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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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Abstract

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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References

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Book  Google Scholar 

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Acknowledgments

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.

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Authors and Affiliations

  1. Department of Plant Sciences, University of California at Davis, 262C Robbins Hall, Mail Stop 4, Davis, CA, 95616, USA

    Fernando P. Guerra, Randi Famula & David B. Neale

  2. Bioenergy Research Center, University of California at Davis, Davis, CA, 95616, USA

    David B. Neale

  3. Department of Land, Air and Water Resources, University of California, Davis, CA, 95616, USA

    James H. Richards

  4. Department of Molecular and Cellular Biology & Genome Center, University of California, Davis, CA, 95616, USA

    Oliver Fiehn

  5. Genetic Resources Conservation Program, GreenWood Resources, Portland, OR, 97201, USA

    Brian J. Stanton & Richard Shuren

  6. National Renewable Energy Laboratory, Golden, CO, 80401, USA

    Robert Sykes & Mark F. Davis

  7. Instituto de Ciencias Biológicas, Universidad de Talca, P.O. Box 747, Talca, Chile

    Fernando P. Guerra

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  1. Fernando P. Guerra
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  2. James H. Richards
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  3. Oliver Fiehn
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  4. Randi Famula
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  9. David B. Neale
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Correspondence to David B. Neale.

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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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