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Intra-specific variability in biomass partitioning and carbon isotopic discrimination under moderate drought stress in seedlings from four Pinus pinaster populations

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Abstract

The response to drought of 20 open-pollinated families from four Pinus pinaster Ait. populations covering a latitudinal cline (France, Central and Southern Spain, and Morocco) was assessed. The seedlings were cultivated in a greenhouse under controlled temperature and vapor pressure deficit for 120 days, and subjected to two watering regimes for 60 days. Different biomass partitioning variables, pre-dawn water potential, and isotopic discrimination of 13C in needles (Δ) as surrogate of long-term water use efficiency were estimated for each seedling at the end of the experiment. In response to the imposed drought, there was no change in the root biomass partitioning, but the overall Δ values decreased in response to water stress. All the families of the population from Morocco showed the highest investment in roots, regardless of the watering regime imposed. Inter-family differences within populations were also significant for most parameters as confirmed by the heritability values estimated (higher under the well-watered treatment). The studied P. pinaster populations showed different strategies of response to drought. This may represent an important mechanism by local populations in facing future climatic change. The results could be of value in forest conservation and breeding programs of maritime pine in the future.

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References

  • Abrams MD (1994) Genotypic and phenotypic variation as stress adaptations in temperate tree species: a review of several case studies. Tree Physiol 14:833–842

    PubMed  Google Scholar 

  • Abrams MD, Kubiske ME, Steiner KC (1990) Drought adaptations and responses in five genotypes of Fraxinus pennsylvanica Marsh: photosynthesis, water relations and leaf morphology. Tree Physiol 6:305–315

    PubMed  Google Scholar 

  • Aitken SN, Kavanagh KL, Yoder BJ (1995) Genetic variation in seedling water-use efficiency as estimated by carbon isotope ratios and its relationship to sapling growth in Douglas-fir. For Genet 2:199–206

    Google Scholar 

  • Alia R, Gil L, Pardos JA (1995) Performance of 43 Pinus-Pinaster Ait provenances on 5 locations in Central Spain. Silvae Genet 44:75–81

    Google Scholar 

  • Alia R, Moro J, Denis JB (1997) Performance of Pinus pinaster provenances in Spain: interpretation of the genotype by environment interaction. Can J For Res 27:1548–1559

    Article  Google Scholar 

  • Ares A, Fownes JH, Sun W (2000) Genetic differentiation of intrinsic water-use efficiency in the Hawaiian native Acacia koa. Int J Plant Sci 161:909–915

    Article  Google Scholar 

  • Aspelmeier S, Leuschner C (2004) Genotypic variation in drought response of silver birch (Betula pendula): leaf water status and carbon gain. Tree Physiol 24:517–528

    CAS  PubMed  Google Scholar 

  • Aspelmeier S, Leuschner C (2006) Genotypic variation in drought response of silver birch (Betula pendula Roth): leaf and root morphology and carbon partitioning. Trees 20:42–52

    Article  Google Scholar 

  • Benowicz A, Guy RD, El-Kassaby YA (2000) Geographic pattern of genetic variation in photosynthetic capacity and growth in two hardwood species from British Columbia. Oecologia 123:168–174

    Article  Google Scholar 

  • Brendel O (2001) Does bulk-needle delta C-13 reflect short-term discrimination? Ann For Sci 58:135–141

    Article  Google Scholar 

  • Brendel O, Pot D, Plomion C, Rozenberg P, Guehl JM (2002) Genetic parameters and QTL analysis of d13C and ring width in maritime pine. Plant Cell Environ 25:945–953

    Article  CAS  Google Scholar 

  • Bucci G, Gonzalez-Martinez SC, Le Provost G, Plomion C, Ribeiro MM, Sebastiani F, Alía R, Vendramin GG (2007) Range-wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers. Mol Ecol 16:2137–2153

    Article  CAS  PubMed  Google Scholar 

  • Burban C, Petit RJ (2003) Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Mol Ecol 8:1487–1495

    Article  Google Scholar 

  • Chambel MR, Climent J, Alia R (2007) Divergence among species and populations of Mediterranean pines in biomass allocation of seedlings grown under two watering regimes. Ann For Sci 64:87–97

    Article  Google Scholar 

  • Correia I, Almeida MH, Aguiar A, Alía R, David TS, Pereira JS (2008) Variations in growth, survival and carbon isotope composition (δ13C) among Pinus pinaster populations of different geographic origins. Tree Physiol 28:1545–1552

    PubMed  Google Scholar 

  • Cregg BM (1993) Seed-source variation in water relations, gas exchange, and needle morphology of mature ponderosa pine trees. Can J For Res 23:749–755

    Article  Google Scholar 

  • Cregg BM, Olivas-Garcia JM, Hennessey TC (2000) Provenance variation in carbon isotope discrimination of mature ponderosa pine trees at two locations in the Great Plains. Can J For Res 30:428–439

    Article  Google Scholar 

  • Danjon F (1994) Stand features and height growth in a 36-year-old maritime pine (Pinus pinaster Ait) provenance test. Silvae Genet 43:52–62

    Google Scholar 

  • de Lucas AI, Robledo-Arnuncio JJ, Hidalgo E, González-Martínez S (2008) Mating system and pollen gene flow in Mediterranean maritime pine. Heredity 100:390–399

    Article  CAS  Google Scholar 

  • Derory J, Mariette S, Gonzalez-Martinez SC, Chagne D, Madur D, Gerber S, Brach J, Persyn F, Ribeiro MM, Plomion C (2002) What can nuclear microsatellites tell us about maritime pine genetic resources conservation and provenance certification strategies? Ann For Sci 59:699–708

    Article  Google Scholar 

  • Ducrey M, Huc R, Ladjal M, Guehl JM (2008) Variability in growth, carbon isotope composition, leaf gas exchange and hydraulic traits in the eastern Mediterranean cedars Cedrus libani and C. brevifolia. Tree Physiol 28:689–701

    CAS  PubMed  Google Scholar 

  • Dudley SA (1996) Differing selection on plant physiological traits in response to water availability: a test of adaptive hypothesis. Evolution 50:92–102

    Article  Google Scholar 

  • Eveno E, Collada C, Guevara MA, Léger V, Soto A, Díaz L, Léger P, González-Martínez SC, Cervera MT, Plomion C, Garnier-Géré P (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Mol Biol Evol 25:417–437

    Article  CAS  PubMed  Google Scholar 

  • Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Ann Rev Plant Physiol Mol Biol 40:503–537

    Article  CAS  Google Scholar 

  • Fernández M, Gil L, Pardos JA (2000) Effects of water supply on gas exchange in Pinus pinaster Ait. provenances during their first growing season. Ann For Sci 57:9–16

    Article  Google Scholar 

  • Fernández M, Novillo C, Pardos JA (2006) Effects of water and nutrient availability in Pinus pinaster Ait. Open pollinated families at an early age: growth, gas exchange and water relations. New For 31:321–342

    Google Scholar 

  • Flanagan LB, Johnsen KH (1995) Genetic variation in carbon isotope discrimination and its relationship to growth under field conditions in full-sib families of Picea mariana. Can J For Res 25:39–47

    Article  Google Scholar 

  • Franco AC, Duarte HM, Gessler A, de Mattos EA, Nahm M, Rennenberg H, Ribeiro K, Scarano F, Luttge U (2005) In situ measurements of carbon and nitrogen distribution and composition, photochemical efficiency and stable isotope ratios in Araucaria angustifolia. Trees 19:422–430

    Article  CAS  Google Scholar 

  • Gaspar MJ, de-Lucas AI, Alía R, Paiva JAP, Hidalgo E, Louzada J, Almeida H, González-Martínez SC (2009) Use of molecular markers for estimating breeding parameters: a case study in a Pinus pinaster Ait. progeny trial. TGG 5:609–616

  • Gilmour AR, Cullis BR, Welham SJ, Thompson R (2001) ASREML Reference Manual. NSW Agriculture, Orange

    Google Scholar 

  • Gonzalez-Martinez SC, Mariette S, Ribeiro MM, Burban C, Raffin A, Chambel MR, Ribeiro CAM, Aguiar A, Plomion C, Alia R, Gil L, Vendramin GG, Kremer A (2004) Genetic resources in maritime pine (Pinus pinaster Aiton): molecular and quantitative measures of genetic variation and differentiation among maternal lineages. For Ecol Manage 197:103–115

    Article  Google Scholar 

  • González-Martinez SC, Burczyk J, Nathan R, Nanos N, Gil L, Alía R (2006) Effective gene dispersal and female reproductive success in Mediterranean maritime pine (Pinus pinaster Aiton). Mol Ecol 15:4577–4588

    Article  PubMed  Google Scholar 

  • González-Martínez SC, Alía R, Gil L (2002) Population genetic structure in a Mediterranean pine (Pinus pinaster Ait.): a comparison of allozyme markers and quantitative traits. Heredity 89:199–206

    Article  PubMed  CAS  Google Scholar 

  • Granier A, Loustau D (1994) Measuring and modelling the transpiration of maritime pine canopy from sap flow data. Agric For Meteorol 71:61–81

    Article  Google Scholar 

  • Grossnickle SC, Fan SH, Russell JH (2005) Variation in gas exchange and water use efficiency patterns among populations of western red cedar. Trees 19:32–42

    Article  Google Scholar 

  • Guehl JM, Fort C, Ferhi A (1995) Differential response of leaf conductance, carbon-isotope discrimination and water-use efficiency to nitrogen deficiency in maritime pine and pedunculate oak plants. New Phytol 131:149–157

    Article  Google Scholar 

  • Guy RD, Holowachuk DL (2001) Population differences in stable carbon isotope ratio of Pinus contorta Dougl. ex Loud.: relationship to environment, climate of origin, and growth potential. Can J Bot 79:274–283

    Article  Google Scholar 

  • Guyon JP, Kremer A (1982) Stabilité phénotypique de la croissance en hauteur et cinétique journalière de la pression de sève et de la transpiration chez le pin maritime (Pinus pinaster Ait.). Can J For Res 12:936–946

    Article  Google Scholar 

  • Howe GT, Aitken SN, Neale DB, Jermstad KD, Wheeler NC, Chen THH (2003) From genotype to phenotype: unraveling the complexities of cold adaptation in forest trees. Can J Bot 81(12):1247–1266

    Article  CAS  Google Scholar 

  • Ibrahim L, Proe MF, Cameron AD (1997) Main effects of nitrogen supply and drought stress upon whole-plant carbon allocation in poplar. Can J For Res 27:1413–1419

    Article  Google Scholar 

  • Joslin JD, Wolfe MH, Hanson PJ (2000) Effects of altered water regimes on forest root systems. New Phytol 147:117–129

    Article  Google Scholar 

  • Laureti M, Scartazza A, Guido MC, Brugnoli E (1997) Genetic variation in photosynthetic capacity, carbon isotope discrimination and mesophyll conductance in provenances of Castanea sativa adapted to different environments. Funct Ecol 11:675–683

    Article  Google Scholar 

  • Malausa T, Guillemaud T, Lapchin L (2005) Combining genetic variation and phenotypic plasticity in trade-off modelling. Oikos 110:330–338

    Article  Google Scholar 

  • Monclus R, Dreyer E, Delmotte FM, Villar M, Delay D, Boudouresque E, Petit J-M, Marron N, Bréchet C, Brignolas F (2005) Productivity, leaf traits and carbon isotope discrimination in 29 Populus deltoides × P. nigra clones. Plant Cell Environ 167:53–62

    Google Scholar 

  • Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit J-M, Barbaroux C, Le TD, Bréchet C, Brignolas F (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides × Populus nigra. Plant Cell Environ 169:765–777

    Google Scholar 

  • Nguyen A, Lamant A (1989) Variation in growth and osmotic regulation of roots of water-stressed maritime pine (Pinus pinaster Ait.) provenances. Tree Physiol 5:123–133

    PubMed  Google Scholar 

  • Nguyen-Queyrens A, Ferhi A, Loustau D, Guehl JM (1998) Within-ring delta C-13 spatial variability and interannual variations in wood cellulose of two contrasting provenances of Pinus pinaster. Can J For Res 28:766–773

    Article  Google Scholar 

  • Osório J, Osório ML, Chaves MM, Pereira JS (1998) Water deficits are more important in delaying growth than in changing patterns of carbon allocation in Eucalyptus globulus. Tree Physiol 18:363–373

    PubMed  Google Scholar 

  • Palmroth S, Berninger F, Nikinmaa E, Lloyd J, Pulkkinen P, Hari P (1999) Structural adaptation rather than water conservation was observed in Scots pine over a range of wet to dry climates. Oecologia 121:302–309

    Article  Google Scholar 

  • Picon C, Guehl JM, Ferhi A (1996) Leaf gas exchange and carbon isotope composition responses to drought in a drought-avoiding (Pinus pinaster) and a drought-tolerant (Quercus petraea) species under present and elevated atmospheric CO2 concentrations. Plant Cell Environ 19:182–190

    Article  Google Scholar 

  • Pigliucci M, Preston K (2004) Phenotypic integration. Studying the ecology and evolution of complex phenotypes. Oxford University Press, New York 464 pp

    Google Scholar 

  • Pinheiro HA, DaMatta FM, Chaves ARM, Loureiro ME, Ducatti C (2005) Drought tolerance is associated with rooting depth and stomatal control of water use in clones of Coffea canephora. Ann Bot 96:101–108

    Article  PubMed  Google Scholar 

  • Poorter H, Nagel O (2000) The role of biomass allocation in the growth response of plants to different levels of light, CO2, nutrients and water: a quantitative review. Aust J Plant Physiol 27:595–607

    Article  CAS  Google Scholar 

  • Read J, Farquhar GD (1991) Comparative studies in Nothofagus (Fagaceae). I. Leaf carbon isotope discrimination. Funct Ecol 5:684–695

    Article  Google Scholar 

  • Rehfeldt GE, Ying ChC, Spittlehouse DL, Hamilton DA (1999) Genetic response to climate in Pinus contorta: niche breadth, climate change, and reforestation. Ecol Monogr 69(3):375–407

    Google Scholar 

  • Roff DA (2001) Life history evolution. Sinauer, Sunderland

    Google Scholar 

  • Roupsard O, Joly HI, Dreyer E (1998) Variability of initial growth, water-use efficiency and carbon isotope discrimination in seedlings of Faidherbia albida (Del.) A. Chev., a multipurpose tree of semi-arid Africa. Provenance and drought effects. Ann For Sci 55:329–348

    Article  Google Scholar 

  • Salvador L, Alía R, Agúndez D, Gil L (2000) Genetic variation and migration pathways of maritime pine (Pinus pinaster Ait) in the Iberian Peninsula. Theor Appl Genet 100:89–95

    Article  Google Scholar 

  • Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Ann Rev Ecol Syst 17:667–693

    Article  Google Scholar 

  • Schulze ED, Turner NC, Nicolle D, Schumacher J (2006) Leaf and wood carbon isotope ratios, specific leaf areas and wood growth of Eucalyptus species across a rainfall gradient in Australia. Tree Physiol 26:479–492

    CAS  PubMed  Google Scholar 

  • Strauss SH, Ledig FT (1985) Seedling architecture and life history evolution in pines. Am Nat 125:702–715

    Article  Google Scholar 

  • Tognetti R, Michelozzi M, Lauteri M, Brugnoli E, Giannini R (2000) Geographic variation in growth, carbon isotope discrimination, and monoterpene composition in Pinus pinaster Ait. provenances. Can J For Res 30:1682–1690

    Article  CAS  Google Scholar 

  • Tschaplinski TJ, Tuskan GA, Gebre GM, Todd DE (1998) Drought resistance of two hybrid Populus clones grown in a large-scale plantation. Tree Physiol 16:653–658

    Google Scholar 

  • Valladares F, Gianoli E, Gomez JM (2007) Ecological limits to plant phenotypic plasticity. New Phytol 176:749–763

    Article  PubMed  Google Scholar 

  • Weng YH, Park YS, Krasowski MJ, Tosh KJ, Adams G (2008) Partitioning of genetic variance and selection efficiency for alternative vegetative deployment strategies for white spruce in Eastern Canada. Tree Genet Genomes 4:809–819

    Article  Google Scholar 

  • Wu HX (1998) Study of early selection in tree breeding: 1. Advantage of early selection through increasing selection intensity and reduction of field test size. Silvae Genet 47:146–155

    Google Scholar 

  • Zhang JW, Marshall JD (1995) Variation in carbon isotope discrimination and photosynthetic gas exchange among populations of Pseudotsuga menziessi and Pinus ponderosa in different environments. Funct Ecol 9:402–412

    Article  Google Scholar 

  • Zhang JW, Feng Z, Cregg BM, Schumann C (1997) Carbon isotopic composition, gas exchange, and growth of three populations of ponderosa pine differing in drought tolerance. Tree Physiol 17:461–466

    CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported by funding of the Projects TREESNIP-QLK3-CT2002-01973 and RTA-2007-00084-00-00. Participation of Drs. I. Aranda and R. Alia was made possible by funding of the projects PLASTOFOR-AGL2004-00536/FOR and NoE EVOLTREE. Dr. M. Cervera, Dr. S.C. González-Martínez, and Dr. M. Robson made valuable comments and improvements to the manuscript. Ernesto Alvarez provided technical support during the experiment, and Fernando del Caño, Sara Herrera, and Neila Godoy kindly helped during the harvest of seedlings.

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  1. Departamento de Sistemas y Recursos Forestales, CIFOR, Instituto Nacional de Investigación y Tecnología Agraria, Carretera de La Coruña, Km. 7.5, 28040, Madrid, Spain

    Ismael Aranda & Ricardo Alía

  2. SERIDA, Sección Forestal, Grado, Estación Experimental La Mata, 33820, Asturias, Spain

    Unai Ortega, Ângelo K. Dantas & Juan Majada

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  1. Ismael Aranda
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  2. Ricardo Alía
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  3. Unai Ortega
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  4. Ângelo K. Dantas
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  5. Juan Majada
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Correspondence to Ismael Aranda.

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Communicated by S. Aitken

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Aranda, I., Alía, R., Ortega, U. et al. Intra-specific variability in biomass partitioning and carbon isotopic discrimination under moderate drought stress in seedlings from four Pinus pinaster populations. Tree Genetics & Genomes 6, 169–178 (2010). https://doi.org/10.1007/s11295-009-0238-5

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