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Analysis of the genetic variation in growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa provenances

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Populus trichocarpa is a biological model and a candidate species for bioethanol production. Although intraspecific variation is recognized, knowledge about genetic variation underlying the properties of its lignocellulosic biomass is still incomplete. Genetic variation is fundamental for continuing genetic improvement. In this study, we carried out a comprehensive phenotypic characterization of this species, analyzing a suite of quantitative traits associated with growth performance and wood quality. Traits involved growth rate (height, diameter), phenology (bud flush), and ecophysiology (leaf carbon and nitrogen content and isotopic composition), along with the chemical composition (contents of sugars and lignin) and metabolome of wood. We utilized 460 clones, representing 101 provenances collected from Oregon and Washington. These genotypes were planted in California, in 2009, and sampled after three growing seasons. Trait characterization was carried out by direct measurements, determination of stable isotopes (leaf samples), and technologies based on mass spectrometry (wood samples). A significant clonal effect was observed for most of the traits, explaining up to 76.4 % of total variation. Estimates of “broad-sense heritability” were moderate to high, reaching 0.96 (for date of bud flush). Phenotypic and genetic correlations varied extensively depending on specific traits. In addition, metabolomic analyses quantified 632 metabolites. Twenty-eight of these varied significantly with experimental factors, showing low to moderate heritability and correlation estimates. The results support the presence of significant clonal variation and inheritance for the assessed traits, required for response to genetic selection.

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  1. Abramson M, Shoseyov O, Shani Z (2010) Plant cell wall reconstruction toward improved lignocellulosic production and processability. Plant Sci 178:61–72. doi:10.1016/j.plantsci.2009.11.003

  2. Al Afas N, Pellis A, Niinemets Ü, Ceulemans R (2005) Growth and production of a short rotation coppice culture of poplar. II. Clonal and year-to-year differences in leaf and petiole characteristics and stand leaf area index. Biomass Bioenergy 28:536–547. doi:10.1016/j.biombioe.2004.11.010

  3. Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics. 1165-1188. doi:10.1214/aos/1013699998

  4. Bonhomme L et al (2009) Leaf proteome analysis of eight Populus x euramericana genotypes: genetic variation in drought response and in water-use efficiency involves photosynthesis-related proteins. Proteomics 9:4121–4142. doi:10.1002/pmic.200900047

  5. Bradshaw HD, Stettler RF (1995) Molecular genetics of growth and development in Populus. IV. Mapping QTLs with large effects on growth, form, and phenology traits in a forest tree. Genetics 139:963–973

  6. Campbell MM, Sederoff RR (1996) Variation in lignin content and composition (mechanisms of control and implications for the genetic improvement of plants). Plant Physiol 110:3–13

  7. Condon AG, Richards RA, Rebetzke GJ, Farquhar GD (2004) Breeding for high water-use efficiency. J Exp Bot 55:2447–2460. doi:10.1093/jxb/erh277

  8. Couturier J, Doidy J, Guinet F, Wipf D, Blaudez D, Chalot M (2010) Glutamine, arginine and the amino acid transporter Pt-CAT11 play important roles during senescence in poplar. Ann Bot 105:1159–1169. doi:10.1093/aob/mcq047

  9. Deslauriers A, Giovannelli A, Rossi S, Castro G, Fragnelli G, Traversi L (2009) Intra-annual cambial activity and carbon availability in stem of poplar. Tree Physiol 29:1223–1235. doi:10.1093/treephys/tpp061

  10. Dillen S et al (2009) Genomic regions involved in productivity of two interspecific poplar families in Europe. 1. Stem height, circumference and volume. Tree Gen Genomes 5:147–164. doi:10.1007/s11295-008-0175-8

  11. Dillen SY, Marron N, Koch B, Ceulemans R (2008) Genetic variation of stomatal traits and carbon isotope discrimination in two hybrid poplar families (Populus deltoides ‘S9-2’ x P. nigra ‘Ghoy’ and P. deltoides ‘S9-2’ x P. trichocarpa ‘V24’). Ann Bot 102:399–407. doi:10.1093/aob/mcn107

  12. Dillen SY, Rood S, Ceulemans R (2010) Growth and physiology. In: Jansson S, Bhalerao R, Groover A (eds) Genetics and genomics of Populus, vol 8, Plant genetics and genomics: crops and models. Springer, New York, pp 39–63. doi:10.1007/978-1-4419-1541-2_10

  13. Dinus R (2001) Genetic improvement of poplar feedstock quality for ethanol production. Appl Biochem Biotechnol 91-93:23–34. doi:10.1385/abab:91-93:1-9:23

  14. Easlon HM, Nemali KS, Richards JH, Hanson DT, Juenger TE, McKay JK (2014) The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana. Photosynth Res 119:119–129. doi:10.1007/s11120-013-9891-5

  15. Eckert AJ et al (2012) Association genetics of the loblolly pine (Pinus taeda, Pinaceae) metabolome. New Phytologist 193:890–902. doi:10.1111/j.1469-8137.2011.03976.x

  16. Ellis B, Jansson S, Strauss SH, Tuskan GA (2010) Why and how Populus became a “model tree”. In: Jansson S, Bhalerao R, Groover A (eds) Genetics and genomics of Populus, vol 8, Plant genetics and genomics: crops and models. Springer, New York, pp 3–14. doi:10.1007/978-1-4419-1541-2_10

  17. Farquhar G, O’Leary M, Berry J (1982) On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves. Funct Plant Biol 9:121–137. doi:10.1071/PP9820121

  18. Farquhar G, Richards R (1984) Isotopic composition of plant carbon correlates with water-use efficiency of wheat genotypes. Funct Plant Biol 11:539–552. doi:10.1071/PP9840539

  19. Farquhar GD, Ehleringer JR, Hubick KT (1989) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Physiol Plant Mol Biol 40:503–537. doi:10.1146/annurev.pp.40.060189.002443

  20. Frewen BE, Chen TH, Howe GT, Davis J, Rohde A, Boerjan W, Bradshaw HD (2000) Quantitative trait loci and candidate gene mapping of bud set and bud flush in Populus. Genetics 154:837–845

  21. Groover AT, Nieminen K, Helariutta Y, Mansfield SD (2010) Wood formation in Populus. In: Jansson S, Bhalerao R, Groover A (eds) Genetics and Genomics of Populus, vol 8, Plant genetics and genomics: crops and models. Springer, New York, pp 201–224. doi:10.1007/978-1-4419-1541-2_10

  22. Guerra FP, Wegrzyn JL, Sykes R, Davis MF, Stanton BJ, Neale DB (2013) Association genetics of chemical wood properties in black poplar (Populus nigra). New Phytol 197:162–176. doi:10.1111/nph.12003

  23. Henderson DE, Jose S (2005) Production physiology of three fast-growing hardwood species along a soil resource gradient. Tree Physiol 25:1487–1494. doi:10.1093/treephys/25.12.1487

  24. Hertzberg M et al (2001) A transcriptional roadmap to wood formation. Proc Natl Acad Sci 98:14732–14737. doi:10.1073/pnas.261293398

  25. Isik F, Toplu F (2004) Variation in juvenile traits of natural black poplar (Populus nigra L.) clones in Turkey. New Forests 27:175–187. doi:10.1023/A:1025071515826

  26. Kačík F, Ďurkovič J, Kačíková D (2012) Chemical profiles of wood components of poplar clones for their energy utilization. Energies 5:5243–5256

  27. Laureysens I, Pellis A, Willems J, Ceulemans R (2005) Growth and production of a short rotation coppice culture of poplar. III. Second rotation results. Biomass Bioenergy 29:10–21. doi:10.1016/j.biombioe.2005.02.005

  28. Marron N, Bastien C, Sabatti M, Taylor G, Ceulemans R (2006) Plasticity of growth and sylleptic branchiness in two poplar families grown at three sites across Europe. Tree Physiol 26:935–946

  29. McKown AD et al (2014) Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa. New Phytologist 201:1263–1276. doi:10.1111/nph.12601

  30. Miller R, Keller M (2009) The DOE BioEnergy Science Center-A U.S. Department of Energy Bioenergys Research Center. In: Tomes D, Lakshmanan P, Songstad D (eds) Biofuels. Global impact on renewable energy, production agriculture, and technological advancements. Springer, New York, pp 9-18. doi:DOI 10.1007/978-1-4419-7145-6

  31. Mitchell CP (1992) Ecophysiology of short rotation forest crops. Biomass Bioenergy 2:25–37. doi:10.1016/0961-9534(92)90085-5

  32. Monclus R et al (2005) Productivity, leaf traits and carbon isotope discrimination in 29 Populus deltoides × P. nigra clones. New Phytol 167:53–62. doi:10.1111/j.1469-8137.2005.01407.x

  33. Monclus R et al (2009) Productivity, water-use efficiency and tolerance to moderate water deficit correlate in 33 poplar genotypes from a Populus deltoides x Populus trichocarpa F1 progeny. Tree Physiol 29:1329–1339. doi:10.1093/treephys/tpp075

  34. Ozel HB, Ertekin M, Tunctaner K (2010) Genetic variation in growth traits and morphological characteristics of eastern cottonwood (Populus deltoides Bartr.) hybrids at nursery stage. Sci Res Essays 5:962–969

  35. Robinson A, Mansfield SD (2011) Metabolomics in poplar. In: Genetics, genomics and breeding of poplar. Science Publishers, pp 166-191. doi:10.1201/b10819-14

  36. Rohde A et al (2011) Bud set in poplar—genetic dissection of a complex trait in natural and hybrid populations. New Phytol 189:106–121. doi:10.1111/j.1469-8137.2010.03469.x

  37. Sauter J, van Cleve B (1992) Seasonal variation of amino acids in the xylem sap of “Populus x canadensis” and its relation to protein body mobilization. Trees 7:26–32. doi:10.1007/BF00225228

  38. Sauter J, van Cleve B (1994) Storage, mobilization and interrelations of starch, sugars, protein and fat in the ray storage tissue of poplar trees. Trees 8:297–304. doi:10.1007/BF00202674

  39. Scaracia-Mugnozza GE, Ceulemans R, Heilman PE, Isebrands JG, Stettler 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 Forest Res 27:285–294. doi:10.1139/x96-180

  40. Slavov GT, Zhelev P (2010) Salient biological features, systematics, and genetic variation of Populus. In: Jansson S, Bhalerao RP, Groover A (eds) Genetics and genomics of Populus, vol 8. Plant genetics and genomics: crops and models. pp 15-38

  41. Smilde AK, Jansen JJ, Hoefsloot HCJ, Lamers R-JAN, van der Greef J, Timmerman ME (2005) ANOVA-simultaneous component analysis (ASCA): a new tool for analyzing designed metabolomics data. Bioinformatics 21:3043–3048. doi:10.1093/bioinformatics/bti476

  42. Soolanayakanahally RY, Guy RD, Silim SN, Drewes EC, Schroeder WR (2009) Enhanced assimilation rate and water use efficiency with latitude through increased photosynthetic capacity and internal conductance in balsam poplar (Populus balsamifera L.). Plant Cell Environ 32:1821–1832. doi:10.1111/j.1365-3040.2009.02042.x

  43. Stanton BJ, Neale D, Li S (2010) Populus breeding: from the classical to the genomic approach. In: Jansson S, Bhalerao R, Groover A (eds) Genetics and genomics of Populus, vol 8, Plant genetics and genomics: crops and models. Springer, New York, pp 309–348. doi:10.1007/978-1-4419-1541-2_10

  44. Stettler RF, Bradshaw HD, Heilman P, Hinckley T (1996) Biology of Populus and its implications for management and conservation. NRC Research Press. doi:10.1139/9780660165066

  45. Sticklen MB (2008) Plant genetic engineering for biofuel production: towards affordable cellulosic ethanol. Nat Rev Genet 9:433–443

  46. Szarka A, Tomasskovics B, Bánhegyi G (2012) The ascorbate-glutathione-α-tocopherol triad in abiotic stress response. Int J Mol Sci 13:4458–4483. doi:10.3390/ijms13044458

  47. Wegrzyn JL et al (2010) Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol 188:515–532. doi:10.1111/j.1469-8137.2010.03415.x

  48. Xia J, Mandal R, Sinelnikov IV, Broadhurst D, Wishart DS (2012) MetaboAnalyst 2.0—a comprehensive server for metabolomic data analysis. Nucleic Acids Res 40:W127–W133. doi:10.1093/nar/gks374

  49. Zabek LM, Prescott CE (2006) Biomass equations and carbon content of aboveground leafless biomass of hybrid poplar in Coastal British Columbia. For Ecol Manage 223:291–302. doi:10.1016/j.foreco.2005.11.009

  50. Zamudio F, Wolfinger R, Stanton B, Guerra F (2008) The use of linear mixed model theory for the genetic analysis of repeated measures from clonal tests of forest trees I. A focus on spatially repeated data. Tree Gen Genomes 4:299–313. doi:10.1007/s11295-007-0110-4

  51. 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. doi:10.1016/j.jaridenv.2004.07.008

  52. Zhao F, Gao R, Shen Y, Su X, Zhang B (2006) Foliar carbon isotope composition (δ13C) and water use efficiency of different Populus deltoides clones under water stress. Front Forest China 1:89–94. doi:10.1007/s11461-005-0005-1

  53. Ziebell AL et al (2013) Sunflower as a biofuels crop: an analysis of lignocellulosic chemical properties. Biomass Bioenergy 59:208–217. doi:10.1016/j.biombioe.2013.06.009

  54. Zobel B, Jett JB (1995) Genetics of wood production. Springer, Berlin, Heidelberg. doi:10.1007/978-3-642-79514-5

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This study was funded by the Advanced Hardwood Biofuels Northwest Project, supported by Agriculture and Food Research Initiative Competitive Grant no. 2011-68005-30407, from the USDA National Institute of Food and Agriculture. Additional support was provided through the California Agricultural Experiment Station.

Data archiving statement

Data used in this manuscript were submitted to the TreeGenes database (http://dendrome.ucdavis.edu/treegenes/) under the accession number TGDR050.

Author information

Correspondence to David B. Neale.

Additional information

Communicated by R. Burdon

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Guerra, F.P., Richards, J.H., Fiehn, O. et al. Analysis of the genetic variation in growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa provenances. Tree Genetics & Genomes 12, 6 (2016). https://doi.org/10.1007/s11295-015-0965-8

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  • Populus trichocarpa
  • Growth
  • Stable isotopes
  • Lignin
  • Cellulose
  • Wood metabolome