Combined use of δ 13C, δ 18O and δ 15N tracks nitrogen metabolism and genotypic adaptation of durum wheat to salinity and water deficit

New Phytologist

Volumn 194, Issue 1, 2012, Pages 230-244

  Yousfi, Salima ^a   Serret, Maria Dolores ^a   Márquez, Antonio José ^b   Voltas, Jordi ^c   Araus, José Luis ^a,d  

^a UNIVERSITY OF BARCELONA   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

^c UNIVERSITY OF LLEIDA   (Spain)

^d INTERNATIONAL MAIZE AND WHEAT IMPROVEMENT CENTER CIMMYT   (Mexico)

Author keywords

13C; 15N; 18O; Durum wheat (Triticum turgidum ssp. durum); Glutamine synthetase; Nitrate reductase; Salinity; Water deficit

Indexed keywords

ADAPTATION; CARBON ISOTOPE; CONCENTRATION (COMPOSITION); DROUGHT RESISTANCE; ECOLOGICAL MODELING; ENZYME ACTIVITY; GAS EXCHANGE; GENOTYPE; IRRIGATION; METABOLISM; NITROGEN ISOTOPE; OXYGEN ISOTOPE; PHENOTYPE; PHYSIOLOGICAL RESPONSE; REPRODUCTIVE BEHAVIOR; SALINITY; TOLERANCE; WHEAT;

TRITICUM TURGIDUM; TRITICUM TURGIDUM SUBSP. DURUM;

CARBON; GLUTAMATE AMMONIA LIGASE; ION; NITRATE REDUCTASE; NITROGEN; OXYGEN; WATER;

ADAPTATION; ARTICLE; BIOMASS; CLUSTER ANALYSIS; DROUGHT; ENZYMOLOGY; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PHOTOSYNTHESIS; PHYSIOLOGY; PLANT; QUANTITATIVE TRAIT; SALINITY; STATISTICAL MODEL; WHEAT;

ADAPTATION, PHYSIOLOGICAL; BIOMASS; CARBON ISOTOPES; CLUSTER ANALYSIS; DROUGHTS; GENOTYPE; GLUTAMATE-AMMONIA LIGASE; IONS; LINEAR MODELS; NITRATE REDUCTASE; NITROGEN; NITROGEN ISOTOPES; OXYGEN ISOTOPES; PHOTOSYNTHESIS; PLANT SHOOTS; QUANTITATIVE TRAIT, HERITABLE; SALINITY; TRITICUM; WATER;

EID: 84857457964     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.04036.x     Document Type: Article

References (92)

1. Abd-El Baki GK, Siefritz F, Man HM, Weiner H, Kaldenhoff R, Kaiser WM. 2000. Nitrate reductase in Zea mays L. under salinity. Plant, Cell & Environment 23: 515-521.
2. Araus JL. 2004. The problem of sustainable water use in the Mediterranean and research requirements for agriculture. Annals of Applied Biology 144: 259-272.
3. Araus JL, Sánchez C, Cabrera-Bosquet L. 2010. Is heterosis in maize mediated through better water use? New Phytologist 187: 392-406.
4. 3 cereals: what should we breed for? Annals of Botany 89: 925-940.
5. Araus JL, Slafer GA, Royo C, Serret MD. 2008. Breeding for yield potential and stress adaptation in cereals. Critical Reviews in Plant Science 27: 377-412.
6. Araus JL, Villegas D, Aparicio N, del Moral LFG, El Hani S, Rharrabti Y, Ferrio JP, Royo C. 2003. Environmental factors determining carbon isotope discrimination and yield in durum wheat under Mediterranean conditions. Crop Science 43: 170-180.
7. Arbuckle JL. 1997. Amos Users' Guide; v. 3.6. Chicago, IL: Small Waters Corporation.
8. Ayers RS, Westcott DW. 1989. Water quality for agriculture. FAO irrigation and drainage paper 29. Rome, Italy: FAO.
9. Barbour MM. 2007. Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology 34: 83-94.
10. Barbour MM, Farquhar GD. 2000. Relative humidity- and ABA-induced variation in carbon and oxygen isotope ratios of cotton leaves. Plant, Cell & Environment 23: 473-485.
11. Barbour MM, Fischer RA, Sayre KD, Farquhar GD. 2000. Oxygen isotope ratio of leaf and grain material correlates with stomatal conductance and grain yield in irrigated wheat. Australian Journal of Plant Physiology 27: 625-637.
12. Bernard SM, Habash DZ. 2009. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytologist 182: 608-620.
13. Blum A. 2005. Drought resistance, water-use efficiency, and yield potential - are they compatible, dissonant, or mutually exclusive? Australian Journal of Agricultural Research 56: 1159-1168.
14. Blum A. 2009. Effective use of water (EUW) and not water-use efficiency (WUE) is the target of crop yield improvement under drought stress. Field Crops Research 112: 119-123.
15. + ratio and salinity. Journal of Plant Physiology 142: 531-536.
16. Botella MA, Martínez V, Nieves M, Cerdá A. 1997. Effect of salinity on the growth and nitrogen uptake by wheat seedlings. Journal of Plant Nutrition 20: 793-804.
17. Brugière N, Dubois F, Limami AM, Lelandais M, Roux Y, Sangwan RS, Hirel B. 1999. Glutamine synthetase in the phloem plays a major role in controlling proline production. Plant Cell 11: 1995-2011.
18. 18O response to water and nitrogen availability and its relationship with yield in field-grown durum wheat. Plant, Cell & Environment 34: 418-433.
19. 18O to gas exchange and growth in durum wheat. Journal of Experimental Botany 60: 1633-1644.
20. 18O) reflects yield potential and drought resistance in maize. Plant, Cell & Environment 32: 1487-1499.
21. Carillo P, Mastrolonardo G, Nacca F, Fuggi A. 2005. Nitrate reductase in durum wheat seedlings as affected by nitrate nutrition and salinity. Functional Plant Biology 32: 209-219.
22. Carillo P, Mastrolonardo G, Nacca F, Parisi D, Verlotta A, Fuggi A. 2008. Nitrogen metabolism in durum wheat under salinity: accumulation of proline and glycine betaine. Functional Plant Biology 35: 412-426.
23. 18O) responses of three tropical tree species to water and nutrient availability. Plant, Cell & Environment 32: 1441-1455.
24. 15N Correlates with the Transpiration Efficiency of Nitrogen Acquisition in Tropical Trees. Plant Physiology 151: 1667-1676.
25. Chen GX, Fu XP, Lips SH, Sagi M. 2003. Control of plant growth resides in the shoot, and not in the root, in reciprocal grafts of flacca and wild-type tomato (Lysopersicon esculentum), in the presence and absence of salinity stress. Plant and Soil 256: 205-215.
26. Condon AG, Richards RA, Rebetzke GT, Farquhar GD. 2002. Improving intrinsic water use efficiency and crop yield. Crop Science 42: 128-133.
27. Coplen TB. 2008. Explanatory glossary of terms used in expression of relative isotope ratios and gas ratios. IUPAC Provisional Recommendations. Inorganic Chemistry Division. Commission on Isotopic Abundances and Atomic Weights.
28. Correia MJ, Fonseca F, Azedo-Silva J, Dias C, David MM, Barrote I, Osorio ML, Osorio J. 2005. Effects of water deficit on the activity of nitrate reductase and content of sugars, nitrate and free amino acids in the leaves and roots of sunflower and white lupin plants growing under two nutrient supply regimes. Physiologia Plantarum 124: 61-70.
29. Cuin TA, Tian Y, Betts SA, Chalmandrier R, Shabala S. 2009. Ionic relations and osmotic adjustment in durum and bread wheat under saline conditions. Functional Plant Biology 36: 1110-1119.
30. Diaz P, Betti M, Sanchez DH, Udvardi MK, Monza J, Márquez AJ. 2010. Deficiency in plastidic glutamine synthetase alters proline metabolism and transcriptomic response in Lotus japonicus under drought stress. New Phytologist 188: 1001-1013.
31. Ellis RP, Forster BP, Gordon DC, Handley LL, Keith RP, Lawrence P, Meyer R, Powell W, Robinson D, Scrimgeour CM et al. 2002. Phenotype/genotype associations for yield and salt tolerance in a barley mapping population segregating for two dwarfing genes. Journal of Experimental Botany 53: 1163-1176.
32. Evans RD. 2001. Physiological mechanism influencing plant nitrogen isotope composition. Trends in Plant Science 6: 121-126.
33. Evans RD, Bloom AJ, Sukrapanna SS, Ehleringer JR. 1996. Nitrogen isotope composition of tomato (Lycopersicon esculentum, Mill cv. T5) grown under ammonium or nitrate nutrition. Plant, Cell & Environment 19: 1317-1323.
34. Farquhar GD, Cernusak LA, Barnes B. 2007. Heavy water fractionation during transpiration. Plant Physiology 143: 11-18.
35. Farquhar GD, Firth PM, Wetselaar R, Weir B. 1980. On the gaseous exchange of ammonia between leaves and the environment: measurements of the ammonia compensation point. Plant Physiology 66: 710-714.
36. Farquhar GD, O'Leary MH, Berry JA. 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Australian Journal of Plant Physiology 9: 121-137.
37. Farquhar GD, Richards RA. 1984. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Australian Journal of Plant Physiology 11: 539-552.
38. 18O with wheat phenology and yield under water-limited conditions. Annals of Applied Biology 150: 207-215.
39. Foyer CH, Valadier MH, Migge A, Becker TW. 1998. Drought induced effects on nitrate reductase activity and mRNA and on the coordination of nitrogen and carbon metabolism in maize leaves. Plant Physiology 117: 283-292.
40. 15N correlates with genotype and salt stress in barley. Planta 201: 100-102.
41. Hirel B, Le Gouis J, Ney B, Gallais A. 2007. The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. Journal of Experimental Botany 58: 2369-2387.
42. Hoagland DR, Arnon DI. 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347: 1-32.
43. Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T. 2000. Enhanced tolerance to salt stress in transgenic rice that overexpress chloroplast glutamine synthetase. Plant Molecular Biology 43: 103-111.
44. Hsiao TC. 1973. Plant response to water stress. Annual Review of Plant Physiology 24: 519-570.
45. Hu Y, Schmidhalter U. 2005. Drought and salinity: a comparison of their effects on mineral nutrition of plants. Journal of Plant Nutrition and Soil Science 168: 541-549.
46. Isla R, Aragues R, Royo A. 1998. Validity of various physiological traits as screening criteria for salt tolerance in barley. Field Crops Research 58: 97-107.
47. - in salt-affected barley and durum wheat. Plant, Cell & Environment 29: 2185-2197.
48. James RA, Von Caemmerer S, Condon AG, Zwart AB, Munns R. 2008. Genetic variation in tolerance to the osmotic stress component of salinity stress in durum wheat. Functional Plant Biology 35: 111-123.
49. 2 availability. Plant Physiology 96: 363-367.
50. 2 prevents nitrate reduction in leaves. Plant Physiology 91: 970-974.
51. Kichey T, Heumez E, Pocholle D, Pageau K, Vanacker H, Dubois F, Le Gouis J, Hirel B. 2006. Combined agronomic and physiological aspects of nitrogen management in wheat highlight a central role for glutamine synthetase. New Phytologist 169: 265-278.
52. 3 plants from photooxidation. Nature 384: 557-560.
53. 4 influx and long-distance N translocation in rice: insights into feed-back processes. Plant Cell Physiology 39: 1287-1293.
54. Lam HM, Coschigano KT, Oliveira IC, Melo-Oliveira R, Coruzzi GM. 1996. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annual Review of Plant Physiology and Plant Molecular Biology 47: 569-593.
55. Li CC. 1975. Path analysis. A primer. Pacific Grove, CA, USA: The Boxwood Press.
56. Li X-P, Zhao X-Q, He X, Zhao G-Y, Li B, Liu D-C, Zhang A-M, Zhang X-Y, Tong Y-P, Li Z-S. 2011. Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use- and yield-related traits in bread wheat. New Phytologist 189: 449-458.
57. Lopes M, Araus JL. 2006. Nitrogen source and water regime effects on durum wheat photosynthesis, and stable carbon and nitrogen isotope composition. Physiologia Plantarum 126: 435-445.
58. Lopes M, Nogués S, Araus JL. 2004. Nitrogen source and water regime effects on barley photosynthesis and isotope discrimination. Functional Plant Biology 31: 995-1003.
59. Mariotti A, Martiotti F, Champigny ML, Amarger N, Moyse A. 1982. Nitrogen isotope fractionation associated with nitrate reductase activity and uptake of nitrate by pearl millet Pennisetum spp. Plant Physiology 69: 880-884.
60. Márquez AJ, Betti M, García-Calderón M, Estivill G, Credali A, Pajuelo P, Orea A, Clemente MT, Pajuelo E, Galván F. 2005. Nitrate and ammonium assimilatory enzymes. In: Márquez AJ, ed. Lotus japonicus handbook. Dordrecht, The Netherlands: Springer, 315-328.
61. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gauflichon L, Suzuki A. 2010. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany 105: 1141-1157.
62. Munns R. 2002. Comparative physiology of salt and water stress. Plant, Cell & Environment 25: 239-250.
63. Munns R, Hare RA, James RA, Rebetzke GJ. 2000. Genetic variation for improving the salt tolerance of durum wheat. Australian Journal of Agricultural Research 51: 69-74.
64. Munns R, James RA. 2003. Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant and Soil 253: 201-218.
65. Munns R, James RA, Sirault XRR, Furbank RT, Jones HG. 2010. New phenotyping methods for screening wheat and barley for beneficial responses to water deficit. Journal of Experimental Botany 61: 3499-3507.
66. Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology 59: 651-681.
67. Ouerghi Z, Cornic G, Roudani M, Ayadi A, Brulfert J. 2000. Effect of NaCl on photosynthesis of two wheat species (Triticum durum and T. aestivum) differing in their sensitivity to salt stress. Journal of Plant Physiology 156: 335-340.
68. Pajuelo P, Pajuelo E, Orea A, Romero JM, Márquez AJ. 2002. Influence of plant age and growth conditions on nitrate assimilation in roots of Lotus japonicus plants. Functional Plant Biology 29: 485-494.
69. Rahnama A, Poustini K, Munns R, James RA. 2010. Stomatal conductance as a screen for osmotic stress tolerance in durum wheat growing in saline soil. Functional Plant Biology 37: 255-263.
70. 15N of wheat grain. Rapid communications in Mass Spectrometry 24: 261-266.
71. Rana NK, Mohanpuria P, Kumar V, Kumar Yadav S. 2010. A CsGS is regulated at transcriptional level during developmental stages and nitrogen utilization in Camellia sinensis (L.) O. Kuntze. Molecular Biology Reports 37: 703-710.
72. Rao KR, Gnanam A. 1990. Inhibition of nitrate and nitrite reductase activities by salinity stress in Sorghum vulgare. Phytochemistry 29: 1047-1049.
73. Rivelli AR, James RA, Munns R, Condon AG. 2002. Effects of salinity on water relations and growth of wheat genotypes with contrasting sodium uptake. Functional Plant Biology 29: 1065-1074.
74. 13C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes. Journal of Experimental Botany 51: 41-50.
75. Sahu AC, Sahoo SK, Sahoo N. 2001. NaCl-stress induced alteration in glutamine synthetase activity in excised senescing leaves of a salt-sensitive and a salt-tolerant rice cultivar in light and darkness. Plant Growth Regulation 34: 287-292.
76. Scheidegger Y, Saurer M, Bahn M, Siegwolf R. 2000. Linking stable oxygen and carbon isotopes with stomatal conductance and photosynthetic capacity, a conceptual model. Oecologia 125: 350-357.
77. Sheshshayee MS, Bindumadhava H, Ramesh R, Prasad TG, Lakshminarayana MR, Udayakumar M. 2005. Oxygen isotope enrichment (Delta O-18) as a measure of time-averaged transpiration rate. Journal of Experimental Botany 56: 3033-3039.
78. Smart DR, Bloom AJ. 2001. Wheat leaves emit nitrous oxide during nitrate assimilation. Proceedings of the National Academy of Sciences, USA 98: 7875-7878.
79. Tardieu F, Granier CH, Muller B. 2011. Water deficit and growth. Co-ordinating processes without an orchestrator?. Current Opinion in Plant Biology 14: 283-289.
80. Tardieu F, Reymond M, Hamard H, Granier C, Muller B. 2000. Spatial distributions of expansion rate, cell division rate and cell size in maize leaves: a synthesis of the effects of soil water status, evaporative demand and temperature. Journal of Experimental Botany 51: 1505-1514.
81. 15N-abundance in key metabolites? Functional Plant Biology, 38: 1-12.
82. Tcherkez G, Farquhar GD. 2006. Isotopic fractionation by plant nitrate reductase, twenty years later. Functional Plant Biology 33: 531-537.
83. 3 leaves. Journal of Experimental Botany 59: 1685-1693.
84. 13C fractionations in plant primary metabolism. Trends in Plant Science 16: 499-506.
85. Tsai YC, Kao CII. 2002. Light-dependent ammonium ion toxicity of rice in response to phosphinothricin treatment. Biologia Plantarum 45: 569-573.
86. Ullrich WR. 2002. Salinity and nitrogen nutrition. In: Läuchli A, Lüttge U, eds. Salinity: environment - plants - molecules. Dordrecht, The Netherlands: Kluwer Academic Publishers, 229-248.
87. Veeranagamallaiah G, Chandraobulreddy P, Jyothsnakumari G, Sudhakar Chinta. 2007. Glutamine synthetase expression and pyrroline-5-carboxylate reductase activity influence proline accumulation in two cultivars of foxtail millet (Setaria italica L.) with differential salt sensitivity. Environmental and Experimental Botany 60: 239-244.
88. 15N natural abundances in Hawaiian rainforest: patterns and possible mechanisms. Oecologia 78: 383-388.
89. Wang ZQ, Yuan YZ, Ou JQ, Lin QH, Zhang CF. 2007. Glutamine synthetase and glutamate dehydrogenase contribute differentially to proline accumulation in leaves of wheat (Triticum aestivum) seedlings exposed to different salinity. Journal of Plant Physiology 164: 695-701.
90. 15N in nitrogenous fractions of Komatsuna plants supplied with nitrate. Plant & Cell Physiology 30: 957-962.
91. 13C of genotypic differences in the response of durum wheat to salinity. Functional Plant Biology 36: 144-155.
92. 15N of durum wheat and related amphiploids. Journal of Experimental Botany 61: 3529-3542.