Genotypic Variability in Carbon Isotope Discrimination and Water Use Efficiency among Recombinant Inbred Lines of Sunflower (Helianthus annuus L.)

Afifuddin Latif Adiredjo, Philippe Grieu


To evaluate genotypic variability in carbon isotope discrimination or CID and water use efficiency or WUE, recombinant inbred lines (RILs) population of sunflower (Helianthus annuus L.) was used. Seventy eight sunflower RILs were grown in greenhouse and 100 sunflower RILs were grown under field condition, and measured some morphological and physiological traits including leaf area at flowering (LAf), net CO2 assimilation rate (A) and transpiration per day at flowering (Ef). WUE, called “potential” WUE (WUEp), was calculated as the ratio of assimilation potential (Ap) to transpiration per day at flowering (Ef) where Ap was derived from the multiplication of A with LAf. The CID was significantly varied among RILs and there was significant negative genetic correlation between CID and WUEp. Heritability of the CID was higher rather than the WUEp which reflected wide genetic variability of CID. The genetic correlation between CID and WUEp and the wide genotypic variability of CID indicated that CID can be proposed as an indicator to determine WUE in sunflower and open a way in understanding the genetic diversity of the RILs which could be used as a basic consideration before applying selection program in sunflower breeding.


CID; Genotypic variability; Sunflower; WUE

Full Text:



Adiredjo, A. L., Navaud, O., Lamaze, T., & Grieu, P. (2014). Leaf carbon isotope discrimination as an accurate indicator of water-use efficiency in sunflower genotypes subjected to five stable soil water contents. Journal of Agronomy and Crop Science, 200(6), 416–424. crossref

Adiredjo, A. L., Navaud, O., Muños, S., Langlade, N. B., Lamaze, T., & Grieu, P. (2014). Genetic control of water use efficiency and leaf carbon isotope discrimination in sunflower (Helianthus annuus L.) subjected to two drought scenarios. PLoS One, 9(7), e101218. crossref

Åkesson, M., Bensch, S., Hasselquist, D., Tarka, M., Hansson, B., Akesson, M., … Hansson, B. (2008). Estimating heritabilities and genetic correlations: Comparing the “animal model” with parent-offspring regression using data from a natural population. PloS One, 3(3), e1739. crossref

Allinne, C., Maury, P., Sarrafi, A., & Grieu, P. (2009). Genetic control of physiological traits associated to low temperature growth in sunflower under early sowing conditions. Plant Science, 177(4), 349–359. crossref

Alza, J. O., & Fernández-Martínez, J. M. (1997). Genetic analysis of yield and related traits in sunflower (Helianthus annuus L.) in dryland and irrigated environments. Euphytica, 95(2), 243–251. crossref

Anyia, A. O., Slaski, J. ., Nyachiro, J. M., Archambault, D. J., & Juskiw, P. (2007). Relationship of carbon isotope discrimination to water use efficiency and productivity of barley under field and greenhouse conditions. Journal of Agronomy and Crop Science, 193, 313–323. crossref

Barbour, M. M., Warren, C. R., Farquhar, G. D., Forrester, G., & Brown, H. (2010). Variability in mesophyll conductance between barley genotypes, and effects on transpiration efficiency and carbon isotope discrimination. Plant, Cell and Environment, 33(7), 1176–1185. crossref

Blum, A. (1983). Genetic and physiological relationships in plant breeding for drought resistance. Agricultural Water Management, 7(1–3), 195-205. crossref

Brendel, O., Le Thiec, D., Scotti-Saintagne, C., Bod้n่s, C., Kremer, A., & Guehl, J. M. (2008). Quantitative trait loci controlling water use efficiency and related traits in Quercus robur L. Trees Genetics & Genomes, 4(2), 263–278. crossref

Brugnoli, E., Hubick, K. T., von Caemmerer, S., Wong, S. C., & Farquhar, G. D. (1988). Correlation between the carbon isotope discrimination in leaf starch and sugars of C(3) plants and the ratio of intercellular and atmospheric partial pressures of carbon dioxide. Plant Physiology, 88(4), 1418–24. crossref

Carelli, M. L. C., Fahl, J. I., Trivelin, P. C. O., & Queiroz-Voltan, R. B. (1999). Carbon isotope discrimination and gas exchange in Coffea species grown under different irradiance regimes. Revista Brasileira de Fisiologia Vegetal, 11(2), 63–68. Retrieved from website

Centritto, M., Lauteri, M., Monteverdi, M. C., & Serraj, R. (2009). Leaf gas exchange, carbon isotope discrimination, and grain yield in contrasting rice genotypes subjected to water deficits during the reproductive stage. Journal of Experimental Botany, 60(8), 2325–2339. crossref

Cernusak, L. A., Arthur, D. J., Pate, J. S., & Farquhar, G. D. (2003). Water relations link carbon and oxygen isotope discrimination to phloem sap sugar concentration in Eucalyptus globulus. Plant Physiology, 131(4), 1544–1554. crossref

Chen, J., Chang, S. X., & Anyia, A. O. (2011). Gene discovery in cereals through quantitative trait loci and expression analysis in water-use efficiency measured by carbon isotope discrimination. Plant, Cell and Environment, 34(12), 2009–2023. crossref

Chen, J., Chang, S. X., & Anyia, A. O. (2012). Quantitative trait loci for water-use efficiency in barley (Hordeum vulgare L.) measured by carbon isotope discrimination under rain-fed conditions on the Canadian Prairies. Theoretical and Applied Genetics, 125(1), 71–90. crossref

Chen, X., Zhang, Y., Zu, Y., Yang, L., Lu, Q., & Wang, W. (2014). Antioxidant effects of rosemary extracts on sunflower oil compared with synthetic antioxidants. International Journal of Food Science and Technology, 49(2), 385–391. crossref

Comstock, J. P. (2002). Hydraulic and chemical signalling in the control of stomatal conductance and transpiration. Journal of Experimental Botany, 53(367), 195–200. crossref

Condon, A. G., Richards, R. A., Rebetzke, G. J., & Farquhar, G. D. (2002). Improving intrinsic water-use efficiency and crop yield. Crop Science, 42(1), 122–131. crossref

Condon, A. G., Richards, R. A., Rebetzke, G. J., & Farquhar, G. D. (2004). Breeding for high water-use efficiency. Journal of Experimental Botany, 55(407), 2447–2460. crossref

De Miguel, M., Sánchez-Gómez, D., Cervera, M. T., & Aranda, I. (2012). Functional and genetic characterization of gas exchange and intrinsic water use efficiency in a full-sib family of Pinus pinaster Ait. in response to drought. Tree Physiology, 32(1), 94–103. crossref

Ebdon, J. S., & Kopp, K. L. (2004). Relationships between water use efficiency, carbon isotope discrimination, and turf performance in genotypes of Kentucky bluegrass during drought. Crop Science, 44(5), 1754–1762. crossref

Ehdaie, B., & Waines, J. G. (1994). Genetic analysis of carbon isotope discrimination and agronomic characters in a bread wheat cross. Theoretical and Applied Genetics, 88(8), 1023–8. crossref

Evett, S. R., & Tolk, J. A. (2009). Introduction: Can water use efficiency be modeled well enough to impact crop management? Agronomy Journal, 101(3), 423–425. crossref

Farquhar, G. D., Ehleringer, J. R., & Hubick, K. T. (1989). Carbon isotope discrimination and photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology, 40(1), 503–537. crossref

Flagella, Z., Rotunno, T., Tarantino, E., Di Caterina, R., & De Caro, A. (2002). Changes in seed yield and oil fatty acid composition of high oleic sunflower (Helianthus annuus L.) hybrids in relation to the sowing date and the water regime. European Journal of Agronomy, 17(3), 221–230. crossref

Frank, A. B., & Berdahl, J. D. (2001). Gas exchange and water relations in diploid and tetraploid Russian wildrye. Crop Science, 41(1), 87–92. crossref

González-Martínez, S. C., Huber, D., Ersoz, E., Davis, J. M., & Neale, D. B. (2008). Association genetics in Pinus taeda L. II. Carbon isotope discrimination. Heredity, 101(1), 19–26. crossref

Gunstone, F. D. (2013). Sunflower seed and oil. Lipid Technology, 25(1), 24. crossref

Jackson, P., Robertson, M., Cooper, M., & Hammer, G. (1996). The role of physiological understanding in plant breeding; From a breeding perspective. Field Crops Research, 49(1), 11–37. crossref

Johnson, M. T. J., Agrawal, A. A., Maron, J. L., & Salminen, J. P. (2009). Heritability, covariation and natural selection on 24 traits of common evening primrose (Oenothera biennis) from a field experiment. Journal of Evolutionary Biology, 22(6), 1296–1307. crossref

Jones, M. B. (1993). Plant microclimate. In: D. O. Hall, J. M. O. Scurlock, H. R. Bolhàr-Nordenkampf, R. C. Leegood, S. P. Long (Eds.), Photosynthesis and production in a changing environment (pp. 47-64). Dordrecht, NL: Springer.

Kearsey, M. J., & Pooni, H. S. (1998). The genetical analysis of quantitative traits. Cheltenham, UK: Stanley Thornes (Publishers) Ltd.

Kiani, S. P., Grieu, P., Maury, P., Hewezi, T., Gentzbittel, L., & Sarrafi, A. (2007). Genetic variability for physiological traits under drought conditions and differential expression of water stress-associated genes in sunflower (Helianthus annuus L.). Theoretical and Applied Genetics, 114(2), 193–207. crossref

Kiani, S. P., Maury, P., Nouri, L., Ykhlef, N., Grieu, P., & Sarrafi, A. (2009). QTL analysis of yield-related traits in sunflower under different water treatments. Plant Breeding, 128(4), 363–373. crossref

Kumar, S., & Singh, B. (2009). Effect of water stress on carbon isotope discrimination and Rubisco activity in bread and durum wheat genotypes. Physiology and Molecular Biology of Plants, 15(3), 281–6. crossref

Lambrides, C. J., Chapman, S. C., & Shorter, R. (2004). Genetic variation for carbon isotope discrimination in sunflower: Association with transpiration efficiency and evidence for cytoplasmic inheritance. Crop Science, 44(5), 1642–1653. crossref

Marguerit, E., Brendel, O., Lebon, E., Van Leeuwen, C., & Ollat, N. (2012). Rootstock control of scion transpiration and its acclimation to water deficit are controlled by different genes. New Phytologist, 194(2), 416-29. crossref

Messina, C. D., Podlich, D., Dong, Z., Samples, M., & Cooper, M. (2011). Yield-trait performance landscapes: From theory to application in breeding maize for drought tolerance. Journal of Experimental Botany, 62(3), 855–868. crossref

Mian, M. A. R., Ashley, D. A., & Boerma, H. R. (1998). An additional QTL for water use efficiency in soybean. Crop Science, 38(2), 390–393. crossref

Pinheiro, H. A., DaMatta, F. M., Chaves, A. R. M., Loureiro, M. E., & Ducatti, C. (2005). Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. Annals of Botany, 96(1), 101–108. crossref

Rajabi, A., Ober, E. S., & Griffiths, H. (2009). Genotypic variation for water use efficiency, carbon isotope discrimination, and potential surrogate measures in sugar beet. Field Crops Research, 112(2–3), 172–181. crossref

Rauf, S. (2008). Breeding sunflower (Helianthus annuus L.) for drought tolerance*. Communications in Biometry and Crop Science, 3(31), 29–44. Retrieved from website

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(1), 123–137. crossref

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(3), 739–745. crossref

Rengel, D., Arribat, S., Maury, P., Martin-Magniette, M. L., Hourlier, T., Laporte, M., … Langlade, N. B. (2012). A gene-phenotype network based on genetic variability for drought responses reveals key physiological processes in controlled and natural environments. PLoS One, 7(10), e45249. crossref

Richards, R. A., Rebetzke, G. J., Condon, A. G., & van Herwaarden, A. F. (2002). Crop physiology & metabolism - breeding opportunities for increasing the efficiency of water use and crop yield in temperate cereals. Crop Science, 42(1), 111–121. crossref

Richards, R. A., Rebetzke, G. J., Watt, M., Condon, A. G., Spielmeyer, W., & Dolferus, R. (2010). Breeding for improved water productivity in temperate cereals: Phenotyping, quantitative trait loci, markers and the selection environment. Functional Plant Biology, 37(2), 85–97. crossref

Serraj, R. (2006). Improving crop water use efficiency using carbon isotope discrimination. Retrieved from website

Singh, R. K., & Chaudhary, B. D. (1977). Biometrical methods in quantitative genetic analysis. New Delhi, IN: Kalyani Publishers.

Singh, S. K., & Reddy, K. R. (2011). Regulation of photosynthesis, fluorescence, stomatal conductance and water-use efficiency of cowpea (Vigna unguiculata [L.] Walp.) under drought. Journal of Photochemistry and Photobiology B: Biology, 105(1), 40–50. crossref

Sternberg, P. (2012). Physiological and morphological basis for differences in growth, water use and drought resistance among Cercis L. Taxa (Doctoral dissertation). Retrieved from website

Stiller, W. N., Read, J. J., Constable, G. A., & Reid, P. E. (2005). Selection for water use efficiency traits in a cotton breeding program: Cultivar differences. Crop Science, 45(3), 1107–1113. crossref

Tardieu, F., & Simonneau, T. (1998). Variability among species of stomatal control under fluctuating soil water status and evaporative demand: Modelling isohydric and anisohydric behaviours. Journal of Experimental Botany, 49(Special), 419–432. crossref

Tardieu, F., & Tuberosa, R. (2010). Dissection and modelling of abiotic stress tolerance in plants. Current Opinion in Plant Biology, 13(2), 206–212. crossref

This, D., Comstock, J., Courtois, B., Xu, Y., Ahmadi, N., Vonhof, W. M., … McCouch, S. (2010). Genetic analysis of water use efficiency in rice (Oryza sativa L.) at the leaf level. Rice, 3(1), 72–86. crossref

Virgona, J. M., & Farquhar, G. D. (1996). Genotypic variation in relative growth rate and carbon isotope discrimination in sunflower is related to photosynthetic capacity. Australian Journal of Plant Physiology, 23(2), 227–236. crossref

White, C. A. (2011). Increasing the water use efficiency (WUE) of tomato (S. lycopersicum) via manipulation of the abscisic acid (ABA) biosynthesis pathway (PhD thesis). Retrieved from Nottingham eTheses. website

Zhao, B., Kondo, M., Maeda, M., Ozaki, Y., & Zhang, J. (2004). Water-use efficiency and carbon isotope discrimination in two cultivars of upland rice during different developmental stages under three water regimes. Plant and Soil, 261(1–2), 61–75. crossref

Zhu, L., Li, S. H., Liang, Z. S., Xu, X., & Li, Y. (2010). Relationship between carbon isotope discrimination, mineral content and gas exchange parameters in vegetative organs of wheat grown under three different water regimes. Journal of Agronomy and Crop Science, 196(3), 175–184. crossref


Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.