Dissecting the roles of osmolyte accumulation during stress

Plant, Cell and Environment

Volumn 21, Issue 6, 1998, Pages 535-553

  Hare, P D ^a   Cress, W A ^a   Van Staden, J ^a  

^a UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

Betaine; Cold stress; Drought; Fructans; Mannitol; Osmolytes; Proline; Salinity; Sugar signalling; Trehalose

Indexed keywords

BETAINE; BUFFER; DISSECTION; FRUCTAN; MANNITOL; ONONITOL; OSMOLYTE; PHENOTYPE; PROLINE; REDOX REACTION; SALT TOLERANCE; SIGNAL TRANSDUCTION; STRESS TOLERANCE; TRANSGENIC PLANT; TREHALOSE;

EID: 0031851152     PISSN: 01407791     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-3040.1998.00309.x     Document Type: Review

References (114)

1. Abe H., Yamaguchi-Shinozaki K., Urao T., Iwasaki T., Hosokawa D. & Shinozaki K. (1997) Role of Arabidopsis MYC and MYB homologs in drought-and abscisic acid-regulated gene expression. The Plant Cell 9, 1859-1868.
2. Artus N.N., Uemura M., Steponkus P.L., Gilmour S.J., Lin C. & Thomashow M.F. (1996) Constitutive expression of the cold-regulated Arabidopsis thaliana COR15a gene affects both chloroplast and protoplast freezing tolerance. Proceedings of the National Academy of Sciences, USA 93, 13404-13409.
3. Babiychuk E., Kushnir S., Belles-Boix E., van Montagu M. & Inzé D. (1995) Arabidopsis thaliana NADPH oxidoreductase homologs confer tolerance of yeasts towards the thiol-oxidizing drug diamide. The Journal of Biological Chemistry 270, 26224-26231.
4. Biehler K. & Fock H. (1996) Evidence for the contribution of the Mehler-peroxidase reaction in dissipating excess electrons in drought-stressed wheat. Plant Physiology 112, 265-272.
5. Blum A. & Sullivan C.Y. (1997) The effect of plant size on wheat response to agents of drought stress. I. Root drying. Australian Journal of Plant Physiology 24, 35-41.
6. Bohnert H.J. & Jensen R.G. (1996) Strategies for engineering water-stress tolerance in plants. Trends in Biotechnology 14, 89-97.
7. Büssis D., Heineke D., Sonnewald U., Willmitzer L., Raschke K. & Heldt H.-W. (1997) Solute accumulation and decreased photosynthesis in leaves of potato plants expressing yeast-derived invertase either in the apoplast, vacuole or cytosol. Planta 202, 126-136.
8. Caimi P.G., McCole L.M., Klein T.M. & Hershey H.P. (1997) Cytosolic expression of the Bacillus amyloliquefaciens SacB protein inhibits tissue development in transgenic tobacco and potato. The New Phytologist 136, 19-28.
9. Close T.J. (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiologia Plantarum 100, 291-296.
10. Crowe J.H., Hoekstra F.A. & Crowe L.M. (1992) Anhydrobiosis. Annual Review of Physiology 54, 579-599.
11. Csonka L.N. (1989) Physiological and genetic responses of bacteria to osmotic stress. Microbiological Reviews 53, 121-147.
12. Dörffling K., Dörffling H., Lesselich G., Luck E., Zimmermann C., Melz G. & Jürgens H.U. (1997) Heritable improvement of frost tolerance in winter wheat by in vitro-selection of hydroxyproline-resistant proline overproducing mutants. Euphytica 93, 1-10.
13. Drennan P.M., Smith M.T., Goldsworthy D. & van Staden J. (1993) The occurrence of trehalose in the leaves of the desiccation-tolerant angiosperm Myrothamnus flabellifolius Welw. Journal of Plant Physiology 142, 493-496.
14. Erskine P.D., Stewart G.R., Schmidt S., Turnbull M.H., Unkovich M. & Pate J.S. (1996) Water availability - a physiological constraint on nitrate utilization in plants of Australian semi-arid mulga woodlands. Plant, Cell and Environment 19, 1149-1159.
15. Essery J.M., McCaldin D.J. & Marion L. (1962) The biogenesis of stachydrine. Phytochemistry 1, 209-213.
16. 1-pyrroline-5-carboxylate dehydrogenase isoforms are expressed in cultured Nicotiana plumbaginifolia cells and are differentially modulated during the culture growth cycle. Planta 202, 242-248.
17. Foyer C.H. (1997) Oxygen metabolism and electron transport in photosynthesis. In The Molecular Biology of Free Radical Scavenging Systems (ed. J. Scandalios), pp. 587-621. Cold Spring Harbour Laboratory Press, New York.
18. Foyer C.H., Lelandais M. & Kunert K.J. (1994) Photooxidative stress in plants. Physiologia Plantarum 92, 696-717.
19. Foyer C.H., Lopez-Delgado H., Dat J.F. & Scott I.M. (1997) Hydrogen peroxide-and glutathione-associated mechanisms of acclimatory stress tolerance and signalling. Physiologia Plantarum 100, 241-254.
20. Furini A., Koncz C., Salamini F. & Bartels D. (1997) High level transcription of a member of a repeated gene family confers dehydration tolerance to callus tissue of Craterostigma plantagineum. The EMBO Journal 16, 3599-3608.
21. Garcia A.B., de Almeida Engler J., Iyer S., Gerats T., van Montagu M. & Caplan A.B. (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiology 115, 159-169.
22. García-Ríos M., Fujita T., LaRosa P.C., Locy R.D., Clithero J.M., Bressan R.A. & Csonka L.N. (1997) Cloning of a polycistronic cDNA from tomato encoding γ-glutamyl kinase and γ-glutamyl phosphate reductase. Proceedings of the National Academy of Sciences, USA 94, 8249-8254.
23. Geigenberger P., Reimholz R., Geiger M., Merlo L., Canale V. & Stitt M. (1997) Regulation of sucrose and starch metabolism in potato tubers in response to short-term water deficit. Planta 201, 502-518.
24. Gibon Y., Bessieres M.A. & Larher F. (1997) Is glycine betaine a non-compatible solute in higher plants that do not accumulate it? Plant, Cell and Environment 20, 329-340.
25. Girousse C., Bournoville R. & Bonnemain J.-L. (1996) Water deficit-induced changes in concentrations in proline and some other amino acids in the phloem sap of alfalfa. Plant Physiology 111, 109-113.
26. Goddijn O.J.M., Verwoerd T.C., Voogd E., Krutwagen R.W.H.H., de Graaf P.T.H.M., Poels J., van Dun K., Ponstein A.S., Damm B. & Pen J. (1997) Inhibition of trehalase activity enhances trehalose accumulation in transgenic plants. Plant Physiology 113, 181-190.
27. Graham I.A., Denby K.J. & Leaver C.J. (1994) Carbon catabolite repression regulates glyoxylate cycle gene expression in cucumber. The Plant Cell 6, 761-772.
28. 1-pyrroline-5-carboxylate reductase in Arabidopsis thaliana. Plant Growth Regulation 19, 249-256.
29. Hare P.D. & Cress W.A. (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation 21, 79-102.
30. Hare P.D., Cress W.A. & van Staden J. (1997) The involvement of cytokinins in plant responses to environmental stress. Plant Growth Regulation 23, 79-103.
31. Hare P.D., duPlessis S., Cress W.A. & van Staden J. (1996) Stress-induced changes in plant gene expression: prospects for enhancing agricultural productivity in South Africa. South African Journal of Science 92, 431-439.
32. Hayashi H., Alia Mustardy L., Deshnium P., Ida M. & Murata N. (1997) Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress. The Plant Journal 12, 133-142.
33. Hincha D.K., Sonnewald U., Willmitzer L. & Schmitt J.M. (1996) The role of sugar accumulation in leaf frost hardiness - investigations with transgenic tobacco expressing a bacterial pyrophosphatase or a yeast invertase gene. Journal of Plant Physiology 147, 604-610.
34. Hirayama T., Ohto C., Mizoguchi T. & Shinozaki K. (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 92, 3903-3907.
35. Holmström K.O., Mäntylä E., Welin B., Mandal A. & Palva E.T. (1996) Drought tolerance in tobacco. Nature 379, 683-684.
36. Hua X.-J., van de Cotte B., van Montagu M. & Verbruggen N. (1997) Developmental regulation of pyrroline-5-carboxylate reductase gene expression in Arabidopsis. Plant Physiology 114, 1215-1224.
37. Ingram J. & Bartels D. (1996) The molecular basis of dehydration tolerance in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 377-403.
38. Ishitani M., Majumder A.L., Bornhouser A., Michalowski C.B., Jensen R.G. & Bohnert H.J. (1996) Coordinate transcriptional induction of myo-inositol metabolism during environmental stress. The Plant Journal 9, 537-548.
39. Ishitani M., Nakamura T., Han S.Y. & Takebe T. (1995) Expression of the betaine aldehyde dehydrogenase gene in barley in response to osmotic stress and abscisic acid. Plant Molecular Biology 27, 307-315.
40. Iturriaga G., Leyns L., Villegas A., Gharaibeh R., Salamini F. & Bartels D. (1996) A family of novel myb-related genes from the resurrection plant Craterostigma plantagineum are specifically expressed in callus and roots in response to ABA or desiccation. Plant Molecular Biology 32, 70-716.
41. Iyer S. & Caplan A. (1998) products of proline catabolism can induce osmotically regulated genes in rice. Plant Physiology 116, 203-211.
42. Jang J.-C., León P., Zhou L. & Sheen J. (1997) Hexokinase as a sugar sensor in higher plants. The Plant Cell 9, 5-19.
43. Juhnke H., Krems B., Kötter P. & Entian K.-D. (1996) Mutants that show increased sensitivity to hydrogen peroxide reveal an important role for the pentose phosphate pathway in protection of yeast against oxidative stress. Molecular and General Genetics 252, 456-464.
44. Karakas B., Ozias-Akins P., Stushnoff C., Suefferheld M. & Rieger M. (1997) Salinity and drought tolerance of mannitol-accumulating transgenic tobacco. Plant, Cell and Environment 20, 609-616.
45. Karsten U., Barrow K.D., Nixdorf O., West J.A. & King R.J. (1997) Characterisation of mannitol metabolism in the mangrove red alga Caloglossa leprieurii (Montagne) J.Agardh. Planta 201, 173-178.
46. 1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology 108, 1387-1394.
47. Keller F. & Ludlow M.M. (1993) Carbohydrate metabolism in drought-stressed leaves of pigeonpea (Cajanus cajan). Journal of Experimental Botany 44, 1351-1359.
48. Kiyosue T., Yoshiba Y., Yamaguchi-Shinozaki K. & Shinozaki K. (1996) A nuclear gene encoding mitochondrial proline dehydrogenase, an enzyme involved in proline metabolism, is upregulated by proline but downregulated by dehydration in Arabidopsis. The Plant Cell 8, 1323-1335.
49. Knight H., Trewavas A.J. & Knight M.R. (1997) Calcium signalling in Arabidopsis thaliana responding to drought and salinity. The Plant Journal 12, 1067-1078.
50. Koch K.E. (1996) Carbohydrate-modulated gene expression in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 509-540.
51. Kozaki A. & Takeba G. (1996) Photorespiration protects C3 plants from photooxidation. Nature 384, 557-560.
52. Kruger N.J. (1997) Carbohydrate synthesis and degradation. In Plant Metabolism (eds D.T. Dennis. D.H. Turpin, D.D. Lefebvre & D.B. Layzell), pp. 83-104. Longman, Harlow.
53. Kumar P.A., Polisetty R. & Abrol Y.P. (1993) Interactions between carbon and nitrogen metabolism. In Photosynthesis: Photoreactions to Plant Productivity (eds Y.P. Abrol, P. Mohanty & Govindjee), pp. 339-350. Kluwer Academic Publishers, Dordrecht.
54. Larher F., Leport L., Petrivalsky M. & Chappart M. (1993) Effectors for the osmoinduced proline response in higher plants. Plant Physiology and Biochemistry 31, 911-922.
55. Leegood R.C., Lea P.J., Adcck M.D. & Häusler R.E. (1995) The regulation and control of photorespiration. Journal of Experimental Botany 46, 1397-1414.
56. Leung J., Merlot S. & Giraudat J. (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. The Plant Cell 9, 759-771.
57. Lilius G., Holmberg N. & Bülow L. (1996) Enhanced NaCl stress tolerance in transgenic tobacco expressing bacterial choline dehydrogenase. Bio/Technology 14, 177-180.
58. Liu J. & Zhu J.-K. (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiology 114, 591-596.
59. Maggio A., Bressan R.A., Hasegawa P.M. & Locy R.D. (1997) Moderately increased constitutive proline does not alter osmotic stress tolerance. Physiologia Plantarum 101, 240-246.
60. 4 turfgrasses. Journal of the American Society for Horticultural Science 119, 779-784.
61. Mayne M.B., Coleman J.R. & Blumwald E. (1996) Differential expression during drought conditioning of a root-specific S-adenosylmethionine synthetase from jack pine (Pinus banksiana Lamb.) seedlings. Plant, Cell and Environment 19, 958-966.
62. McKersie B.D., Bowley S.R., Harjanto E. & Leprince O. (1996) Water-deficit tolerance and field performance of transgenic alfalfa overexpressing Superoxide dismutase. Plant Physiology 111, 1177-1181.
63. Müller J., Boller T. & Wiemken A. (1995a) Trehalose and trehalase in plants: recent developments. Plant Science 112, 1-9.
64. Müller J., Boiler T. & Wiemken A. (1995b) Effects of validamycin A, a potent trehalase inhibitor, and phytohormones on trehalose metabolism in roots and root nodules of soybean and cowpea. Planta 197, 362-368.
65. Munns R. (1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant, Cell and Environment 16, 15-24.
66. Nakamura T., Yokota S., Muramoto Y, Tsutsui K., Oguri Y., Kukui K. & Takabe T. (1997) Expression of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine nonaccumulator, and possible localisation of its protein in peroxisomes. The Plant Journal 11, 1115-1120.
67. Noctor G., Arisi A.-C.M., Jouanin L., Valadier M.-H., Roux Y. & Foyer C.H. (1997a) Light-dependent modulation of foliar glutathione synthesis and associated amino acid metabolism in poplar overexpressing γ-glutamylcysteine synthetase. Planta 202, 357-369.
68. Noctor G., Arisi A.-C.M., Jouanin L., Valadier M.-H., Roux Y. & Foyer C.H. (1997b) The role of glycine in determining the rate of glutathione synthesis in poplar. Possible implications for glutathione production during stress. Physiologia Plantarum 100, 255-263.
69. Nolte K.D., Hanson A.D. & Gage D.A. (1997) Proline accumulation and methylation to proline betaine in Citrus: implications for genetic engineering of stress resistance. Journal of the American Society for Horticultural Science 122, 8-13.
70. Parrou J.L., Teste M.-A. & François J. (1997) Effects of various types of stress on the metabolism of reserve carbohydrates in Saccharomyces cerevisiae: genetic evidence for a stress-induced recycling of glycogen and trehalose. Microbiology 143, 1891-1900.
71. Pelleschi S., Rocher J.-P. & Prioul J.L. (1997) Effect of water restriction on carbohydrate metabolism and photosynthesis in mature maize leaves. Plant, Cell and Environment 20, 493-503
72. 1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Molecular and General Genetics 253, 334-341.
73. Pilon-Smits E.A.H., Ebskamp M.J.M., Paul M.J.J.. Jeuken M.J.W., Weisbeek P.J. & Smeekens S.C.M. (1995) Improved performance of transgenic fructan-accumulating tobacco under drought stress. Plant Physiology 107, 125-130.
74. Polle A. (1996) Developmental changes of antioxidative systems in tobacco leaves as affected by limited sucrose export in transgenic plants expressing yeast-invertase in the apoplastic space. Planta 198, 253-262.
75. Prata R.T.N., Williamson J.D., Conkling M.A. & Pharr D.M. (1997) Sugar repression of mannitol dehydrogenase activity in celery cells. Plant Physiology 114, 307-314.
76. Rajendrakumar C.S.V., Suryanarayana T. & Reddy A.R. (1997) DNA helix destabilization by proline and betaine: possible role in the salinity tolerance process. FEBS Letters 410, 201-205.
77. Rathinasabapathi B.. Burnet M., Russell B.L., Gage D.A., Liao P.-C., Nye G.J., Scott P., Golbeck J.H. & Hanson A.D. (1997) Choline monooxygenase, an unusual iron-sulfur enzyme catalysing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proceedings of the National Academy of Sciences, USA 94, 3454-3458.
78. Rathinasabapathi B., McCue K.F., Gage D.A. & Hanson A.D. (1994) Metabolic engineering of glycine betaine synthesis: plant betaine aldehyde dehydrogenases lacking typical transit peptides are targeted to tobacco chloroplasts where they confer betaine aldehyde resistance. Planta 193, 155-162.
79. Raychaudhuri A. & Majumder A.L. (1996) Salinity-induced enhancement of 1-myo-inositol 1-phosphate synthase in rice (Oryza sativa L.) Plant, Cell and Environment 19, 1437-1442.
80. Rentsch D., Hirner B., Schmelzer E. & Frommer W.B. (1996) Salt stress-induced proline transporters and salt stress-repressed broad specificity amino acid permeases identified by suppression of a yeast amino acid permease-targeting mutant. The Plant Cell 8, 1437-1446.
81. Rhodes D. & Hanson A.D. (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 44, 357-384.
82. Romero C., Bellés J.M., Vayá J.L., Serrano R. & Culiáňez-Macià F.A. (1997) Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: pleiotropic phenotypes include drought tolerance. Planta 201, 293-297.
83. Salmon S., Lemoine R., Jamai A., Bouché-Pillon S. & Fromont J.C. (1995) Study of sucrose and mannitol transport in plasma-membrane vesicles from phloem and non-phloem tissues of celery (Apium graveolens L.) petioles. Planta 197, 76-83.
84. Samuel D., Kumar T.K.S., Jayaraman G., Wang P.W. & Yu C. (1997) Proline is a protein solubilizing solute. Biochemistry and Molecular Biology International 41, 235-242.
85. Sanada Y., Ueda H., Kuribayashi K., Andoh T., Hayashi R, Tamai N. & Wada K. (1995) Novel light-dark change of proline levels in halophyte (Mesembryanthemum crystallinum L.) and glycophytes (Hordeum vulgare L. & Triticum aestivum L.) leaves and roots under salt stress. Plant and Cell Physiology 36, 965-970.
86. Sánchez-Fernández R., Fricker M., Corben L.B., White N.S., Sheard N., Leaver C.J., van Montagu M., Inzé D. & May M.J. (1997) Cell proliferation and hair tip growth in the Arabidopsis root are under mechanistically different forms of redox control. Proceedings of the National Academy of Sciences, USA 94, 2745-2750.
87. Saneoka H., Nagasaka C., Hahn D.T., Yang W.J., Premachandra G.S., Joly R.J. & Rhodes D. (1995) Salt tolerance of glycinebetaine-deficient and -containing maize lines. Plant Physiology 107, 631-638.
88. Savouré A., Hua X.-J., Bertauche N., van Montagu M. & Verbruggen N. (1997) Abscisic acid-independent and abscisic acid-dependent regulation of proline biosynthesis following cold and osmotic stresses in Arabidopsis thaliana. Molecular and General Genetics 254, 104-109.
89. Serrano R. (1996) Salt tolerance in plants and microorganisms: toxicity targets and defence responses. International Review of Cytology 165, 1-52.
90. 2+-dependent protein kinases and stress signal transduction in plants. Science 274, 1900-1902.
91. Shen B., Jensen R.G. & Bohnert H.J. (1997) Increased resistance to oxidative stress in transgenic plants by targeting mannitol biosynthesis to chloroplasts. Plant Physiology 113, 1177-1183.
92. Sheveleva E., Chmara W., Bohnert H.J. & Jensen R.G. (1997) Increased salt and drought tolerance by D-ononitol production in transgenic Nicotiana tabacum L. Plant Physiology 115, 1211-1219.
93. Smart C.C. & Flores S. (1997) Overexpression of d-myo-inositol-3-phosphate synthase leads to elevated levels of inositol in Arabidopsis. Plant Molecular Biology 33, 811-820.
94. Smeekens S. & Rook F. (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiology 115, 7-13.
95. Stoop J.M.H., Williamson J.D. & Pharr D.M. (1996) Mannitol metabolism in plants: a method for coping with stress. Trends in Plant Science 1, 139-144.
96. Streb P., Tel-Or E. & Feierabend J. (1997) Light stress effects and antioxidant protection in two desert plants. Functional Ecology 11, 416-424.
97. Strizhov N., Abraham E., Okresz L., Blickling S., Zilberstein A., Schell J., Koncz C. & Szabados L. (1997) Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. The Plant Journal 12, 557-569.
98. Tao R., Uratsu S.L. & Dandekar A.M. (1995) Sorbitol synthesis in transgenic tobacco with apple cDNA encoding NADP-dependent sorbitol-6-phosphate dehydrogenase. Plant and Cell Physiology 36, 525-532.
99. Tarczynski M.C., Jensen R.G. & Bohnert H.J. (1992) Expression of a bacterial mtlD gene in transgenic tobacco leads to production and accumulation of mannitol. Proceedings of the National Academy of Sciences, USA 89, 2600-2604.
100. Tarczynski M.C., Jensen R.G. & Bohnert H.J. (1993) Stress protection of transgenic tobacco by production of the osmolyte mannitol. Science 259, 508-510.
101. Thomas J.C., Sepahi M., Arendall B. & Bohnert H.J. (1995) Enhancement of seed germination in high salinity by engineering mannitol expression in Arabidopsis thaliana. Plant, Cell and Environment 18, 801-806.
102. Toroser D. & Huber S.C. (1997) Protein phosphorylation as a mechanism for osmotic-stress activation of sucrose-phosphate synthase in spinach leaves. Plant Physiology 114, 947-955.
103. Trossat C., Rathinasabapathi B. & Hanson A.D. (1997) Trangenically expressed betaine aldehyde dehydrogenase efficiently catalyses oxidation of dimethylsulfoniopropionaldehyde and ω-aminoaldehydes. Plant Physiology 113, 1457-1461.
104. Turk S.C.H.J., de Roos K., Scotti P.A., van Dun K., Weisbeek P. & Smeekens S.C.M. (1997) The vacuolar sorting domain of sporamin transports GUS, but not levansucrase, to the plant vacuole. The New Phytologist 136, 29-38.
105. Verbruggen N., Hua X.-J., May M. & van Montagu M. (1996) Environmental and developmental signals modulate proline homeostasis: evidence for a negative transcriptional regulator. Proceedings of the National Academy of Sciences, USA 93, 8787-8791.
106. Weretilnyk E.A., Smith D.D., Wilch G.A. & Summers P.S. (1995) Enzymes of choline synthesis in spinach: response of phosphobase N-methyltransferase activities to light and salinity. Plant Physiology 109, 1085-1091.
107. Werner J.E. & Finkelstein R.R. (1995) Arabidopsis mutants with reduced response to NaCl and osmotic stress. Physiologia Plantarum 93, 659-666.
108. Westgate M.E. & Boyer J.S. (1985) Osmotic adjustment and the inhibition of leaf, root, stem and silk growth at low water potentials in maize. Planta 164, 540-549.
109. 3 plants. The EMBO Journal 16, 4806-4816.
110. Xu D., Duan X., Wang B., Hong B., Ho T.-H.D. & Wu R. (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiology 110, 249-257.
111. Yang W.J., Nadolska-Orczyk A., Wood K.V., Hahn D.T., Rich P.J., Wood A.J., Saneoka H., Premachandra G.S., Bonham C.C., Rhodes J.C., Joly R.J., Samaras Y., Goldsbrough P.B. & Rhodes D. (1995) Near-isogenic lines of maize differing for glycinebetaine. Plant Physiology 107, 621-630.
112. 2-resistant photosynthesis. Plant Physiology 98, 1330-1335.
113. 1-pyrroline-S-carboxylate synthetase, a bifunctional enzyme catalysing the first two steps of proline biosynthesis in plants. Journal of Biological Chemistry 270, 20491-20496.
114. 1-pyrroline-5-carbxylate synthetase gene promoter in transgenic Arabidopsis thaliana subjected to water stress. Plant Science 129, 81-89.