Evidence that differential gene expression between the halophyte, Thellungiella halophila, and Arabidopsis thaliana is responsible for higher levels of the compatible osmolyte proline and tight control of Na+ uptake in T. halophila

Plant, Cell and Environment

Volumn 29, Issue 7, 2006, Pages 1220-1234

  Kant, Surya ^a   Kant, Pragya ^a   Raveh, Eran ^b   Barak, Simon ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b VOLCANI CENTER   (Israel)

Author keywords

1 pyrroline 5 carboxylate synthetase; Proline dehydrogenase; Real time PCR; Salt overly sensitive 1; Salt stress

Indexed keywords

ANTHOCYANIN; MESSENGER RNA; PROLINE; PROLINE DEHYDROGENASE; SODIUM; SODIUM CHLORIDE; SODIUM PROTON EXCHANGE PROTEIN; SOS1 PROTEIN, ARABIDOPSIS;

ENZYME; GENE EXPRESSION; HALOPHYTE; SALT; XYLEM;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; BRASSICACEAE; COMPARATIVE STUDY; DRUG EFFECT; ENZYMOLOGY; GENE; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PLANT; PLANT GENE; PLANT ROOT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; XYLEM;

ANTHOCYANINS; ARABIDOPSIS; BRASSICACEAE; GENE DOSAGE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; PLANT ROOTS; PLANT SHOOTS; PROLINE; PROLINE OXIDASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SODIUM; SODIUM CHLORIDE; SODIUM-HYDROGEN ANTIPORTER; XYLEM;

ARABIDOPSIS; ARABIDOPSIS THALIANA; THELLUNGIELLA HALOPHILA;

EID: 33744961149     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2006.01502.x     Document Type: Article

References (63)

1. Apel K. Hirt H. 2004 Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annual Review of Plant Biology 55, 373 399.
2. Apse M.P. Aharon G.S. Snedden W.A. Blumwald E. 1999 Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiporter in Arabidopsis. Science 285, 1256 1258.
3. Asada K. 1997 The role of ascorbate peroxidase and monohydroascorbate reductase in H2O2 scavenging in plants. In Oxidative Stress and the Molecular Biology of Antioxidant Defenses (ed. J.G. Scandalios, pp. 353 373. Cold Spring Harbor Laboratory Press, New York, USA.
4. Bartley G.E. Scolnik P.A. 1995 Plant carotenoids: pigments for photoprotection, visual attraction and human health. Plant Cell 7, 1027 1038.
5. Bates L.S. Waldren R.P. Teare I.D. 1973 Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205 207.
6. Bradford M.M. 1976 A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Annals of Biochemistry 72, 248 254.
7. Bray E.A. Bailey-Serres J. Weretilnyk E. 2000 Responses to abiotic stresses. In Biochemistry and Molecular Biology of Plants (eds B.B. Buchanan W. Gruissem R.L. Jones, pp. 1158 1203. American Society of Plant Physiologists, Rockville, MD, USA.
8. Bressan R.A. Zhang C. Zhang H. Hasegawa P.M. Bohnert H.J. Zhu J.-K. 2001 Learning from the Arabidopsis experience. The next gene search paradigm. Plant Physiology 127, 1354 1360.
9. Burdon R.H. O'Kane D. Fadzilla N. Gill V. Boyd P.A. Finch R.R. 1996 Oxidative stress and responses in Arabidopsis thaliana and Oryza sativa subjected to chilling and salinity stress. Biochemical Society Transcriptions 24, 469 472.
10. Chalker-Scott L. 1999 Environmental significance of anthocyanins in plant stress responses. Photochemistry and Photobiology 70, 1 9.
11. Chaves M.M. Pereira J.S. Maroco J. Rodrigues M.L. Ricardo C.P.P. Osorio M.L. Carvalho I. Faria T. Pinheiro C. 2002 How plants cope with water stress in the field. Photosynthesis and growth. Annals of Botany 89, 907 916.
12. Chen W. Provart N.J. Glazebrook J., et al. 2002 Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14, 559 574.
13. Delauney A.J. Verma D.P.S. 1993 Proline biosynthesis and osmoregulation in plants. Plant Journal 4, 215 223.
14. Dixon R.A. Paiva N.L. 1995 Stress-induced phenylpropanoid metabolism. Plant Cell 7, 1085 1097.
15. Doebley J. Lukens L. 1998 Transcriptional regulators and the evolution of plant form. Plant Cell 10, 1075 1082.
16. Eimer M. 2004 Transgenic drought and salt tolerant plants. Genetic Engineering Newsletter, Special Issue 15, 1 14.
17. Gaxiola R. Li J. Undurraga S. Dang L.M. Allen G.J. Alper S.L. Fink G.R. 2001 Drought- and salt-tolerant plants result from overexpression of the AVP1 H+ pump. Proceedings of the National Academy of Sciences of the USA 99, 11444 11449.
18. Gibeaut D.M. Hulett J. Cramer G.R. Seemann J.R. 1997 Maximal biomass of Arabidopsis thaliana using a simple, low-maintenance hydroponic method and favorable environmental conditions. Plant Physiology 115, 317 319.
19. Gong Q. Li P. Ma S. Rupassara S.I. Bohnert H.J. 2005 Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant Journal 44, 826 839.
20. Hasegawa P.M. Bressan R.A. Zhu J.-K. Bonhert H.J. 2000 Plant cellular and molecular responses to high salinity. Annual Review of Plant Physiology and Plant Molecular Biology 51, 463 499.
21. Hoagland D.F. Arnon D.I. 1950 The water culture for growing plants without soil. Berkeley, California Agriculture Experimental Station Circular 347, 39.
22. Hong Z. Lakkineni K. Zhang Z. Verma D.P.S. 2000 Removal of feedback inhibition of 1-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiology 122, 1129 1136.
23. 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 Physiology 135, 1718 1737.
24. Kavi-Kishor P.B. Hong Z. Miao G.H. Hu C.-A.A. Verma D.P.S. 1995 Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology 108, 1387 1394.
25. Kavi-Kishor P.B. Sangam S. Amrutha R.N. Sri Laxmi P. Naidu K.R. Rao K.R.S.S. Rao S. Reddy K.J. Theriappan P. Sreenivasulu N. 2005 Regulation of proline biosynthesis, degradation, uptake and transport in higher plants: its implications in plant growth and abiotic stress tolerance. Current Science 88, 424 438.
26. 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. Plant Cell 8, 1323 1335.
27. Kreps J.A. Wu Y. Chang H.-S. Zhu T. Wang X. Harper J.F. 2002 Transcriptome changes for Arabidopsis in response to salt, osmotic and cold stress. Plant Physiology 130, 2129 2141.
28. Lawlor D. 1995 The effects of water deficit on photosynthesis. In Environment and Plant Metabolism (ed. N. Smirnoff, pp. 129 160. Bios Scientific Publishers, Oxford, UK.
29. Livak K.J. Schmittgen T.D. 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCΤ method. Methods 25, 402 408.
30. Lutts S. Majerus V. Kinet J.M. 1999 NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiologia Plantarum 105, 405 458.
31. 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.
32. Mani S. Van de Cotte B. Van Montagu M. Verbruggen N. 2002 Altered levels of proline dehydrogenase cause hypersensitivity to proline and its analogs in Arabidopsis. Plant Physiology 128, 73 83.
33. Munns R. 2002 Comparative physiology of salt and water stress. Plant, Cell and Environment 25, 239 250.
34. Murashige T. Skoog F. 1962 A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiologia Plantarum 15, 473 497.
35. Nakashima K. Satoh R. Kiyosue T. Yamaguchi-Shinozaki K. Shinozaki K. 1998 A gene encoding proline dehydrogenase is not only induced by proline and hypoosmolarity, but is also developmentally regulated in the reproductive organs of Arabidopsis. Plant Physiology 118, 1233 1241.
36. Nanjo T. Kobayashi M. Yoshiba Y. Kakubari Y. Yamaguchi-Shinozaki K. Shinozaki K. 1999 Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Letters 461, 205 210.
37. Nanjo T. Fujita M. Seki M. Kato M. Tabata S. Shinozaki K. 2003 Toxicity of free proline revealed in an Arabidopsis T-DNA-tagged mutant deficient in proline dehydrogenase. Plant Cell and Physiology 44, 541 548.
38. Neff M.M. Chory J. 1998 Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. Plant Physiology 118, 27 36.
39. Ort D.R. Oxborough K. Wise R.R. 1994 Depressions of photosynthesis in crops with water deficits. In Photoinhibition of Photosynthesis from Molecular Mechanisms to the Field (eds N.R. Baker J.R. Bowyer, pp. 315 329. Bios Scientific Publishers, Oxford, UK.
40. Peng Z. Lu Q. Verma D.P.S. 1996 Reciprocal regulation of Δ1-pyrroline-5-carboxylate synthetase and proline dehydrogenase genes controls proline levels during and after osmotic stress in plants. Molecular Genetics and Genomics 253, 334 341.
41. Perez-Alfocea F. Balibrea M.E. Alarcon J.J. Bolarin M.C. 2000 Composition of xylem and phloem exudates in relation to the salt tolerance of domestic and wild tomato species. Journal of Plant Physiology 156, 367 374.
42. Rajendrakumar C.S.V. Reddy B.V.D. Reddy A.R. 1994 Proline-protein interactions: protection of structural and functional integrity of M4 lactate dehydrogenase. Biochemistry and Biophysics Research Communications 201, 957 963.
43. Seki M. Narusaka M. Ishida J., et al. 2002 Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high salinity stresses using a full-length cDNA microarray. Plant Cell 31, 279 292.
44. Shi H. Ishitani M. Kim C. Zhu J.-K. 2000 The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proceedings of the National Academy of Sciences of the USA 97, 6896 6901.
45. Shi H. Quintero F.J. Pardo J.M. Zhu J.-K. 2002 The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14, 465 477.
46. Shi H. Lee B.H. Wu S.J. Zhu J.-K. 2003 Overexpression of a plasma membrane Na+/H+ antiporter gene improves salt tolerance in Arabidopsis thaliana. Nature Biotechnology 21, 81 85.
47. Shinozaki K. Shinozaki-Yamaguchi K. Seki M. 2003 Regulatory network of gene expression in the drought and cold stress responses. Current Opinion in Plant Biology 6, 410 417.
48. Smirnoff N. Cumbes Q.J. 1989 Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28, 1057 1060.
49. Strizhov N. Abraham E. Okresch 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. Plant Journal 12, 557 569.
50. Taji T. Seki M. Satou M. Sakurai T. Kobayashi M. Ishiyama K. Narusaka Y. Narusaka M. Zhu J.-K. Shinozaki K. 2004 Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiology 135, 1697 1709.
51. Tester M. Davenport R. 2003 Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 1 25.
52. Tsugane K. Kobayashi K. Niwa Y. Ohba Y. Wada K. Kobayashi H. 1999 A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11, 1195 1206.
53. Vera-Estrella R. Barkla B.J. Garcia-Ramirez L. Pantoja O. 2005 Salt stress in Thellungiella halophila activates Na+ transport mechanisms required for salinity tolerance. Plant Physiology 139, 1507 1517.
54. 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 of the USA 93, 8787 8791.
55. Volkov V. Wang B. Dominy P.J. Fricke W. Amtmann A. 2004 Thellungiella halophila, a salt-tolerant relative of Arabidopsis thaliana, possesses effective mechanisms to discriminate between potassium and sodium. Plant, Cell and Environment 27, 1 14.
56. Wang Z.-L. Li P.-H. Fredricksen M., et al. 2004 Expressed sequence tags from Thellungiella halophila, a new model to study plant salt-tolerance. Plant Science 166, 609 616.
57. Ward J.M. Hirschi K.D. Sze H. 2003 Plants pass the salt. Trends in Plant Science 8, 200 201.
58. Wessler S. Bureau T. White S. 1995 LTR-retrotransposons and MITEs: important players in the evolution of plant genomes. Current Opinion in Genetics and Development 5, 814 821.
59. Wong C.E. Li Y. Whitty B.R. Dýaz-Camino C. Akhter S.R. Brandle J.E. Golding G.B. Weretilnyk E.A. Moffatt B.A. Griffith M. 2005 Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Molecular Biology 58, 561 574.
60. Xiong L. Zhu J.-K. 2002a Salt tolerance. In The Arabidopsis Book (eds C.R. Somerville E.M. Meyerowitz. American Society of Plant Biologists, Rockville, MD, USA. doi: 10.1199/tab.0048, URL http://www.aspb.org/publications/ arabidopsis/ [accessed on 5 April 2005]
61. Xiong L. Zhu J.-K. 2002b Molecular and genetic aspects of plant responses to osmotic stress. Plant, Cell and Environment 25, 131 139.
62. Zhu J.-K. 2000 Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiology 124, 941 948.
63. Zhu J.-K. 2001 Plant salt tolerance. Trends in Plant Science 6, 66 72.