SODIUM CHLORIDE; WATER;

ARABIDOPSIS; ARTICLE; COMPARATIVE STUDY; DRUG EFFECT; ELECTROLYTE BALANCE; GROWTH, DEVELOPMENT AND AGING; HALOPHYTE; METABOLISM; METABOLOME; METABOLOMICS; PHYSIOLOGICAL STRESS; SALINITY;

ARABIDOPSIS; METABOLOME; METABOLOMICS; SALINITY; SALT-TOLERANT PLANTS; SODIUM CHLORIDE; STRESS, PHYSIOLOGICAL; WATER; WATER-ELECTROLYTE BALANCE;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BRASSICACEAE; THELLUNGIELLA; THELLUNGIELLA SALSUGINEA;

EID: 78649538949     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04323.x     Document Type: Article

References (74)

1. Adams, M A. Chen, Z.L., Landman, P. and Colmer, T.D. (1999) Simultaneous determination by capillary gas chromatography of organic acids, sugars, and sugar alcohols in plant tissue extracts as their trimethylsilyl derivatives. Anal. Biochem. 266, 77-84.
2. Alberty, R.A. (2001) BasicBiochemData 2-data and programs for biochemical thermodynamics [WWW document]. http://library.wolfram.com/infocenter/ MathSource/797 [accessed 30 May 2008].
3. Amend, J.P. and Helgeson, H. (1997) Calculation of the standard molal thermodynamic properties of aqueous biomolecules at elevated temperatures and pressures. Part 1: l-α-amino acids. J. Chem. Soc. Faraday Trans. 93, 1927-1941.
4. Amtmann, A. (2009) Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. Mol. Plant, 2, 3-12.
5. Amtmann, A., Bohnert, H.J. and Bressan, R.A. (2005) Abiotic stress and plant genome evolution. Search for new models. Plant Physiol. 138, 127-130.
6. Armengaud, P., Sulpice, R., Miller, A.J., Stitt, M., Amtmann, A. and Gibon, Y. (2009) Multilevel analysis of primary metabolism provides new insights into the role ofpotassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots. Plant Physiol. 150, 772-785.
7. Bentley, R., Franzen, J. and Chasteen, T.G. (2002) Oxidation numbers in the study of metabolism. Biochem. Mol. Biol. Educ. 30, 288-292.
8. Bohnert, H.J. and Jensen, R.G. (1996) Strategies for engineering water-stress tolerance in plants. Trends Biotechnol. 14, 89-97.
9. Bohnert, H.J., Nelson, D.E. and Jensen, R.G. (1995) Adaptations to environmental stresses. Plant Cell, 7, 1099-1111.
10. Bouchereau, A., Aziz, A., Larher, F. and Martin-Tanguy, J. (1999a) Polyamines and environmental challenges: recent development. Plant Sci. 140, 103-125.
11. Bouchereau, A., Duhazé, C., Martin-Tanguy, J., Guégan, J.-P. and Larher, F. (1999b) Improved analytical methods for determination of nitrogenous stress metabolites occurring in Limonium species. J. Chromatogr. A, 836, 209-221.
12. Boyes, D.C., Zayed, A.M., Ascenzi, R., McCaskill, A.J., Hoffman, N.E., Davis, K.R. and Gorlach, J. (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell, 13, 1499-1510.
13. Bray, E.A. (1993) Molecular responses to water deficit. Plant Physiol. 103, 1035-1040.
14. Bressan, R.A., Zhang, C., Zhang, H., Hasegawa, P.M., Bohnert, H.J. and Zhu, J.-K. (2001) Learning from the Arabidopsis experience. The next gene search paradigm. Plant Physiol. 127, 1354-1360.
15. Cohen, S.A. and Michaud, D.P. (1993) Synthesis of a fluorescent derivatizing reagent, 6-aminoquinolyl-N-hydroxysuccinimidyl carbamate, and its application for the analysis of hydrolysate amino acids via high-performance liquid chromatography. Anal. Biochem. 211, 1-9.
16. Colebatch, G., Desbrosses, G., Ott, T., Krusell, L., Montanari, O., Kloska, S., Kopka, J. and Udvardi, M.K. (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J. 39, 487-512.
17. Cuevas, J.C., Lopez-Cobollo, R., Alcazar, R., Zarza, X., Koncz, C., Altabella, T., Salinas, J., Tiburcio, A.F. and Ferrando, A. (2008) Putrescine is involved in Arabidopsis freezing tolerance and cold acclimation by regulating abscisic acid levels in response to low temperature. Plant Physiol. 148, 1094-1105.
18. Cushman, C. (2001) Crassulacean acid metabolism. A plastic photosynthetic adaptation to arid environment: celebrating plant diversity. Plant Physiol. 127, 1439-1448.
19. Desbrosses, G., Kopka, J. and Udvardi, M.K. (2005) Lotus japonicus metabolic profiling. Development of gas chromatography-mass spectrometry resources for the study of plant-microbe interactions. Plant Physiol. 137, 1302-1318.
20. Faraday, C.D. and Thomson, W.W. (1986) Structural aspects of the salt glands in the Plumbaginaceae. J. Exp. Bot. 37, 461-470.
21. Fiehn, O., Kopka, J., Trethewey, R.N. and Willmitzer, L. (2000) Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry. Anal. Chem. 72, 3573-3580.
22. Fiehn, O., Sumner, L.W., Rhee, S.Y., Ward, J., Dickerson, J., Lange, B.M., Lane, G., Roessner, U., Last, R. and Nikolau, B. (2007) Minimum reporting standards for plant biology context information in metabolomic studies. Metabolomics, 3, 195-201.
23. Flowers, T.J. (2004) Improving crop salt tolerance. J. Exp. Bot. 55, 307-319.
24. Gagneul, D., Ainouche, A., Duhazé, C., Lugan, R., Larher, F.R. and Bouchereau, A. (2007) A reassessment of the function of the so-called compatible solutes in the halophytic Plumbaginaceae Limonium latifolium. Plant Physiol. 144, 1598-1611.
25. + selectivity and proline accumulation. J. Plant Physiol. 165, 588-599.
26. Gilles, R. (1997) 'Compensatory' organic osmolytes in high osmolarity and dehydration stresses: historyand perspectives. Comp. Biochem. Physiol. A Physiol. 117, 279-290.
27. Gong, Q., Li, P., Ma, S., Rupassara, S.I. and Bohnert, H.J. (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J. 44, 826-839.
28. Hanzawa, Y., Takahashi, T., Michael, A.J., Burtin, D., Long, D., Pineiro, M., Coupland, G. and Komeda, Y. (2000) ACAULIS5, an Arabidopsis gene required for stem elongation, encodes a spermine synthase. EMBO J. 19, 4248-4256.
29. Hare, P.D., Cress, W.A. and Staden, J.V. (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ. 21, 535-553.
30. Hayman, A.R., Gray, D.O. and Evans, S.V. (1985) New high-performance liquid chromatography system for the separation of biogenic amines as their Dns derivatives. J. Chromatogr. 325, 462-466.
31. Hendrawati, O., Yao, Q., Kim, H.K., Linthorst, H.J.M., Erkelens, C., Lefeber, A.W.M., Choi, Y.H. and Verpoorte, R. (2006) Metabolic differentiation of Arabidopsis treated with methyl jasmonate using nuclear magnetic resonance spectroscopy. Plant Sci. 170, 1118-1124.
32. Hincha, D.K. and Hagemann, M. (2004) Stabilization of model membranes during drying by compatible solutes involved in the stress tolerance of plants and microorganisms. Biochem. J. 383, 277-283.
33. Inan, G., Zhang, Q., Li, P. et al. (2004) Salt cress. 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.
34. Jubault, M., Hamon, C., Gravot, A., Lariagon, C., Delourme, R., Bouchereau, A. and Manzanares-Dauleux, M.J. (2008) Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes. Plant Physiol. 146, 2008-2019.
35. + uptake in T. halophila. Plant Cell Environ. 29, 1220-1234.
36. Kant, S., Bi, Y.-M., Weretilnyk, E., Barak, S. and Rothstein, S.J. (2008) The Arabidopsis halophytic relative Thellungiella halophila tolerates nitrogenlimiting conditions by maintaining growth, nitrogen uptake, and assimilation. Plant Physiol. 147, 1168-1180.
37. Kartashov, A., Radyukina, N., Ivanov, Y., Pashkovskii, P., Shevyakova, N. and Kuznetsov, V. (2008) Role of antioxidant systems in wild plant adaptation to salt stress. Russ. J. Plant Physiol. 55, 463-468.
38. Kopka, J., Schauer, N., Krueger, S. et al. (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics, 21, 1635-1638.
39. Kreps, J.A., Wu, Y., Chang, H.-S., Zhu, T., Wang, X. and Harper, J.F. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129-2141.
40. Le Gall, G., Metzdorff, S.B., Pedersen, J., Bennett, R.N. and Colquhoun, I.J. (2005) Metabolite profiling of Arabidopsis thaliana (L.) plants transformed with an antisense chalcone synthase gene. Metabolomics 1,181-198.
41. Levitt, J. (1972) Responses of Plants to Environmental Stresses. New York: Academic Press.
42. Lugan, R., Niogret, M.-F., Kervazo, L., Larher, F.R., Kopka, J. and Bouchereau, A. (2009) Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant Cell Environ. 32, 95-108.
43. Luttge, U. (1993) The role of Crassulacean acid metabolism (CAM) in the adaptation of plants to salinity. New Phytol. 125, 59-71.
44. Meyer, R.C., Steinfath, M., Lisec, J. et al. (2007) The metabolic signature related to high plant growth rate in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA, 104, 4759-4764.
45. Michel, B.E. (1983) Evaluation of the water potentials of solutions of polyethylene glycol 8000 both in the absence and presence of other solutes. Plant Physiol. 72, 66-70.
46. Morgan, J.M. (1984) Osmoregulation and water stress in higher plants. Annu. Rev. Plant Physiol. 35, 299-319.
47. M'rah, S., Ouerghi, Z., Berthomieu, C., Havaux, M., Jungas, C., Hajji, M., Grignon, C. and Lachaal, M. (2006) Effects of NaCl on the growth, ion accumulation and photosynthetic parameters of Thellungiella halophila. J. Plant Physiol. 163, 1022-1031.
48. Munns, R. (2002) Comparative physiology of salt and water stress. Plant Cell Environ. 25, 239-250.
49. Nishizawa, A., Yabuta, Y. and Shigeoka, S. (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol. 147, 1251-1263.
50. Oliver, M.J., Tuba, Z.N. and Mishler, B.D. (2000) The evolution of vegetative desiccation tolerance in land plants. Plant Ecol. 151, 85-100.
51. Peters, S., Mundree, S.G., Thomson, J.A., Farrant, J.M. and Keller, F. (2007) Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J. Exp. Bot. 58, 1947-1956.
52. Richards, R.A. (1996) Defining selection criteria to improve yield under drought. Plant Growth Regul. 20, 157-166.
53. Roessner, U., Wagner, C., Kopka, J., Trethewey, R.N. and Willmitzer, L. (2000) Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J. 23, 131-142.
54. Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L. and Fernie, A.R. (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell, 13, 11-29.
55. Rontein, D., Basset, G. and Hanson, A.D. (2002) Metabolic engineering of osmoprotectant accumulation in plants. Metab. Eng. 4, 49-56.
56. Sanchez, D.H., Lippold, F., Redestig, H., Hannah, M.A., Erban, A., Kraemer, U., Kopka, J. and Udvardi, M.K. (2008a) Integrative functional genomics of salt acclimatization in the model legume Lotus japonicus. Plant J. 53, 973-987.
57. Sanchez, D.H., Siahpoosh, M.R., Roessner, U., Udvardi, M. and Kopka, J. (2008b) Plant metabolomics reveals conserved and divergent metabolic responses to salinity. Physiol. Plant. 132, 209-219.
58. Schobert, B. (1977) Is there an osmotic regulatory mechanism in algae and higher plants? J. Theor. Biol. 68, 17-26.
59. Smith, M.A. and Davies, P.J. (1985) Separation and quantitation of polyamines in plant tissue by high performance liquid chromatography of their dansyl derivatives. Plant Physiol. 78, 89-91.
60. Stepien, P. and Johnson, G.N. (2009) 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.
61. Sumner, L.W., Amberg, A., Barrett, D. et al. (2007) Proposed minimum reporting standards for chemical analysis. Metabolomics, 3, 211-221.
62. Taji, T., Seki, M., Satou, M., Sakurai, T., Kobayashi, M., Ishiyama, K., Narusaka, Y., Narusaka, M., Zhu, J.-K. and Shinozaki, K. (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol. 135, 1697-1709.
63. Tipirdamaz, R., Gagneul, D., Duhazé, C., A'inouche, A., Monnier, C., Ozkum, D. and Larher, F.R. (2006) Clustering of halophytes from an inland salt marsh in Turkey according to their ability to accumulate sodium and nitrogenous osmolytes. Environ. Exp. Bot. 57, 139-153.
64. + transport mechanisms required for salinity tolerance. Plant Physiol. 139, 1507-1517.
65. Verpoorte, R., Choi, Y. and Kim, H. (2007) NMR-based metabolomics at work in phytochemistry. Phytochem. Rev. 6, 3-14.
66. Verslues, P.E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J. and Zhu, J.-K. (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45, 523-539.
67. + homeostasis under salinity stress. Plant J. 48, 342-353.
68. Volkov, V., Wang, B., Dominy, P.J., Fricke, W. and Amtmann, A. (2004) Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant Cell Environ. 27, 1-14.
69. Wang, W., Vinocur, B. and Altman, A. (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta, 218, 1-14.
70. Wang, Z.I., Li, P.-H., Fredricksen, M. et al. (2004) Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerance. Plant Sci. 166, 609-616.
71. Wang, B., Davenport, R.J., Volkov, V. and Amtmann, A. (2006) Low unidirectional sodium influx into root cells restricts net sodium accumulation in Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana. J. Exp. Bot. 57, 1161-1170.
72. Wingler, A., Lea, P.J., Quick, W.P. and Leegood, R.C. (2000) Photorespiration: metabolic pathways and their role in stress protection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 1517-1529.
73. Wong, C.E., Li, Y., Labbe, A. et al. (2006) Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. Plant Physiol. 140, 1437-1450.
74. Yancey, P.H. (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J. Exp. Biol. 208, 2819-2830.