Genetic variation in seedling water-use efficiency of Patagonian Cypress populations from contrasting precipitation regimes assessed through carbon isotope discrimination

M. J. Pastorino, A. G. Aparicio, P. Marchelli, L. A. Gallo


Water-use efficiency (WUE) is a physiological parameter that plays a significant role in the evolutionary dynamics of many forest tree species. It can be estimated indirectly through carbon isotope discrimination (Δ). In general, plants of more arid origins have lower values of Δ. In order to study the degree of genetic control of this parameter and the genetic variation in Δ of Patagonian Cypress seedlings, three Argentinean natural populations chosen to represent two contrasting precipitation regimes were sampled in a common garden trial. The dry situation was represented by two neighboring marginal forest patches from the steppe, while the humid condition was represented by a population with 1,200 mm higher mean annual precipitation. Height (H) and Δ were measured in 246 five-year-old seedlings from 41 open-pollinated families. The factor ‘family’ had a significant effect on both variables; however heritability for Δ was found not to be significant in two out of the three populations. This could be explained by low sample size in one of them and by a real evolutionary effect in the other. An inverse association between H and Δ was verified, which is interpreted as evidence of an adaptation process at the intra-population level. The studied populations were not shown to discriminate carbon isotopes differently; hence evidence of adaptation to current environmental conditions could not be obtained. On the other hand, the arid populations proved to be quite different in terms of genetic variation, which seems to be the consequence of genetic drift and isolation.

Full Text:



Aparicio A.G., Pastorino M.J., Gallo L.A., 2010. Genetic variation of early height growth traits at the xeric limits of Austrocedrus chilensis (Cupressaceae). Austral Ecol 35, 825-836.

Aparicio A.G., Zuki S., Pastorino M.J., Martinez-Meier A., Gallo L.A., in press. Heritable variation in the survival of seedlings from Patagonian cypress marginal xeric populations coping with drought and extreme cold. Tree Genet Genomes.

Arana M.V., Gallo L.A., Vendramin G.G., Pastorino M.J., Sebastiani F., Marchelli P., 2010. High genetic variation in marginal fragmented populations at extreme climatic conditions of the Patagonian Cypress Austrocedrus chilensis. Mol Phylogenet Evol 54, 941-949.

Aranda I., Alía R., Ortega U., Dantas Â.K., Majada J., 2010. Intra-specific variability in biomass partitioning and carbon isotopic discrimination under moderate drought stress in seedlings from four Pinus pinaster populations. Tree Genet Genomes 6, 169-178.

Berry S.C., Varney G.T., Flanagan L.B., 1997. Leaf δ13C in Pinus resinosa trees and understory plants: variation associated with light and CO2 gradients. Oecologia 109, 499-506.

Bonhomme L., Barbaroux C., Monclus R., Morabito D., Berthelot A., Villar M., Dreyer E., Brignolas F., 2008. Genetic variation in productivity, leaf traits and carbon isotope discrimination in hybrid poplars cultivated on contrasting sites. Ann For Sci 65, 503-512.

Brendel O., 2001. Does bulk-needle delta C-13 reflect shortterm discrimination? Ann For Sci 58, 135–141.

Brendel O., Pot D., Plomion C., Rozenberg P., Guehl J.-M., 2002. Genetic parameters and QTL analysis of δ13C and ring width in maritime pine. Plant Cell Environ 25, 945-953.

Conifer Specialist Group, 1998. Austrocedrus chilensis. In: IUCN 2006. 2006 IUCN Red List of Threatened Species,, downloaded on 31 August 2007.

Constantino I.N., 1949. Parcelas experimentales permanentes. Libocedrus chilensis (Don) Endl. Min. Agric. y Ganadería, Publ. Técn. Nº 13, Buenos Aires.

Constantino I.N., 1958. Primeros resultados de las parcelas permanentes de Libocedrus chilensis. Rev Fac Agron La Plata 34, 131-159.

Falconer D.S., Mackay T.F., 1996. Introduction to Quantitative Genetics. Longman, Harlow, Essex, England. 464 pp.

Farquhar G.D., O’Leary M.H., Berry J.A., 1982. On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Aust J Plant Physiol 9, 121-137.

Farquhar G.D., O’Leary M.H., Condon A.G., Richards R.A., 1989. Carbon isotope fractionation and plant water-use efficiency. In: Stable Isotopes in Ecological Research (Rundel P.W., Ehleringer J.R., Nagy K.A., eds). Springer Verlag, Berlin, pp. 21-40.

Farquhar G.D., Richards P.A., 1984. Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Aust J Plant Physiol 11, 539-552.

Gallo L.A., 1996. Reforestación con cipreses. Presencia 39, 20-21.

Gallo L.A., Pastorino M.J., 2010. Evidence of genetic drift in neutral and adaptive genome. In: Evoltree Conference “Forest Ecosystem Genomics and Adaptation”. San Lorenzo de El Escorial, Madrid, 9-11 June 2010.

Goya J.P., Ferrando J.J., Bocos D.A., Yapura P.F., 1995. Estructura y desarrollo de un rodal coetáneo de Austrocedrus chilensis en El Bolsón, Río Negro, Argentina. Rev Fac Agron La Plata 71, 165-171.

Guy R.D., Holowachuk D.L., 1993. Population differences in carbon isotope discrimination in lodgepole pine. Plant Physiol 102 (Suppl.), 89.

Gyenge J.E., Fernández M.E., Dalla Salda G., Schlichter T., 2005. Leaf and whole-plant water relations of the Patagonian conifer Autrocedrus chilensis (D.Don) Pic. Ser. Et Bizzarri: implications on its drought resistance capacity. Ann For Sci 62, 297-302.

Gyenge J.E., Fernández M.E., Schlichter T., 2007. Influence of radiation and drought on gas exchange of Austrocedrus chilensis seedlings. Bosque 28, 220-225.

Gyenge J.E., Fernández M.E., Schlichter T., 2008. Are differences in productivity between native and exotic trees in N.W. Patagonia related to differences in hydraulic conductance? Trees 22, 483-490.

Houle D., 1992. Comparing evolvability and variability of quantitative traits. Genetics 130, 195-204.
PMid:1732160 PMCid:1204793

Johnsen K.H., Flanagan L.B., Huber D.A., Major J.E., 1999. Genetic variation in growth, carbon isotope discrimination, and foliar N concentration in Picea mariana: analyses from a half-diallel mating design using field-grown trees. Can J For Res 29, 1727-1735.

Lauteri M., Pliura A., Monteverdi M.C., Brugnoli E., Villani F., Eriksson G., 2004. Genetic variation in carbon isotope discrimination in six European populations of Castanea sativa Mill. originating from contrasting localities. J Evol Biol 17, 1286-1296.

Loguercio G.A., Buduba C., La Manna L., 2005. Plantación de ciprés de la cordillera de 57 años de edad: una experiencia en el Parque Nac. Los Alerces. Patagonia Forestal 11(1), 7-8.

Lynch M., Walsh B., 1998. Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MA, USA. 980 pp.

Olivas-García J.M., Cregg B.M., Hennessey T.C., 2000. Genotypic variation in carbon isotope discrimination and gas exchange of ponderosa pine seedlings under two levels of water stress. Can J For Res 30, 1581-1590.

O’Neill G., Adams T.W., Aitken S.N., 2001. Quantitative genetics of spring and fall cold hardiness in seedlings from two Oregon populations of coastal Douglas-fir. For Ecol Manage 149, 305–318.

Oudkerk L., Pastorino M.J., Gallo L.A., 2003. Siete años de experiencia en la restauración postincendio de un bosque de Ciprés de la Cordillera. Patagonia Forestal 9, 4-7.

Pastorino M.J., Gallo L.A., 2006. Mating system in a lowdensity natural population of the dioecious wind-pollinated Patagonian Cypress. Genetica 126, 315-321.

Pastorino M.J., Gallo L.A., 2009. Preliminary operational genetic management units of a highly fragmented forest tree species of southern South America. For Ecol Manage 257, 2350-2358.

Pastorino M.J., Ghirardi S., Grosfeld J., Gallo L.A., Puntieri J.G., 2010. Genetic variation in architectural seedling traits of Patagonian Cypress natural populations from the extremes of a precipitation range. Ann For Sci 67, 508-518.

Pennington R.E., Tischler C.R., Johnson H.B., Polley H.W., 1999. Genetic variation for carbon isotope composition in honey mesquite (Prosopis glandulosa). Tree Physiol 19, 583-589.

Prasolova N.V., Xu Z.H., Farquhar G.D., Saffigna P.G., Dieters M.J., 2000. Variation in branchlet δ13C in relation to branchlet nitrogen concentration and growth in 8-year-old hoop pine families (Araucaria cunninghamii) in subtropical Australia. Tree Physiol 20, 1049-1055.

Prasolova N.V., Xu Z.H., Lundkvist K., Farquhar G.D., Dieters M.J., Walker S., Saffigna P.G., 2003. Genetic variation in foliar carbon isotope composition in relation to tree growth and foliar nitrogen concentration in clones of the F1 hybrid between slash pine and Caribbean pine. For Ecol Manage 172, 145-160.

R Development Core Team, 2009. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051- 07-0, URL

Read J., Farquhar G.D., 1991. Comparative studies in Nothofagus (Fagaceae). I. Leaf carbon isotope discrimination. Funct Ecol 5, 684-695.

Ritland K., 2002. Extensions of models for the estimation of mating systems using n independent loci. Heredity 88, 221–228.

Rovere A.E., 2008. Restauración de Bosque Andino-Patagónico con Austrocedrus chilensis URL:

Spitze K., 1993. Population structure in Daphnia obtusa: quantitative genetic and allozyme variation. Genetics 135, 367-374.
PMid:8244001 PMCid:1205642

Sun Z.J., Livingston N.J., Guy R.D., Ethier G.J., 1996. Stable carbon isotopes as indicators of increased water-use efficiency and productivity in white spruce (Picea glauca (Moench) Voss) seedlings. Plant Cell Environ 19, 887-894.

Wright J.W., 1976. Introduction to forest genetics. Academic Press, New York, San Francisco, London. 463 pp.

Xu Z., Prasolova N., Lundkvist K., Beadle C., Leaman T., 2003. Genetic variation in branchlet carbon and nitrogen isotope composition and nutrient concentration of 11-yearold hoop pine families in relation to tree growth in subtropical Australia. For Ecol Manage 186, 359-371.

Zhang J., Fins L., Marshall J.D., 1994. Stable carbon isotope discrimination, photosynthetic gas exchange, and growth differences among western larch families. Tree Physiol 14, 531-539.

Zhang J., Marshall J.D., 1994. Population differences in water-use efficiency of well-watered and water-stressed western larch seedlings. Can J For Res 24, 92-99.

Zhang J., Marshall J.D., Jaquish B.C., 1993. Genetic differentiation in carbon isotope discrimination and gas exchange in Pseudotsuga menziessi. Oecologia 93, 80-87.

Zhang J., Marshall J.D., Jaquish B.C., 1995. Genetic differentiation in carbon isotope discrimination and gas exchange in Pseudotsuga menziessi (erratum). Oecologia 101, 132.

Zhang X., Zang R., Li C., 2004. Population differences in physiological and morphological adaptations of Populus davidiana seedlings in response to progressive drought stress. Plant Sci 166, 791–797.

DOI: 10.5424/fs/2012212-02272