Abstract
Populus is a genus of fast growing trees that may be suitable as a bioenergy crop grown in short rotation, but understanding the genetic nature of yield and genotype interactions with the environment is critical in developing new high-yield genotypes for wide-scale planting. In the present study, 210 genotypes from an F2 population (Family 331; POP1) derived from a cross between Populus trichocarpa 93-968 and P. deltoides ILL-129 were grown in southern UK, central France and northern Italy. The performance of POP1, based upon first- and second-year main stem traits and biomass production, improved from northern to southern Europe. Trees at the Italian site produced the highest mean biomass ranging from 0.77 to 18.06 oven-dried tonnes (ODT) ha−1 year−1, and the UK site produced the lowest mean biomass ranging from 0.18 to 10.31 ODT ha−1 year−1. Significant genotype × environment interactions were seen despite heritability values across sites being moderate to high. Using a pseudo-testcross analysis, 37 quantitative trait loci (QTL) were identified for the maternal parent and 45 for the paternal parent for eight stem and biomass traits across the three sites. High genetic correlations between traits suggested that collocating QTL could be inferred as a single pleiotropic QTL, reducing the number of unique QTL to 23 and 24 for the maternal and paternal parent, respectively. Additive genetic effects were seen to differ significantly for eight QTL on the maternal map and 20 on the paternal map across sites. An additive main effects and multiplicative interaction analysis was carried out to obtain stability parameters for each trait. These parameters were mapped as QTL, and collocation to trait QTL was accessed. Two of the eight stability QTL collocate to trait QTL on the maternal map, and 8 of the 20 stability QTL collocate to trait QTL on the paternal map, suggesting that a regulatory gene model is prevalent over an allele sensitivity model for stem trait stability across these environments.
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Andersson A, Keskitalo J, Sjodin A, Bhalerao R, Sterky F, Wissel K, Tandre K, Aspeborg H, Moyle R, Ohmiya Y, Bhalerao R, Brunner A, Gustafsson P, Karlsson J, Lundeberg J, Nilsson O, Sandberg G, Strauss S, Sundberg B, Uhlen M, Jansson S, Nilsson P (2004) A transcriptional timetable of autumn senescence. Genome Biology 5:R24
Barigah TS, Saugier B, Mousseau M, Guittet J, Ceulemans R (1994) Photosynthesis, leaf area and productivity of 5 poplar clones during their establishment year. Ann For Sci 51:613–625
Basford KE, Cooper M (1998) Genotype × environment interactions and some considerations of their implications for wheat breeding in Australia. Aust J Agric Res 49(2):153–174
Bergez JE, Auclair D, Bouvarel L (1989) First year growth of hybrid poplar shoots from cutting or coppice origin. For Sci 35:1105–1113
Boerjan W (2005) Biotechnology and the domestication of forest trees. Curr Opin Biotechnol 16:159–166
Bradshaw HD, Stettler RF (1995) Molecular genetics of growth development in Populus. IV. Mapping QTLs with large effects on growth, form and phenology traits in a forest tree. Genetics 139:963–973
Bradshaw HD, Villar M, Watson BD, Otto KG, Stewart S, Stettler RF (1994) Molecular genetics of growth and development in Populus. III. A genetic linkage map of a hybrid poplar composed of RFLP, STS and RAPD markers. Theor Appl Genet 89:167–178
Broadmeadow MSJ, Ray D, Samuel CJA (2005) Climate change and the future for broadleaved tree species in Britain. Forestry 78:145–161
Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56
Bungart R, Huttl RF (2004) Growth dynamics and biomass accumulation of 8-year-old hybrid poplar clones in a short-rotation plantation on a clayey–sandy mining substrate with respect to plant nutrition and water budget. European Journal of Forest Research 123(2):105–115
Cannell MGR (2003) Carbon sequestration and biomass energy offset: theoretical, potential and achievable capacities globally, in Europe and the UK. Biomass Bioenergy 24(2):97–116
Cervera MT, Storme V, Ivens B, Gusmão J, Liu BH, Hostyn V, Van Slycken J, Van Montagu M, Boerjan W (2001) Dense genetic linkage maps of three Populus species (Populus deltoides, P. nigra and P. trichocarpa) based on AFLP and microsatellite markers. Genetics 158:787–809
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Cline M, Dong-il K (2002) A preliminary investigation of the role of auxin and cytokinin in sylleptic branching of three hybrid poplar clones exhibiting contrasting degrees of sylleptic branching. Ann Bot 90:417–421
Costes E, Guedon Y (2002) Modelling branching patterns on 1-year-old trunks of six apple cultivars. Ann Bot 89:513–524
Crow P, Houston TJ (2004) The influence of soil and coppice cycle on the rooting habit of short rotation poplar and willow coppice. Biomass Bioenergy 26(6):497–505
Dickmann DI, Stuart KW (1983) The culture of poplars in eastern North America. McNaughton and Gunn, Ann Arbor, MI, p 168
Eberhart SA, Russell WA (1966) Stability parameters for comparing yields. Crop Sci 6:36–40
El Bassam N (1998) Energy Plant Species: their uses and impact on environment and development. James and James, London
Emebiri LC, Moody DB (2006) Heritable basis for some genotype-environment stability statistics: inferences from QTL analysis of heading date in two-rowed barley. Field Crops Res 96:243–251
Ferris R, Long L, Bunn SM, Robinson KM, Bradshaw HD, Rae AM, Taylor G (2002) Leaf stomatal and epidermal cell development: identification of putative quantitative trait loci in relation to elevated carbon dioxide concentration in poplar. Tree Physiol 22:633–640
Frewen BE, Chen THH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD Jr (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845
Gauch HG (1992) Statistical analysis of regional yield trials: AMMI analysis of factorial designs. Elsevier, Amsterdam, The Netherlands
Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137
Grattapaglia D, Bertolucci FLG, Penchel R, Sederoff RR (1996) Genetic mapping of quantitative trait loci controlling growth and wood quality traits in Eucalyptus grandis using a maternal half-sib family and RAPD markers. Genetics 144:1205–1214
Hansen EA (1991) Poplar woody biomass yields: a look to the future. Biomass Bioenergy 1:1–7
Heilman PE, Xie F (1993) Influence of nitrogen growth and productivity of short-rotation Populus trichocarpa × Populus deltoides hybrids. Can J For Res 23:1863–1869
Heilman PE, Ekuan G, Fogle D (1994) Above- and below-ground biomass and fine roots of 4-year-old hybrids of Populus trichocarpa × Populus deltoides and parental species in short rotation culture. Can J For Res 24:1186–1192
Henderson CR (1953) Estimation of variance and co-variance components. Biometrics 9:226–252
Hervé C, Ceulemans R (1996) Short-rotation coppiced vs non-coppiced poplar: a comparative study at two different field sites. Biomass Bioenergy 11:139–150
Ikuko N, Masahiko O (2001) Geographical transition of sylleptic/proleptic branching in three Cinnamomum species with different bud types. Ann Bot 87:35–45
Jansen RC, Van Ooijen JW, Stam P, Lister C, Dean C (1995) Genotype-by-environment interaction in genetic mapping of multiple quantitative trait loci. Theor Appl Genet 91:33–37
Jorge V, Dowkiw A, Faivre-Rampant P, Bastien C (2005) Genetic architecture of qualitative and quantitative Melampsora larici-populina leaf rust resistance in hybrid poplar: genetic mapping and QTL detection. New Phytologist 167:113–127
Korol AB, Ronin YI, Nevo E (1998) Approximate analysis of QTL-environment interaction with no limits on the number of environments. Genetics 148:2015–2028
Kraakman ATW, Niks RE, Van den Berg PMMM, Stam P, van Eeuwijk FA (2004) Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics 168:435–446
Li BL, Wu RL (1997) Heterosis and genotype × environment interactions of juvenile aspens in two contrasting sites. Can J For Res 27:1525–1537
Lin CS, Binns MR (1991) Genetic properties of four types of stability parameter. Theor Appl Genet 82:505–509
Lin CY, Togashi K (2002) Genetic improvement in the presence of genotype by environment interaction. Anim Sci J 73:3–11
Madgwick HAI (1971) The accuracy and precision of estimates of the dry matter in stems, branches and foliage in an old-field Pinus virginiana stand. Miscellaneous Publication 132, Agricultural Experiment Station, University of Maine, Orono, pp 105–112
Mandel J (1969) The partitioning of interaction in analysis of variance. J Res Natl Bur Stand B Math Sci 73B:309–328
Marron N, Bastien C, Sabatti M, Taylor G, Ceulemans R (2006) Plasticity of growth and sylleptic branchiness in two poplar families grown at three contrasting sites across Europe. Tree Physiol 26:935–946
McCamant T, Black RA (2000) Cold hardiness in coastal, montane, and inland populations of Populus trichocarpa. Can J For Res 30:91–99
Morreel K, Goeminne G, Storme V, Sterck L, Ralph J, Coppieters W, Breyne P, Steenackers M, Georges M, Messens E, Boerjan W (2006) Genetical metabolomics of flavonoid biosynthesis in Populus: a case study. Plant J 47:224–237
Neale DB, Savolainen O (2004) Association genetics of complex traits in conifers. Trends Plant Sci 9:325–330
Newcombe G, Bradshaw HD, Chastagner GA, Stettler RF (1996) A major gene for resistance to Melampsora medusae f.sp. deltoidae in a hybrid poplar pedigree. Phytopathology 86:87–94
Papadakis JS (1984) Advances in the analysis of field experiments. Proc Acad Athens 59:326–342
Pontailler JY, Ceulemans R, Guittet J, Mau F (1997) Linear and non-linear functions of volume index to estimate woody biomass in high density young poplar stands. Ann Sci For 54:335–345
Proe MF, Craig J, Griffiths J, Wilson A, Reid E (1999) Comparison of biomass production in coppice and single stem woodland management systems on imperfectly drained gley soil in central Scotland. Biomass Bioenergy 17:141–151
Rae AM, Robinson KM, Street NR, Taylor G (2004) Morphological and physiological traits influencing biomass productivity in short-rotation coppice poplar. Can J For Res 54:335–345
Rae AM, Ferris R, Tallis MJ, Taylor G (2006) Elucidating genomic regions determining enhanced leaf growth and delayed senescence in elevated CO2. Plant Cell Environ 29:1730–1741
Robinson KM, Karp A, Taylor G (2004) Defining leaf traits linked to yield in short-rotation coppice Salix. Biomass Bioenergy 26:417–431
Ronnberg-Wastljung AC, Ahman I, Glynn C, Widenfalk O (2006) Quantitative trait loci for resistance to herbivores in willow: field experiments with varying soils and climates. Entomol Exp Appl 118:163–174
Scarascia-Mugnozza GE (1991) Physiological and morphological determinants of yield in intensively cultured poplar (Populus spp.). Ph.D. thesis, University of Washington, Seattle, WA
Scarascia-Mugnozza GE, Ceulemans R, Heilman PE, Isebrands JG, Settler RF, Hinckley TM (1997) Production physiology and morphology of Populus species and their hybrids grown under short rotation. II. Biomass components and harvest index of hybrid and parental species clones. Can J For Res 27:285–294
Sims REH, Maiava TG, Bullock BT (2001) Short rotation coppice tree species selection for woody biomass production in New Zealand. Biomass Bioenergy 20:329–335
Sims REH, Hastings A, Schlamadinger B, Taylor G, Smith P (2006) Energy crops: current status and future prospects. Glob Chang Biol 12:2459–2471
Singh M, Ceccarelli S, Hamblin J (1993) Estimation of heritability from varietal trials data. Theor Appl Genet 86:437–441
Taylor G (2002) Populus: arabidopsis for forestry. Do we need a model tree? Ann Bot 90:681–689
Tsarouhas V, Gullberg U, Lagercrantz U (2002) An AFLP and RFLP linkage map and quantitative trait locus (QTL) analysis of growth traits in Salix. Theor Appl Genet 105:277–288
Tsarouhas V, Gullberg U, Lagercrantz U (2003) Mapping of quantitative trait loci controlling timing of bud flush in Salix. Hereditas 138:172–178
Tsarouhas V, Gullberg U, Lagercrantz U (2004) Mapping of quantitative trait loci (QTLs) affecting autumn freezing resistance and phenology in Salix. Theor Appl Genet 108:1335–1342
Tuskan GA (1998) Short rotation woody crop supply systems in the United States: what do we know and what do we need to know? Biomass Bioenergy 14:307–315
Updegraff K, Baughman MJ, Taff SJ (2004) Environmental benefits of cropland conversion to hybrid poplar: economic and policy considerations. Biomass Bioenergy 27:411–428
Van Volkenburgh E, Taylor G (1996) Leaf growth physiology. In: Stettler RF, Bradshaw HD, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research, Ottawa, pp 283–300
Via S, Gomulkkiewicz R, de Jong G, Scheiner SM, Schlichting CD, van Tienderen PH (1995) Adaptive phenotypic plasticity: consensus and controversy. Trend Ecol E 10:212–217
Wricke G (1962) Über eine Methode zur Erfassung der ökologischen Streubreite in Feldversuchen. Zeitschur f Pflanzenz 47:92–96
Wu R, Stettler RF (1997) Quantitative genetics of growth and development in Populus. II. The partitioning of genotype × environment interaction in stem growth. Heredity 78:124–134
Wu R, Stettler RF (1998) Quantitative genetics of growth and development in Populus. III. Phenotypic plasticity of crown structure and function. Heredity 81:124–134
Wu R, Bradshaw HD, Stettler RF (1997) Molecular genetics of growth and development in Populus (Salicaceae). V. Mapping quantitative trait loci affecting leaf variation. Am J Bot 84:143–153
Wu R, Bradshaw HD Jr, Stettler RF (1998) Developmental quantitative genetics of growth in Populus. Theor Appl Genet 97:1110–1119
Wu R, Ma CX, Yang MCK, Chang M, Littell RC, Santra U, Wu S, Yin TM, Huang M, Wang M, Casella G (2003) Quantitative trait loci for growth trajectories in Populus. Genet Res 81:51–64
Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favourite. Plant Cell 14:2651–2655
Wullschleger SD, Yin TM, Difazio SP, Tschaplinski TJ, Gunter LE, Davis MF, Tuskan GA (2005) Phenotypic variation in growth and biomass distribution for two advanced-generation pedigrees of hybrid poplar. Can J For Res 35:1779–1789
Zhang X, Wu N, Li C (2005) Physiological and growth responses of Populus davidiana ecotypes to different soil water contents. J Arid Environ 60:567–579
Acknowledgements
This research was supported by the European Commission through the Directorate General Research within the Fifth Framework for Research—Quality of Life and Management of the Living Resources Programme, contract no. QLK5-CT-2002-00953 (POPYOMICs), coordinated by the University of Southampton. Field work assistance was provided by MR Cotton, M Rodregas, (UK), Dr. F Nardin, L Ricciotti, F Salani (Italy), Dr. M Villar, P Poursat and J Gauvin (France). Research in the laboratory of Prof. Gail Taylor is also supported by the Department for Environment Food and Rural Affairs contracts (NF0410, NF0424). SY Dillen is a Research Assistant of the FWO—Flanders (Fund for Scientific Research—Flanders). We are grateful to GA Tuskan for the linkage map data.
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Rae, A.M., Pinel, M.P.C., Bastien, C. et al. QTL for yield in bioenergy Populus: identifying G×E interactions from growth at three contrasting sites. Tree Genetics & Genomes 4, 97–112 (2008). https://doi.org/10.1007/s11295-007-0091-3
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DOI: https://doi.org/10.1007/s11295-007-0091-3