Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T03:09:22.009Z Has data issue: false hasContentIssue false
  • English
  • Français

Comparative performance of the stable isotope signatures of carbon, nitrogen and oxygen in assessing early vigour and grain yield in durum wheat

Published online by Cambridge University Press:  23 May 2013

J. BORT ,
M. BELHAJ ,
K. LATIRI ,
Z. KEHEL  and
J. L. ARAUS
J. BORT*
Affiliation:
Plant Biology Department, Faculty of Biology, University of Barcelona, Diagonal 643, 08028 Barcelona, Spain
M. BELHAJ
Affiliation:
INRAT, Field Crops Laboratory, Rue Hédi Karray, 2049 Ariana, Tunisia
K. LATIRI
Affiliation:
INRAT, Field Crops Laboratory, Rue Hédi Karray, 2049 Ariana, Tunisia
Z. KEHEL
Affiliation:
Biodiversity and Integrated Gene Management, International Centre for Agricultural Research in the Dry Areas (ICARDA), PO Box 5466, Aleppo, Syria
J. L. ARAUS
Affiliation:
Plant Biology Department, Faculty of Biology, University of Barcelona, Diagonal 643, 08028 Barcelona, Spain
*
*To whom all correspondence should be addressed. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The present paper studied the performance of the stable isotope signatures of carbon (δ13C), nitrogen (δ15N) and oxygen (δ18O) in plants when used to assess early vigour and grain yield (GY) in durum wheat growing under mild and moderate Mediterranean stress conditions. A collection of 114 recombinant inbred lines was grown under rainfed (RF) and supplementary irrigation (IR) conditions. Broad sense heritabilities (H2) for GY and harvest index (HI) were higher under RF conditions than under IR. Broad sense heritabilities for δ13C were always above 0·60, regardless of the plant part studied, with similar values for IR and RF trials. Some of the largest genetic correlations with GY were those shown by the δ13C content of the flag leaf blade and mature grains. Under both water treatments, mature grains showed the highest negative correlations between δ13C and GY across genotypes. Flag leaf δ13C was negatively correlated with GY only under RF conditions. The δ13C in seedlings was negatively correlated, under IR conditions only, with GY but also with early vigour. The sources of variation in early vigour were studied by stepwise analysis using the stable isotope signatures measured in seedlings. The δ13C was able to explain almost 0·20 of this variation under RF, but up to 0·30 under IR. In addition, nitrogen concentration in seedlings accounted for another 0·05 of variation, increasing the amount explained to 0·35. The sources of variation in GY were also studied through stable isotope signatures and biomass of different plant parts: δ13C was always the first parameter to appear in the models for both water conditions, explaining c. 0·20 of the variation. The second parameter (δ15N or N concentration of grain, or biomass at maturity) depended on the water conditions and the plant tissue being analysed. Oxygen isotope composition (δ18O) was only able to explain a small amount of the variation in GY. In this regard, despite the known and previously described value of δ13C as a tool in breeding, δ15N is confirmed as an additional tool in the present study. Oxygen isotope composition does not seem to offer any potential, at least under the conditions of the present study.

Type
Crops and Soils Research Papers
Information
The Journal of Agricultural Science , Volume 152 , Issue 3 , June 2014 , pp. 408 - 426
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Acevedo, E. (1993). Potential of carbon isotope discrimination as a selection criterion in barley breeding. In Stable Isotopes and Plant Carbon-Water Relations (Eds Ehleringer, J. R., Hall, A. E. & Farquhar, G. D.), pp. 399–417. New York: Academic Press.Google Scholar
Acevedo, E. H., Silva, P. C., Silva, H. R. & Solar, B. R. (1999). Wheat production in Mediterranean environments. In Wheat: Ecology and Physiology of Yield Determination (Eds Satorre, E. H. & Slafer, G. A.), pp. 295–332. New York: Food Products Press.Google Scholar
Aparicio, N., Villegas, D., Araus, J. L., Blanco, R. & Royo, C. (2002). Seedling development and biomass as affected by seed size and morphology in durum wheat. Journal of Agricultural Science, Cambridge 139, 143–150.Google Scholar
Araus, J. L. (2004). The problem of sustainable water use in the Mediterranean and research requirements for agriculture. Annals of Applied Biology 144, 259–272.Google Scholar
Araus, J. L., Alegre, L., Tapia, L. & Calafell, R. (1986). Relationship between leaf structure and gas exchange in wheat leaves at different insertion levels. Journal of Experimental Botany 37, 1323–1333.Google Scholar
Araus, J. L., Tapia, L. & Alegre, L. (1989). The effect of changing sowing date on leaf structure and gas exchange characteristics of wheat flag leaves grown under Mediterranean conditions. Journal of Experimental Botany 40, 639–646.Google Scholar
Araus, J. L., Amaro, T., Zuhair, Y. & Nachit, M. M. (1997). Effect of leaf structure and water status on carbon isotope discrimination in field-grown durum wheat. Plant Cell and Environment 20, 1484–1494.Google Scholar
Araus, J. L., Amaro, T., Casadesús, J., Asbati, A. & Nachit, M. M. (1998). Relationships between ash content, carbon isotope discrimination and yield in durum wheat. Australian Journal of Plant Physiology 25, 835–842.Google Scholar
Araus, J. L., Slafer, G. A., Reynolds, M. P. & Royo, C. (2002). Plant breeding and water relations in C3 cereals: what should we breed for? Annals of Botany, London 89, 925–940.Google Scholar
Araus, J. L., Villegas, D., Aparicio, N., García Del Moral, L. F., El Hani, S., Rharrabti, Y., Ferrio, J. P. & Royo, C. (2003). Environmental factors determining carbon isotope discrimination and yield in durum wheat under Mediterranean conditions. Crop Science 43, 170–180.Google Scholar
Araus, J. L., Slafer, G. A., Royo, C. & Serret, M. D. (2008). Breeding for yield potential and stress adaptation in cereals. Critical Reviews in Plant Science 27, 377–412.Google Scholar
Austin, R. B. (1999). Yield of wheat in the United Kingdom: recent advances and prospects. Crop Science 39, 1604–1610.Google Scholar
Bänziger, M., Edmeades, G. O., Beck, D. & Bellon, M. (2000) Breeding for Drought and Nitrogen Stress Tolerance in Maize: From Theory to Practice. Mexico, DF: CIMMYT.Google Scholar
Barbour, M. M. (2007). Stable oxygen isotope composition of plant tissue: a review. Functional Plant Biology 34, 83–94.Google Scholar
Barbour, M. M., Fischer, R. A., Sayre, K. D. & Farquhar, G. D. (2000 a). 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.Google Scholar
Barbour, M. M., Schurr, U., Henry, B. K., Chin Wong, S. & Farquhar, G. D. (2000 b). Variation in the oxygen isotope ratio of phloem sap sucrose from castor bean. Evidence in support of the Péclet effect. Plant Physiology 123, 671–679.Google Scholar
Blum, A. (2006). Drought adaptation in cereal crops: a prologue. In Drought Adaptation in Cereals (Ed. Ribaut, J. M.), pp. 3–15. New York: The Harworth Press, Inc.Google Scholar
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.Google Scholar
Bort, J., Araus, J. L., Hazzam, H., Grando, S. & Ceccarelli, S. (1998). Relationships between early vigour, grain yield, leaf structure and stable isotope composition in field grown barley. Plant Physiology and Biochemistry 36, 889–897.CrossRefGoogle Scholar
Botwright, T. L., Condon, A. G., Rebetzke, G. J. & Richards, R. A. (2002). Field evaluation of early vigour for genetic improvement of grain yield in wheat. Australian Journal of Agricultural Research 53, 1137–1145.Google Scholar
Cabrera-Bosquet, L., Molero, G., Nogués, S. & Araus, J. L. (2009). Water and nitrogen conditions affect the relationships of Δ13C and Δ18O with gas exchange and growth in durum wheat. Journal of Experimental Botany 60, 1633–1644.Google Scholar
Cabrera-Bosquet, L., Albrizio, R., Nogués, S. & Araus, J. L. (2011). Dual Δ13C/δ 18O response to water and nitrogen availability and its relationship with yield in field-grown durum wheat. Plant Cell and Environment 34, 418–433.Google Scholar
Cernusak, L. A., Wong, S. C. & Farquhar, G. D. (2003). Oxygen isotope composition of phloem sap in relation to leaf water in Ricinus communis. Functional Plant Biology 30, 1059–1070.Google Scholar
Condon, A. G. (2012). Comparative evaluation of oxygen isotope composition and carbon isotope discrimination in selecting for greater agronomic water use efficiency in wheat. In Greater Agronomic Water Use Efficiency in Wheat and Rice using Carbon Isotope Discrimination (Ed. International Atomic Energy Agency), pp. 267–275. IAEA-TECDOC-1671. Vienna, Austria: International Atomic Energy Agency.Google Scholar
Condon, A. G. & Richards, R. A. (1992). Broad sense heritability and genotype×environment interaction for carbon isotope discrimination in field-grown wheat. Australian Journal of Agricultural Research 43, 921–934.CrossRefGoogle Scholar
Condon, A. G., Richards, R. A., Rebetzke, G. J. & Farquhar, G. D. (2002). Improving intrinsic water-use efficiency and crop yield. Crop Science 42, 122–131.Google Scholar
Condon, A. G., Richards, R. A., Rebetzke, G. J. & Farquhar, G. D. (2004). Breeding for high water-use efficiency. Journal of Experimental Botany 55, 2447–2460.Google Scholar
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.Google Scholar
Craig, H. & Gordon, L. I. (1965). Deuterium and oxygen 18 variations in the ocean and marine atmosphere. In Stable Isotopes in Oceanographic Studies and Paleotemperatures (Ed. Tongiorgi, E.), pp. 9–130. Pisa, Italy: Consiglio Nazionale Delle Ricerche Laboratorio Di Geologia Nucleare.Google Scholar
Cullis, B. R., Smith, A. B. & Coombes, N. E. (2006). On the design of early generation variety trials with correlated data. Journal of Agricultural, Biological, and Environmental Statistics 11, 381–393.Google Scholar
Dongmann, G., Nurnberg, H. W., Forstel, H. & Wagener, K. (1974). On the enrichment of H218O in the leaves of transpiring plants. Radiation and Environmental Biophysics 11, 41–52.Google Scholar
Ehdaie, B. & Waines, J. G. (1993). Variations in water use efficiency and its components in wheat: I. Well-watered pot experiment. Crop Science 33, 294–299.Google Scholar
Ellis, R. P., Forster, B. P., Waugh, R., Bonar, N., Handley, L. L., Robinson, D., Gordon, D. C. & Powell, W. (1997). Mapping physiological traits in barley. New Phytologist 137, 149–157.Google Scholar
Ellis, R. P., Forster, B. P., Gordon, D. C., Handley, L. L., Keith, R. P., Lawrence, P., Meyer, R., Powell, W., Robinson, D., Scrimgeour, C. M., Young, G. & Thomas, W. T. B. (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.Google Scholar
Evans, L. T., Wardlaw, I. F. & Fischer, R. A. (1975). Wheat. In Crop Physiology; Some Case Histories (Ed. Evans, L. T.), pp. 101–149. London: Cambridge University Press.Google Scholar
Falconer, D. S. & Mackay, T. F. C. (1996). Introduction to Quantitative Genetics, 4th edn, New York: Longman.Google Scholar
Farquhar, G. D. & Lloyd, J. (1993). Carbon and oxygen isotope effects in the exchange of carbon dioxide between terrestrial plants and the atmosphere. In Stable Isotopes and Plant Carbon–Water Relations (Eds Ehleringer, J. R., Hall, A. E. & Farquhar, G. D.), pp. 47–70. San Diego, USA: Academic Press, Inc.Google Scholar
Farquhar, G. D. & Richards, R. A. (1984). Isotopic composition of plant carbon correlates with water-use-efficiency of wheat genotypes. Australian Journal of Plant Physiology 11, 539–552.Google Scholar
Farquhar, G. D., Firth, P. M., Wetselaar, R. & Weir, B. (1980). On the gaseous exchange of ammonia between leaves and the environment: determination of the ammonia compensation point. Plant Physiology 66, 710–714.CrossRefGoogle ScholarPubMed
Farquhar, G. D., Cernusak, L. A. & Barnes, B. (2007). Heavy water fractionation during transpiration. Plant Physiology 143, 11–18.Google Scholar
Febrero, A., Blum, A., Romagosa, I. & Araus, J. L. (1993). Relationship between carbon isotope discrimination in field grown barley and some physiological traits of juvenile plants in growth chamber. In Supplemental Abstracts of the First International Crop Science Congress (Eds Buxton, D. R., Shibles, R., Forsberg, R. A., Blad, B. L., Asay, K. H., Paulsen, G. M. & Wilson, R. F.), pp. 717–726, 14–22 July 1992, Iowa State Center, Ames, Iowa, USA. Madison, WI: CSSA.Google Scholar
Ferrio, J. P., Mateo, M. A., Bort, J., Abdalla, O., Voltas, J. & Araus, J. L. (2007). Relationships of grain δ 13C and δ 18O with wheat phenology and yield under water-limited conditions. Annals of Applied Biology 150, 207–215.Google Scholar
Fischer, R. A. (2007). Understanding the physiological basis of yield potential in wheat. Journal of Agricultural Science, Cambridge 145, 99–113.Google Scholar
Fischer, R. A., Rees, D., Sayre, K. D., Lu, Z-M., Condon, A. G. & Saavedra, A. L. (1998). Wheat yield progress associated with higher stomatal conductance and photosynthetic rate and cooler canopies. Crop Science 38, 1467–1475.Google Scholar
Foulkes, M. J., Slafer, G. A., Davies, W. J., Berry, P. M., Sylvester-Bradley, R., Martre, P., Calderini, D. F., Griffiths, S. & Reynolds, M. P. (2011). Raising yield potential of wheat. III. Optimizing partitioning to grain while maintaining lodging resistance. Journal of Experimental Botany 62, 469–486.Google Scholar
García Del Moral, L. F., Rharrabti, Y., Villegas, D. & Royo, C. (2003). Evaluation of grain yield and its components in durum wheat under Mediterranean conditions. Agronomy Journal 95, 266–274.Google Scholar
Handley, L. L., Robinson, D., Forster, B. P., Ellis, R. P., Scrimgeour, C. M., Gordon, D. C., Nero, E. & Raven, J. A. (1997). Shoot δ 15N correlates with genotype and salt stress in barley. Planta 201, 100–102.Google Scholar
Hubick, K. T. & Farquhar, G. D. (1989). Carbon isotope discrimination and the ratio of carbon gained to water lost in barley cultivars. Plant, Cell and Environment 12, 795–804.Google Scholar
ICARDA (2004). ICARDA Annual Report 2003. Aleppo, Syria: ICARDA.Google Scholar
Kehel, Z., Habash, D. Z., Gezan, S. A., Welham, S. J. & Nachit, M. M. (2010). Estimation of spatial trend and automatic model selection in augmented designs. Agronomy Journal 102, 1542–1552.Google Scholar
Kelly, A. M., Smith, A. B., Eccleston, J. A. & Cullis, B. R. (2007). The accuracy of varietal selection using factor analytic models for multi-environment plant breeding trials. Crop Science 47, 1063–1070.Google Scholar
Latiri-Souki, K., Nortcliff, S. & Lawlor, D. W. (1998). Nitrogen fertilizer can increase dry matter, grain production and radiation and water use efficiencies for durum wheat under semi-arid conditions. European Journal of Agronomy 9, 21–34.Google Scholar
Latiri, K., Lhomme, J. P., Annabi, M. & Setter, T. L. (2010). Wheat production in Tunisia: Progress, inter-annual variability and relation to rainfall. European Journal of Agronomy 33, 33–42.Google Scholar
Maccaferri, M., Sanguineti, M. C., Demontis, A., El-Ahmed, A., Garcia Del Moral, L., Maalouf, F., Nachit, M., Nserallah, N., Ouabbou, H., Rhouma, S., Royo, C., Villegas, D. & Tuberosa, R. (2010). Association mapping in durum wheat grown across a broad range of water regimes. Journal of Experimental Botany 62, 409–438.Google Scholar
Maydup, M. L., Graciano, C., Guiamet, J. J. & Tambussi, E. A. (2012). Analysis of early vigour in twenty modern cultivars of bread wheat (Triticum aestivum L.). Crop and Pasture Science 63, 987–996.Google Scholar
Merah, O., Deleéns, E. & Monneveux, P. (1999). Grain yield, carbon isotope discrimination, mineral and silicon content in durum wheat under different precipitation regimes. Physiologia Plantarum 107, 387–394.Google Scholar
Merah, O., Deleéns, E., Souyris, I., Nachit, M. & Monneveux, P. (2001 a). Stability of carbon isotope discrimination and grain yield in durum wheat. Crop Science 41, 677–681.Google Scholar
Merah, O., Monneveux, P. & Deléens, E. (2001 b). Relationships between flag leaf carbon isotope discrimination and several morpho-physiological traits in durum wheat genotypes under Mediterranean conditions. Environmental and Experimental Botany 45, 63–71.CrossRefGoogle ScholarPubMed
Morgan, J. A., Lecain, D. R., Mccaig, T. N. & Quick, J. S. (1993). Gas exchange, carbon isotope discrimination and productivity in winter wheat. Crop Science 33, 178–186.Google Scholar
Nachit, M. M., Elouafi, I., Pagnotta, M. A., El Saleh, A., Iacono, E., Labhilili, M., Asbati, A., Azrak, M., Hazzam, H., Benscher, D., Khairallah, M., Ribaut, J.-M., Tanzarella, O. A., Porceddu, E. & Sorrells, M. E. (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.Google Scholar
Parry, M. A. J., Reynolds, M., Salvucci, M. E., Raines, C., Andralojc, P. J., Zhu, X-G., Price, G. D., Condon, A. G. & Furbank, R. T. (2011). Raising yield potential of wheat. II. Increasing photosynthetic capacity and efficiency. Journal of Experimental Botany 62, 453–467.Google Scholar
Passioura, J. B. (2002). Environmental biology and crop improvement. Functional Plant Biology 29, 537–546.Google Scholar
Payne, R. W., Murray, D. A., Harding, S. A., Baird, D. B. & Soutar, D. M. (2009). GenStat for Windows. Introduction, 12th edn, Hemel Hempstead, UK: VSN Int.Google Scholar
Pritchard, E. S. & Guy, R. D. (2005). Nitrogen isotope discrimination in white spruce fed with low concentrations of ammonium and nitrate. Trees – Structure and Function 19, 89–98.Google Scholar
Raimanová, I. & Haberle, J. (2010). The effects of differentiated water supply after anthesis and nitrogen fertilization on δ 15N of wheat grain. Rapid Communications in Mass Spectrometry 24, 261–266.Google Scholar
Rao, R. C. N., Udayakumar, M., Farquhar, G. D., Talwar, H. S. & Prasad, T. G. (1995). Variation in carbon isotope discrimination and its relationship to specific leaf area and ribulose-1,5-bisphosphate carboxylase content in groundnut genotypes. Australian Journal of Plant Physiology 22, 545–551.Google Scholar
Rebetzke, G. J., Condon, A. G., Richards, R. A. & Farquhar, G. D. (2002). Selection for reduced carbon isotope discrimination increases aerial biomass and grain yield of rainfed bread wheat. Crop Science 42, 739–745.Google Scholar
Rebetzke, G. J., Bruce, S. E. & Kirkegaard, J. A. (2005). Longer coleoptiles improve emergence through crop residues to increase seedling number and biomass in wheat (Triticum aestivum L.). Plant Soil 272, 87–100.Google Scholar
Rebetzke, G. J., Condon, A. G., Farquhar, G. D., Appels, R. & Richards, R. A. (2008). Quantitative trait loci for carbon isotope discrimination are repeatable across environments and wheat mapping populations. Theoretical and Applied Genetics 118, 123–137.Google Scholar
Reynolds, M., Condon, A. G., Rebetzke, G. J. & Richards, R. A. (2004). Evidence for excess photosynthetic capacity and sink-limitation to yield and biomass in elite spring wheat. In New Directions for a Diverse Planet. Proceedings of the 4th International Crop Science Congress (Eds Fischer, T., Turner, N., Angus, J., McIntyre, L., Robertson, M., Borrell, A. & Lloyd, D.). Gosford, Australia: The Regional Institute Ltd. Available from: http://www.cropscience.org.au/icsc2004/poster/2/7/3/1315_reynoldsmp.htm (verified 25 March 2013).Google Scholar
Reynolds, M., Foulkes, J. M., Slafer, G. A., Berry, P., Parry, M. A. J., Snape, J. W. & Angus, W. J. (2009). Raising yield potential in wheat. Journal of Experimental Botany 60, 1899–1918.Google Scholar
Reynolds, M., Bonnett, D., Chapman, S. C., Furbank, R. T., Manès, Y., Mather, D. E. & Parry, M. A. J. (2011). Raising yield potential of wheat. I. Overview of a consortium approach and breeding strategies. Journal of Experimental Botany 62, 439–452.Google Scholar
Richards, R. A. (2006). Physiological traits used in the breeding of new cultivars for water-scarce environments. Agricultural Water Management 80, 197–211.Google Scholar
Richards, R. A. & Lukacs, Z. (2002). Seedling vigour in wheat—sources of variation for genetic and agronomic improvement. Australian Journal of Agricultural Research 53, 41–50.CrossRefGoogle Scholar
Richards, R. A., López-Castañeda, C., Gomez-Macpherson, H. & Condon, A. G. (1993). Improving the efficiency of water use by plant breeding and molecular biology. Irrigation Science 14, 93–104.Google Scholar
Richards, R. A., Condon, A. G. & Rebetzke, G. J. (2001). Traits to improve yield in dry environments. In Application of Physiology in Wheat Breeding (Eds Reynolds, M. P., Ortiz-Monasterio, J. I. & McNab, A.), pp. 88–100. México DF: CIMMYT.Google Scholar
Richards, R. A., Rebetzke, G. J., Condon, A. G., & Van Herwaarden, A. F. (2002). Breeding opportunities for increasing the efficiency of water use and crop yield in temperate cereals. Crop Science 42, 111–121.Google Scholar
Robinson, D., Handley, L. L., Scrimgeour, C. M., Gordon, D. C., Forster, B. P. & Ellis, R. P. (2000). Using stable isotope natural abundances (δ 15N and δ 13C) to integrate the stress responses of wild barley (Hordeum spontaneum C. Koch.) genotypes. Journal of Experimental Botany 51, 41–50.Google Scholar
Saurer, M., Aellen, K. & Siegwolf, R. (1997). Correlating δ 13C and δ 18O in cellulose of trees. Plant, Cell and Environment 20, 1543–1550.Google Scholar
Sayre, K. D., Acevedo, E. & Austin, R. B. (1995). Carbon isotope discrimination and grain yield for three bread wheat germplasm groups grown at different levels of water stress. Field Crops Research 41, 45–54.Google Scholar
Slafer, G. A. & Araus, J. L. (2007). Physiological traits for improving wheat yield under a wide range of conditions. In Scale and Complexity in Plant Systems Research: Gene-Plant-Crop Relations (Eds Spiertz, J. H. J., Struik, P. C. and van Laar, H. H.), pp. 147–156. Dordrecht: Springer.Google Scholar
Slafer, G. A., Araus, J. L. & Richards, R. A. (1999). Physiological traits that increase the yield potential of wheat. In Wheat: Ecology and Physiology of Yield Determination (Eds Satorre, E. H. & Slafer, G. A.), pp. 379–415. New York: Food Products Press.Google Scholar
Smart, D. R. & Bloom, A. J. (2001). Wheat leaves emit nitrous oxide during nitrate assimilation. Proceedings of the National Academy of Scinces, USA 98, 7875–7878.Google Scholar
Serret, M. D., Ortiz-Monasterio, I., Pardo, A. & Araus, J. L. (2008). The effects of urea fertilisation and genotype on yield, nitrogen use efficiency, δ 15N and δ 13C in wheat. Annals of Applied Biology 153, 243–257.Google Scholar
Tambussi, E. A., Nogués, S. & Araus, J. L. (2005 a). Ear of durum wheat under water stress: water relations and photosynthetic metabolism. Planta 221, 446–458.Google Scholar
Tambussi, E. A., Nogués, S., Ferrio, J. P., Voltas, J. & Araus, J. L. (2005 b). Does higher yield potential improve barley performance in Mediterranean conditions? A case study. Field Crops Research 91, 149–160.CrossRefGoogle Scholar
Tambussi, E. A., Bort, J. & Araus, J. L. (2007). Water use efficiency in C3 cereals under Mediterranean conditions: a review of physiological aspects. Annals of Applied Biology 150, 307–321.Google Scholar
Trethowan, R. M., Van Ginkel, M. & Rajaram, S. (2002). Progress in breeding wheat for yield and adaptation in global drought affected environments. Crop Science 42, 1441–1446.Google Scholar
Villegas, D., Aparicio, N., Nachit, M. M., Araus, J. L. & Royo, C. (2000). Photosynthetic and developmental traits associated with genotypic differences in durum wheat yield across the Mediterranean basin. Australian Journal of Agricultural Research 51, 891–901.Google Scholar
Yakir, D. (1992). Variations in the natural abundance of oxygen-18 and deuterium in plant carbohydrates. Plant, Cell and Environment 15, 1005–1020.Google Scholar
Yakir, D. & Deniro, M. J. (1990). Oxygen and hydrogen isotope fractionation during cellulose metabolism in Lemna gibba. L. Plant Physiology 93, 325–332.CrossRefGoogle ScholarPubMed
Yakir, D., Deniro, M. J. & Gat, J. R. (1990). Natural deuterium and oxygen-18 enrichment in leaf water of cotton plants grown under wet and dry conditions—evidence for water compartmentation and its dynamics. Plant, Cell and Environment 13, 49–56.Google Scholar
Yousfi, S., Serret, M. D. & Araus, J. L. (2009). Shoot δ 15N gives a better indication than ion concentration or Δ13C of genotypic differences in the response of durum wheat to salinity. Functional Plant Biology 36, 144–155.Google Scholar