Comparative metabolome analysis of the salt response in breeding cultivars of rice

Advances in Molecular Breeding Toward Drought and Salt Tolerant Crops

Volumn , Issue , 2007, Pages 285-315

  Zuther, Ellen ^a   Koehl, Karin ^a   Kopka, Joachim ^a  

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

Author keywords

GC TOF MS; metabolite profiling; Metabolome; rice; salinity

Indexed keywords

EID: 38149137783     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-4020-5578-2_12     Document Type: Chapter

References (123)

1. Abbasi FM, Komatsu S (2004) A proteomic approach to analyze salt-responsive proteins in rice leaf sheath. Proteomics 4:2072-2081.
2. Alpaslan M, Gunes A, Taban S (1999) Salinity resistance of certain rice (Oryza sativa L.) cultivars. Turkish J Biol 23:499-506.
3. Anoop N, Gupta AK (2003) Transgenic indica rice cv IR-50 over-expressing Vigna aconitifolia DELTA-1-pyrroline-5-carboxylate synthetase cDNA shows tolerance to high salt. J Plant Biochem Biotechnol 12:109-116.
4. Babu CR, Vijayalakshmi C, Mohandass S (2005) Evaluation of rice (Oryza sativa L.) genotypes for salt tolerance. J Food Agricult Environ 3:190-194.
5. Basu R, Maitra N, Ghosh B (1988) Salinity results in polyamine accumulation in early rice Oryza sativa L. seedlings. Austral J Plant Physiol 15:777-786.
6. Bino RJ, Hall RD, Fiehn O, Kopka J, Saito K, Draper J, Nikolau BJ, Mendes P, Roessner-Tunali U, Beale MH, Trethewey RN, Lange BM, Wurtele ES, Sumner LW (2004) Potential of metabolomics as a functional genomics tool. Trends Plant Sci 9:418-425.
7. Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099-1111.
8. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: Recent development. Plant Sci 140:103-125.
9. Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909-9914.
10. Carrari F, Schauer N, Willmitzer L, Fernie AR (2006) Systems biology: a renaissance of the top-down approach. In: Nagata T, Lörz H, Widholm JM (eds) Biotechnology in agriculture and forestry Vol 57: Saito K, Dixon RA, Willmitzer L (eds) Plant metabolomics. Springer-Verlag, Berlin Heidelberg New York, pp 185-198.
11. Chao DY, Luo YH, Shi M, Luo D, Lin HX (2005) Salt-responsive genes in rice revealed by cDNA microarray analysis. Cell Res 15:796-810.
12. Chattopadhyay MK, Gupta S, Sengupta DN, Ghosh B (1997) Expression of arginine decarboxylase in seedlings of indica rice (Oryza sativa L.) cultivars as affected by salinity stress. Plant Mol Biol 34:477-483.
13. Chattopadhyay MK, Ghosh B (1998) Molecular analysis of polyamine biosynthesis in higher plants. Current Sci 74:517-522.
14. Colebatch G, Desbrosses G, Ott T, Krusell L, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39:487-512.
15. Cook D, Fowler S, Fiehn O, Thomashow MF (2004) A prominent role for the CBF cold response pathway in configuring the low-temperature metabolome of Arabidopsis. Proc Natl Acad Sci USA 101:15243-15248.
16. Denby K, Gehring C (2005) Engineering drought and salinity tolerance in plants: lessons from genome-wide expression profiling in Arabidopsis. Trends Biotech 23:547-552.
17. Dubey RS, Rani M (1989) Salinity induced accumulation of free amino acids in germinating rice seeds differing in salt tolerance. J Agronomy Crop Sci 163:236-247.
18. Erban A, Schauer N, Fernie AR, Kopka J (2007) Non-supervised construction and application of mass spectral and retention time index libraries from time-of-flight GC-MS metabolite profiles. In: Weckwerth W (ed) Metabolomics: methods and protocols. Humana Press, Totowa, pp 19-38.
19. Fan TWM, Lane AN, Higashi RA (2003) In vivo and in vitro metabolomic analysis of anaerobic rice coleoptiles revealed unexpected pathways. Russian J Plant Physiol 50:787-793.
20. Fernie AR, Trethewey RN, Krotzky AJ, Willmitzer L (2004) Metabolite profiling: from diagnostics to systems biology. Nat Rev Mol Cell Biol 5:763-769.
21. Fiehn O (2002) Metabolomics-The link between genotypes and phenotypes. Plant Mol Biol 48:155-171.
22. Fiehn O, Kopka J, Dörmann P, Altmann T, Trethewey RN, Willmitzer L (2000) Metabolite profiling for plant functional genomics. Nat Biotechnol 18:1157-1161.
23. Fischer RA, Maurer R (1978) Drought resistance in spring wheat cultivars. 1. Grain-yield responses. Australian J Agricultural Res 29:897-912.
24. Frenzel T, Miller A, Engel KH (2002) Metabolite profiling-A fractionation method for analysis of major and minor compounds in rice grains. Cereal Chem 79:215-221.
25. Garcia AB, Engler JD, Iyer S, Gerats T, VanMontagu M, Caplan AB (1997) Effects of osmoprotectants upon NaCl stress in rice. Plant Physiol 115:159-169.
26. Garg AK, Kim JK, Owens TG, Ranwala AP, Choi YD, Kochian LV, Wu RJ (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898-15903.
27. Gregorio GB, Senadhira D, Mendoza RD, Manigbas NL, Roxas JP, Guerta CQ (2002) Progress in breeding for salinity tolerance and associated abiotic stresses in rice. Field Crops Res 76:91-101.
28. Gullberg J, Jonsson P, Nordström A, Sjöström M, Moritz T (2004) Design of experiments: an efficient strategy to identify factors influencing extraction and derivatization of Arabidopsis thaliana samples in metabolomic studies with gas chromatography/mass spectrometry. Anal Biochem 331:283-295.
29. Halket JM, Przyborowska AM, Stein SE, Mallard WG, Down S, Chalmers RA (1999) Deconvolution gas chromatography mass spectrometry of urinary organic acids-potential for pattern recognition and automated identification of metabolic disorders. Rapid Commun Mass Spectrom 13:279-284.
30. Halket JM, Waterman D, Przyborowska AM, Patel RKP, Fraser PD, Bramley PM (2005) Chemical derivatization and mass spectral libraries in metabolic profling by GC/MS and LC/MS/MS. J Exp Bot 56:219-243.
31. Hien DT, Jacobs M, Angenon G, Hermans C, Thu TT, Van Son L, Roosens NH (2003) Proline accumulation and DELTA-1-pyrroline-5-carboxylate synthetase gene properties in three rice cultivars differing in salinity and drought tolerance. Plant Sci 165:1059-1068.
32. Ienaga K, Nakamura K, Kurohashi M, Nakanishi T, Ichii T (1990) Simple peptides. 5-Hydroxyproline-containing diketopiperazines inducing drought resistance in rice. Phytochem 29:35-39.
33. Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K, Wada K, Shinozaki K (1997) Characterization of the gene for DELTA-1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33:857-865.
34. Ishitani M, Arakawa K, Mizuno K, Kishitani S, Takabe T (1993) Betaine aldehyde dehydrogenase in the Gramineae: levels in leaves of both betaine-accumulating and nonaccumulating cereal plants. Plant Cell Physiol 34:493-495.
35. Jacob ST, Stetler DA (1989) Polyamines and RNA synthesis. In: Bachrach U, Heimer QM (eds.) The physiology of polyamines Vol. 1. CRC Press, Boca Raton, FL, pp 133-140.
36. Jain RK, Saini N, Jain S, Singh R (2003) Molecular strategies for developing salt tolerant crops. Indian J Biotechnol 2:121-137.
37. Jang IC, Oh SJ, Seo JS, Choi WB, Song SI, Kim CH, Kim YS, Seo HS, Choi YD, Nahm BH (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516-524.
38. Jenkins H, Hardy N, Beckmann M, Draper J, Smith AR, Taylor J, Fiehn O, Goodacre R, Bino RJ, Hall RD, Kopka J, Lane GA, Lange BM, Liu JR, Mendes P, Nikolau BJ, Oliver SG, Paton NW, Rhee S, Roessner-Tunali U, Saito K, Smedsgaard J, Sumner LW, Wang T, Walsh S, Wurtele ES, Kell DB (2004) A proposed framework for the description of plant metabolomics experiments and their results. Nature Biotechnol 22:1601-1606.
39. Jonsson P, Gullberg J, Nordström A, Kusano M, Kowalczyk M, Sjöström M, Moritz T (2004) A strategy for identifying differences in large series of metabolomic samples analyzed by GC/MS. Anal Chem 76:1738-1745
40. Jonsson P, Johansson AI, Gullberg J, Trygg J, Jiye A, Grung B, Marklund S, Sjöström M, Antti H, Moritz T (2005) High-throughput data analysis for detecting and identifying differences between samples in GC/MS-based metabolomic analyses. Anal Chem 77:5635-5642.
41. Kafi M, Stewart WS, Borland AM (2003) Carbohydrate and proline contents in leaves, roots, and apices of salt-tolerant and salt-sensitive wheat cultivars. Russian J Plant Physiol 50:155-162.
42. Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159-4168.
43. Kakkar RK, Bhaduri S, Rai VK, Kumar S (2000) Amelioration of NaCl stress by arginine in rice seedlings: Changes in endogenous polyamines. Biol Plantarum 43:419-422.
44. Katiyar S, Dubey RS (1990) Changes in polyamines titer in rice seedlings following sodium chloride salinity stress. J Agron Crop Sci 165:19-27.
45. Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kawai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889-905.
46. Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482-487.
47. Kim D-W, Rakwal R, Agrawal GK, Jung Y-H, Shibato J, Jwa N-S, Iwahashi Y, Iwahasi H, Kim DH, Shim I-S, Usui K (2005) A hydroponic rice seedling culture model system for investigating proteome of salt stress in rice leaf. Electrophoresis 26:4521-4539.
48. Kinzel H (1982) Pflanzenökologie und Mineralstoffwechsel. Ulmer, Stuttgart.
49. Kishitani S, Takanami T, Suzuki M, Oikawa M, Yokoi S, Ishitani M, Alvarez-Nakase AM, Takabe T (2000) Compatibility of glycinebetaine in rice plants: evaluation using transgenic rice plants with a gene for peroxisomal betaine aldehyde dehydrogenase from barley. Plant Cell Environ 23:107-114.
50. Kopka J (2006a) Current challenges and developments in GC-MS based metabolite profiling technology. J Biotechnol 124:312-322.
51. Kopka J (2006b) Gas chromatography mass spectrometry. In: Nagata T, Lörz H, Widholm JM (eds) Biotechnology in agriculture and forestry Vol 57: Saito K, Dixon RA, Willmitzer L (eds) Plant metabolomics. Springer-Verlag, Berlin Heidelberg New York, pp 3-20.
52. Kopka J, Fernie AF, Weckwerth W, Gibon Y, Stitt M (2004) Metabolite profiling in plant biology: platforms and destinations. Genome Biol 5:109-117.
53. Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmüller E, Dörmann P, Gibon Y, Stitt M, Willmitzer L, Fernie AR, Steinhauser D (2005) GMD@CSBDB: The Golm metabolome database. Bioinformatics 21:1635-1638.
54. Koyama ML, Levesley A, Koebner RMD, Flowers TJ, Yeo AR (2001) Quantitative trait loci for component physiological traits determining salt tolerance in rice. Plant Physiol 125:406-422.
55. Krishnamurthy R, Anbazhagan M, Bhagwat KA (1988) Evaluation of quaternary ammonium compounds as index of salt tolerance using rice cultivars. Indian J Experiment Biol 26:137-139.
56. Krishnamurthy R, Bhagwat KA (1989) Polyamines as modulators of salt tolerance in rice cultivars. Plant Physiol 91:500-504.
57. Lefevre I, Gratia E, Lutts S (2001) Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci 161:943-952.
58. Li YG, Zhang F, Wang ZT, Hu ZB (2004) Identification and chemical profiling of monacolins in red yeast rice using high-performance liquid chromatography with photodiode array detector and mass spectrometry. J Pharmaceut Biomed Anal 35:1101-1112.
59. Li ZY, Chen SY (2000) Differential accumulation of the S-adenosylmethionine decarboxylase transcript in rice seedlings in response to salt and drought stresses. Theoret Appl Genet 100:782-788.
60. + uptake of the shoots and roots controlling rice salt tolerance. Theoret Appl Genet 108:253-260.
61. Lopez-Bucio J, Nieto-Jacobo MF, Ramirez-Rodriguez V, Herrera-Estrella L (2000) Organic acid metabolism in plants: from adaptive physiology to transgenic varieties for cultivation in extreme soils. Plant Sci 160:1-13.
62. Lutts S, Majerus V, Kinet JM (1999) NaCl effects on proline metabolism in rice (Oryza sativa) seedlings. Physiol Plantarum 105:450-458.
63. Maiale S, Sanchez DH, Guirado A, Vidal A, Ruiz OA (2004) Spermine accumulation under salt stress. J Plant Physiol 161:35-42.
64. Majee M, Maitra S, Dastidar KG, Pattnaik S, Chatterjee A, Hait NC, Das KP, Majumder AL (2004) A novel salt-tolerant L-myo-inositol-1-phosphate synthase from Porteresia coarctata (Roxb.) Tateoka, a halophytic wild rice-Molecular cloning, bacterial overexpression, characterization, and functional introgression into tobacco-conferring salt tolerance phenotype. J Biol Chem 279:28539-28552.
65. Martin-Tanguy J (1997) Conjugated polyamines and reproductive development: Biochemical, molecular and physiological approaches. Physiol Plantarum 100:675-688.
66. Mohanty A, Kathuria H, Ferjani A, Sakamoto A, Mohanty P, Murata N, Tyagi AK (2002) Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress. Theoret Appl Genet 106:51-57.
67. Morino K, Matsuda F, Miyazawa H, Sukegawa A, Miyagawa H, Wakasa K (2005) Metabolic profiling of tryptophan-overproducing rice calli that express a feedback-insensitive alpha subunit of anthranilate synthase. Plant Cell Physiol 46:514-521.
68. Nakamura T, Yokota S, Muramoto Y, Tsutsui K, Oguri Y, Fukui K, Takabe T (1997) Expression of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine nonaccumulator, and possible localization of its protein in peroxisomes. Plant J Cell Mol Biol 11:1115-1120.
69. Oksman-Caldentey K-M, Saito K (2005) Integrating genomics and metabolomics for engineering plant metabolic pathways. Curr Opin Biotech 16:174-179.
70. Parker R, Flowers TJ, Moore AL, Harpham NVJ (2006) An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 57:1109-1118.
71. Penna S (2003) Building stress tolerance through over-producing trehalose in transgenic plants. Trends Plant Sci 8:355-357.
72. Ponnameruma F (1984) Role of cultivar tolerance in increasing rice production on saline lands. In: Staples R, Toenniessen G (eds) Salinity tolerance in plants-strategies for crop improvement. Wiley, New York, pp 255-271.
73. Prakash L, Prathapasenan G (1988) Effect of NaCl salinity and putrescine on shoot growth, tissue ion concentration and yield of rice (Oryza sativa). J Agron Crop Sci 160:325-334.
74. Rabbani MA, Maryuama K, Abe H, Khan A, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755-1767.
75. Ratcliffe RG, Shachar-Hill Y (2006) Measuring multiple fluxes through plant metabolic networks. Plant J 45:490-511.
76. Rathert G (1983) Carbohydrate status in response to ion regulation of two rice varieties (Oryza sativa) grown in saline medium. J Plant Nutrit 6:817-830.
77. Rathinasabapathi B, Gage DA, Mackill DJ, Hanson AD (1993) Cultivated and wild rices do not accumulate glycinebetaine due to deficiencies in two biosynthetic steps. Crop Sci 33:534-538.
78. Ritambhara GK, Dubey RS (1995) Influence of NaCl salinity on the behaviours of malate, isocitrate and glucose 6-phosphate dehydrogenases in growing rice seedlings in relation to salt tolerance. Indian J Plant Physiol 38:48-53.
79. Roessner U, Luedemann A, Brust D, Fiehn O, Linke T, Willmitzer L, Fernie AR (2001a) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13:11-29.
80. Roessner U, Wagner C, Kopka J, Trethewey RN, Willmitzer L (2000) Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J 23:131-142.
81. Roessner U, Willmitzer L, Fernie AR (2001b) High-resolution metabolic phenotyping of genetically and environmentally diverse plant systems-identification of phenocopies. Plant Physiol 127:749-764.
82. Roessner U, Willmitzer L, Fernie AR (2002) Metabolic profiling and biochemical phenotyping of plant systems. Plant Cell Rep 21:189-196
83. Roessner-Tunali U, Hegemann B, Lytovchenko A, Carrari F, Bruedigam C, Granot D, Fernie AR (2003) Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol 133:84-99.
84. 13C labelled isotopes. Plant J 39:668-679.
85. Roy M, Wu R (2001) Arginine decarboxylase transgene expression and analysis of environmental stress tolerance in transgenic rice. Plant Sci 160:869-875.
86. Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987-992.
87. Ryan PR, Delhaize E, Jones DL (2001) Function and mechanism of organic anion exudation from plant roots. Annu Rev Plant Phys Plant Mol Biol 52:527-560.
88. Sahi C, Agarwal M, Reddy MK, Sopory SK, Grover A (2003) Isolation and expression analysis of salt stress-associated ESTs from contrasting rice cultivars using a PCR-based subtraction method. Theor Appl Genet 106:620-628.
89. Salekdeh GH, Siopongco J, Wade LJ, Ghareyazie B, Bennett J (2002) A proteomic approach to analyzing drought-and salt-responsiveness in rice. Field Crops Res 76:199-219.
90. Sato S, Soga T, Nishioka T, Tomita M (2004) Simultaneous determination of the main metabolites in rice leaves using capillary electrophoresis mass spectrometry and capillary electrophoresis diode array detection. Plant J 40:151-163.
91. Sauer U (2004) High-throughput phenomics: experimental methods for mapping fluxomes. Curr Opin Biotechnol 15:58-63.
92. Schauer N, Semel Y, Roessner U, Gur A, Balbo I, Carrari F, Pleban T, Perez-Melis A, Bruedigam C, Kopka J, Willmitzer L, Zamir D, Fernie AR (2006) Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotech 24:447-454.
93. Schauer N, Steinhauser D, Strelkov S, Schomburg D, Allison G, Moritz T, Lundgren K, Roessner-Tunali U, Forbes MG, Willmitzer L, Fernie AR, Kopka J (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Lett 579:1332-1337.
94. Scholz M, Gatzek S, Sterling A, Fiehn O, Selbig J (2004) Metabolite fingerprinting: detecting biological features by independent component analysis. Bioinformatics 20:2447-2454.
95. Scholz M, Kaplan F, Guy CL, Kopka J, Selbig J (2005) Non-linear PCA: a missing data approach. Bioinformatics 21:3887-3895.
96. Shiozaki N, Yamada EM, Yoshiba EY (2005) Analysis of salt-stress- inducible ESTs isolated by PCR-subtraction in salt-tolerant rice. Theor Appl Genet 110:1177-1186.
97. Slocum RD, Kaur-Sawhney R, Galston AW (1984) The physiology and biochemistry of polyamines in plants. Arch Biochem Biophys 235:283-303.
98. Sohn YG, Lee BH, Kang KY, Lee JJ (2005) Effects of NaCl stress on germination, antioxidant responses, and proline content in two rice cultivars. J Plant Biol 48:201-208.
99. Steinhauser D and Kopka J (2007) Methods, applications and concepts of metabolite profiling: primary metabolism. In: Fernie AR, Baginsky S (eds) Plant systems biology. Birkhäuser, in press
100. Stone JV (2002) Independent component analysis: an introduction. Trends Cognitive Sci 6:59-64.
101. Sumner LW, Mendes P, Dixon RA (2003) Plant metabolomics: large-scale phytochemistry in the functional genomics era. Phytochem 62:817-836.
102. Takabe T, Nakamura T, Nomura M, Hayashi Y, Ishitani M, Muramoto Y, Tanaka A (1998) Glycine-betaine and the genetic engineering of salinity tolerance in plants. In: Stress responses of photosyn-thetic organisms: molecular mechanisms and molecular regulations. Amsterdam, New York, Elsevier, pp 115-131.
103. Trethewey RN (2004) Metabolite profiling as an aid to metabolic engineering in plants. Curr Opin Plant Biol 7:196-201.
104. Trethewey RN, Krotzky AJ, Willmitzer L (1999) Metabolic profiling: a Rosetta stone for genomics? Curr Opin Plant Biol 2:83-85.
105. Trygg J, Gullberg J, Johansson AI, Jonsson P, Moritz T (2006) Chemometrics in metabolomics-an introduction. In: Nagata T, Lörz H, Widholm JM (eds) Biotechnology in agriculture and forestry Vol 57: Saito K, Dixon RA, Willmitzer L (eds) Plant metabolomics. Springer-Verlag, Berlin Heidelberg New York, pp 117-128.
106. Ueda A, Kathiresan A, Bennet J, Takabe T (2006) Comparative transcriptome analysis of barley and rice under salt stress. Theor Appl Genet 112:1286-1294.
107. Urbanczyk-Wochniak E, Luedemann A, Kopka J, Selbig J, Roessner-Tunali U, Willmitzer L, Fernie AR (2003) Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. EMBO Reports 4:989-993.
108. Vance CP, Uhde-Stone C, Allan DL (2003) Phosphorus acquisition and use: critical adaptations by plants for securing a non renewable resource. New Phytologist 157:423-447.
109. Wagner C, Sefkow M, Kopka J (2003) Construction and application of a mass spectral and retention time index database generated from plant GC/EI-TOF-MS metabolite profiles. Phytochem 62:887-900.
110. Walia H, Wilson C, Condamine P, Liu X, Ismail AM, Zeng L, Wanamaker SI, Mandal J, Xu J, Cui X, Close TJ (2005) Comparative transcriptional profiling of two contrasting rice genotypes under salinity stress during the vegetative growth stage. Plant Physiol 139:822-835.
111. Weckwerth W, Wenzel K, Fiehn O (2004) Process for the integrated extraction, identification and quantification of metabolites, proteins and RNA to reveal their co-regulation in biochemical networks. Proteomics 4:78-83.
112. Wu Y, Wang Q, Ma Y, Chu C (2005) Isolation and expression analysis of salt up-regulated ESTs in upland rice using PCR-based subtractive suppression hybridization method. Plant Sci 168:847-853.
113. Yakubov BA, Chkanikov DI (1994) Use of polyol quantitative analysis for the estimation of rice varieties resistance to pyriculariosis. Mikologiya i Fitopatologiya 28:65-69.
114. Yamamoto A, Shim IS, Fujihara S, Yoneyama T, Usui K (2004) Effect of difference in nitrogen media on salt-stress response and contents of nitrogen compounds in rice seedlings. Soil Sci Plant Nutrit 50:85-93.
115. Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235-244.
116. Yang X, Romheld V, Marschner H (1994) Effect of bicarbonate on root-growth and accumulation of organic-acids in Zn-inefficient and Zn-efficient rice cultivars (Oryza sativa L). Plant Soil 164:1-7.
117. Yeo AR, Flowers TJ (1982) Accumulation and localization of sodium ions within the shoots of rice Oryza sativa varieties differing in salinity resistance. Physiol Plantarum 56:343-348.
118. Yeo AR, Flowers TJ (1983) Varietal differences in the toxicity of sodium ions in rice Oryza sativa leaves. Physiol Plantarum 59:189-195.
119. Yeo AR, Yeo ME, Flowers SA, Flowers TJ (1990) Screening of rice (Oryza sativa L.) genotypes for physiological characters contributing to salinity resistance, and their relationship to overall performance. Theoret Appl Genet 79:377-384.
120. Young ND, Galston A.W. (1984) Physiological control of arginine decarboxylase activity in K-deficient oat shoots. Plant Physiol 76:331-335.
121. Zhou W, Sun QJ, Zhang CF, Yuan YZ, Ji Z, Lu BB (2004) Effect of salt stress on ammonium assimilation enzymes of the roots of rice (Oryza sativa) cultivars differing in salinity resistance. Acta Botanica Sinica 46:921-927.
122. Zhu BC, Su J, Chang M, Verma DPS, Fan YL, Wu R (1998) Overexpression of a delta(1)-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water-and salt-stress in transgenic rice. Plant Sci 139:41-48.
123. Zhu GY, Kinet JM, Lutts S (2001) Characterization of rice (Oryza sativa L.) F3 populations selected for salt resistance. I. Physiological behaviour during vegetative growth. Euphytica: Netherlands J Plant Breeding 121:251-263.