Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Shoot δ15N gives a better indication than ion concentration or Δ13C of genotypic differences in the response of durum wheat to salinity

Salima Yousfi A , Maria Dolores Serret A and José Luis Araus B C
+ Author Affiliations
- Author Affiliations

A Unitat de Fisiologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Av. Diagonal, 647, 08028 Barcelona, Spain.

B International Maize and Wheat Improvement Center (CIMMYT), El Batán, Texcoco, CP 56130, Mexico.

C Corresponding author. Email: jaraus@cgiar.org

Functional Plant Biology 36(2) 144-155 https://doi.org/10.1071/FP08135
Submitted: 25 April 2008  Accepted: 18 November 2008   Published: 5 February 2009

Abstract

We compared the performance of different physiological traits that reveal genotypic variations in tolerance to salinity in durum wheat. A set of 114 genotypes was grown in hydroponics for over 3 months. Three conditions: control, moderate (12 dS m-1) and severe (17 dS m-1) salinity, were maintained for nearly 8 weeks before harvest. The genotype biomass in control conditions correlated with the biomass at the two salinity levels. Subsequently, two subsets of 10 genotypes each were selected on the basis of extreme differences in biomass at the two salinity levels while showing relatively similar biomass in control conditions. Carbon isotope discrimination (Δ13C), nitrogen isotope composition (δ15N), and the concentration of nitrogen, phosphorus and several ions (K+, Na+, Ca2+, Mg2+) were analysed in the two subsets for the three treatments. At 12 dS m-1, K+ concentration, K+/Na+ ratio, Δ13C and δ15N correlated positively and Na+ correlated negatively with shoot biomass. Under control conditions and at 17 dS m-1 no correlation was observed. However, the trait that correlated best with genotypic differences in biomass was δ15N at 12 dS m-1. This trait was the first variable chosen at each of the two salinity levels in a stepwise analysis. We consider the possible mechanisms relating δ15N to biomass and the use of this isotopic signature as a selection trait.

Additional keywords: NaCl, photosynthesis, potassium, salt, sodium, stable isotopes, Triticum turgidum ssp. durum.


Acknowledgements

This study was supported in part by the European research project TRITIMED (INCO-CT-2004–509136) and by the Spanish Ministry of Science and Technology project, AGL-2006–13541-C02–1. We also thank the support of SRG2005D0468 from the Gerenalitat de Catalunya, Spain. Salima Yousfi was the recipient of a doctoral fellowship from the AECI, Spanish Ministry of Foreign Affairs, Spain. We thank Dr J. Bort and Ll. Cabrera for their help.


References


Araus JL, Villegas D, Aparicio N, García del Moral LF, 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. open url image1

Arslan A, Zapata F, Kumarasinghe KS (1999) Carbon isotope discrimination as an indicator of water use efficiency of spring wheat as affected by salinity and gypsum addition. Communications in Soil Science and Plant Analysis 30, 2681–2693.
CrossRef | CAS | open url image1

Ayers RS , Westcott DW (1989) Water quality for agriculture. FAO irrigation and drainage paper 29 Rev.1. FAO, Rome.

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.
CrossRef | CAS | open url image1

Chhipa BR, Lal P (1995) Na/K ratios as the basis of salt tolerance in wheat. Australian Journal of Agricultural Research 46, 533–539.
CrossRef | open url image1

Colmer TD, Munns R, Flowers TJ (2005) Improving salt tolerance of wheat and barley: future prospects. Australian Journal of Experimental Agriculture 45, 1425–1443.
CrossRef | CAS | open url image1

Coplen TB (2008) ‘Explanatory glossary of terms used in Expression of relative isotope ratios and gas Ratios. IUPAC Recommendations 2008.’ (International Union of Pure and Applied Chemistry Inorganic Chemistry Division, Commission on Isotopic Abundances and Atomic Weights: Research Triangle Park, NC, USA)

Coque M, Bertin P, Hirel B, Gallais A (2006) Genetic variation and QTLs for 15N natural abundance in a set of maize recombinant inbred lines. Field Crops Research 97, 310–321.
CrossRef | open url image1

Cuin TA, Miller AJ, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. Journal of Experimental Botany 54, 657–661.
CrossRef | CAS | PubMed | open url image1

Dvorak J, Noaman M, Goyal S, Gorham J (1994) Enhancement of salt-tolerance of Triticum turgidum L. by the Knal locus transferred from the Triticum aestivum L. Theoretical and Applied Genetics 87, 872–877.
CrossRef | open url image1

Ellis RP, Foster BP, Waugh R, Bonar N, Handley LL, Robinson D, Gordon D, Powell W (1997) Mapping physiological traits in barley. New Phytologist 137, 149–157.
CrossRef | CAS | open url image1

Ellis RP, Forster BP, Gordon DC, Handley LL, Keith RP , 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.
CrossRef | CAS | PubMed | open url image1

Evans RD (2001) Physiological mechanism influencing plant nitrogen isotope composition. Trends in Plant Science 6, 121–126.
CrossRef | CAS | PubMed | open url image1

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.
CAS | CrossRef | PubMed |
open url image1

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.
CrossRef | CAS | open url image1

Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 40, 503–537.
CrossRef | CAS | open url image1

Flowers TJ (2004) Improving crop salt tolerance. Journal of Experimental Botany 55, 307–319.
CrossRef | CAS | PubMed | open url image1

Gorham J (1993) Genetics and physiology of enhanced K/Na discrimination. In ‘Genetic aspects of plant mineral nutrition’. (Eds PJ Randall, E Delhaize, RA Richards, R Munns) pp. 151–158. (Kluwer Academic Publishers: Dordrecht, the Netherlands)

Handley LL, Robinson D, Forster BP, Ellis RP, Scrimgeour CM, Gordon DC, Nero E, Raven JA (1997) Shoot δ15N correlates with genotype and salt stress in barley. Planta 201, 100–102.
CrossRef | CAS | open url image1

Handley LL, Austin AT, Robinson D, Scrimgeour CM, Raven JA, Heaton TH, Schmidt S, Stewart GR (1999) The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Australian Journal of Plant Physiology 26, 185–199.
CrossRef | open url image1

Heuer B, Plaut Z (1989) Photosynthesis and osmotic adjustment of two sugar beet cultivars grown under saline conditions. Journal of Experimental Botany 40, 437–440.
CrossRef | open url image1

Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular 347, 1–32. open url image1

Husain S, von Caemmerer S, Munns R (2004) Control of salt transport from roots to shoots of wheat in saline soil. Functional Plant Biology 31, 1115–1126.
CrossRef | CAS | open url image1

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.
CrossRef | open url image1

Islam TMT, Sedgley RH (1981) Evidence for a ‘uniculm effect’ in spring wheat (Triticum aestivum L.) in a Mediterranean environment. Euphytica 30, 277–282.
CrossRef | open url image1

James RA, Rivelli AR, Munns R, von Caemmerer S (2002) Factors affecting CO2 assimilation, leaf injury and growth in salt-stressed durum wheat. Functional Plant Biology 29, 1393–1403.
CrossRef | CAS | open url image1

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.
CrossRef | CAS | open url image1

Kingsbury RW, Epstein E (1984) Selection for salt-resistant spring wheat. Crop Science 24, 310–314. open url image1

Ledgard SF, Woo KC, Bergersen FJ (1985) Isotopic fractionation during reduction of nitrate and nitrite by extracts of spinach leaves. Australian Journal of Plant Physiology 12, 631–640.
CrossRef | CAS | open url image1

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.
CrossRef | CAS | open url image1

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.
CrossRef | CAS | open url image1

Maas EV, Lesch SM, Francois LE, Grieve CM (1994) Tiller development in salt stressed wheat. Crop Science 34, 1594–1603. open url image1

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.
CAS | CrossRef | PubMed |
open url image1

Munns R (2008) ‘The impact of salinity stress.’ Available at www.plantstress.com/Articles/index.asp [verified February 2008].

Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant and Soil 253, 201–218.
CrossRef | CAS | open url image1

Munns R, Husain S, Rivelli AR, James RA, Condon AG (2002) Avenues for increasing salt tolerance of crops, and the role of physiologically based selection traits. Plant and Soil 247, 93–105.
CrossRef | CAS | open url image1

Nachit MM, Elouafi I, Pagnotta MA, El Saleh A, Iacono E , et al . (2001) Molecular linkage map for an intraspecific recombinant inbred population of durum wheat (Triticum turgidum L. var. durum). Theoretical and Applied Genetics 102, 177–186.
CrossRef | CAS | open url image1

Nicolas ME, Munns R, Samarakoon AB, Gifford RM (1993) Elevated CO2 improves the growth of wheat under salinity. Australian Journal of Plant Physiology 20, 349–360.
CrossRef | CAS | open url image1

Nogués S, Tcherkez G, Cornic G, Ghashgaie J (2004) Respiratory carbon metabolism following illumination in intact French bean leaves using 13C/12C isotope labelling. Plant Physiology 137, 1–10.
CrossRef | open url image1

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.
CAS |
open url image1

Pakniyat H, Handley LL, Thomas WTB, Connolly T, Macaulay M, Caligari PDS, Foster BP (1997) Comparison of shoot dry weight, Na+ concentration and δ13C values of ari-e and other semi-dwarf barley mutants under salt stress. Euphytica 94, 7–14.
CrossRef | CAS | open url image1

Passioura JB, Munns R (2000) Rapid environmental changes that affect leaf water status induce transient surges or pauses in leaf expansion rate. Australian Journal of Plant Physiology 27, 941–948.
CrossRef | open url image1

Peuke AD, Gessler A, Rennenberg H (2006) The effect of drought on C and N stable isotopes in different fractions of leaves, stems and roots of sensitive and tolerant beech ecotypes. Plant, Cell & Environment 29, 823–835.
CrossRef | CAS | PubMed | open url image1

Pritchard ES, Guy RD (2005) Nitrogen isotope discrimination in white spruce fed with low concentrations of ammonium and nitrate. Trees – Structure and Function 19, 89–98.
CrossRef | CAS | open url image1

Rasmuson KE, Anderson JE (2002) Salinity affects development, growth, and photosynthesis in cheatgrass. Journal of Range Management 55, 80–87.
CrossRef | open url image1

Rebetzke GJ, Read JJ, Barbour MM, Condon AG, Rawson HM (2000) A hand-held porometer for rapid assessment of leaf conductance in wheat. Crop Science 40, 277–280. open url image1

Rengasamy P (2002) Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overwiev. Australian Journal of Experimental Agriculture 42, 351–361.
CrossRef | open url image1

Richards RA (1983) Should selection for yield in saline regions be made on saline or non-saline soils? Euphytica 32, 431–438.
CrossRef | open url image1

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.
CrossRef | CAS | open url image1

Robinson D, Handley LL, Scrimgeour CM, Gordon C, Forster BP, Ellis RP (2000) Using stable isotope natural abundances (δ15N and δ13C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes. Journal of Experimental Botany 51, 41–50.
CrossRef | CAS | PubMed | open url image1

Sayed HI (1985) Diversity of salt tolerance in a germplasm collection of wheat (Triticum spp.). Theoretical and Applied Genetics 69, 651–657.
CrossRef | open url image1

Shaheen R, Hood-Nowotny RC (2005) Effect of drought and salinity on carbon isotope discrimination in wheat cultivars. Plant Science 168, 901–909.
CrossRef | CAS | open url image1

Sharkey TD, Raschke K (1981) Separation and measurement of direct and indirect effects of light on stomata. Plant Physiology 68, 33–40.
CrossRef | PubMed |
open url image1

Smart DR, Bloom AJ (2001) Wheat leaves emit nitrous oxide during nitrate assimilation. Proceedings of the National Academy of Sciences of the United States of America 98, 7875–7878.
CrossRef | CAS | PubMed | open url image1

Srivastava JP , Jana S (1984) Screening wheat and barley germplasm for salt tolerance. In ‘Salinity tolerance in plants: strategies for crop improvement’. (Eds RC Staples, GH Toenniessen) pp. 273–283. (Wiley & Sons: New York)

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
CrossRef | CAS | PubMed | open url image1

Vitousek PM, Shearer G, Kohl DH (1989) Foliar 15N natural abundances in Hawaiian rainforest: patterns and possible mechanisms. Oecologia 78, 383–388.
CrossRef | open url image1

Wang Z-Q, Yuan Y-Z, Ou J-Q, Lin Q-H, Zhang C-F (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.
CrossRef | CAS | PubMed | open url image1

World Bank (2007) ‘World development report 2008. Agriculture for development.’ Available at http://siteresources.worldbank.org/INTWDR2008/Resources/WDR_00_book.pdf [verified 4 December 2008].

Yoneyama T, Kamachi K, Yamaya T, Mae T (1993) Fractionation of nitrogen isotopes by glutamine synthetase isolated from spinach leaves. Plant & Cell Physiology 34, 489–491.
CAS |
open url image1








Rent Article (via Deepdyve) Export Citation Cited By (27)