Bioenergy Trees: Genetic and Genomic Strategies to Improve Yield

  • G. TaylorEmail author
  • M. R. Allwright
  • H. K. Smith
  • A. Polle
  • H. Wildhagen
  • M. Hertzberg
  • R. Bhalerao
  • J. J. B. Keurentjes
  • S. Scalabrin
  • D. Scaglione
  • M. Morgante
Conference paper


Growing energy demand, the need to reduce greenhouse gas (GHG) emissions and the move towards a low carbon economy are driving the development of non-food lignocellulosic crops to provide an alternative to fossil fuels and to support bioenergy with carbon capture and storage (CCS). Trees offer significant potential in this role. Poplar, willow and eucalyptus are suggested here as three target tree crops however, a significant yield gap (the difference between potential and observed yield) exists that may be as much as 10 tonnes ha−1y−1. New technologies offer great potential to accelerate the breeding pipeline and provide the bioeconomy with fast growing, stress tolerant and low-input bioenergy trees with higher potential yields and smaller yield gaps. These technologies include both genomic selection (GS) and genome editing, where significant progress for trees has been made in recent years. The most challenging remaining bottleneck is the accurate phenotyping of large populations of trees for traits that underpin yield; more research is required on target traits for the sustainable intensification of the production of bioenergy tree crops.


Biomass trees Sustainable intensification Eucalyptus Populus 



We acknowledge support from the Seventh Framework for Research of the European Commission, for the project WATBIO (, project number, FP7-311929.


  1. Adegbidi HG, Volk TA, White EH et al (2001) Biomass and nutrient removal by willow clones in experimental bioenergy plantations in New York State. Biomass and Bioenergy 20:399–411CrossRefGoogle Scholar
  2. Adegbidi HG, Briggs RD, Volk TA et al (2003) Effect of organic amendments and slow-release nitrogen fertilizer on willow biomass production and soil chemical characteristics. Biomass and Bioenergy 25:389–398CrossRefGoogle Scholar
  3. Affholder F, Poeydebat C, Corbeels M et al (2013) The yield gap of major food crops in family agriculture in the tropics: assessment and analysis through field surveys and modelling. F Crop Res 143:106–118CrossRefGoogle Scholar
  4. Allwright MR, Taylor G (2016) Molecular breeding for improved second generation bioenergy crops. Trends Plant Sci 21:43–54PubMedCrossRefGoogle Scholar
  5. Alves AA, Rosado CCG, Faria DA et al (2012) Genetic mapping provides evidence for the role of additive and non-additive QTLs in the response of inter-specific hybrids of Eucalyptus to Puccinia psidii rust infection. Euphytica 183:27–38CrossRefGoogle Scholar
  6. Arbelaez JD, Moreno LT, Singh N et al (2015) Development and GBS-genotyping of introgression lines (ILs) using two wild species of rice, O. meridionalis and O. rufipogon, in a common recurrent parent, O.sativa cv. Curinga. Mol Breed 35:81PubMedPubMedCentralCrossRefGoogle Scholar
  7. Barkley NA, Wang ML (2008) Application of TILLING and EcoTILLING as reverse genetic approaches to elucidate the function of genes in plants and animals. Curr Genomics 9:212–226PubMedPubMedCentralCrossRefGoogle Scholar
  8. Beaulieu J, Doerksen TK, MacKay J et al (2014) Genomic selection accuracies within and between environments and small breeding groups in white spruce. BMC Genomics 15:1048PubMedPubMedCentralCrossRefGoogle Scholar
  9. Berlin S, Lagercrantz U, von Arnold S et al (2010) High-density linkage mapping and evolution of paralogs and orthologs in Salix and Populus. BMC Genomics 11:129PubMedPubMedCentralCrossRefGoogle Scholar
  10. Berlin S, Trybush SO, Fogelqvist J et al (2014) Genetic diversity, population structure and phenotypic variation in European Salix viminalis L. (Salicaceae). Tree Genet Genomes 10:1595–1610CrossRefGoogle Scholar
  11. Blanca J, Montero-Pau J, Sauvage C et al (2015) Genomic variation in tomato, from wild ancestors to contemporary breeding accessions. BMC Genomics 16:257PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bredemeier M, Busch G, Hartmann L et al (2015) Fast growing plantations for wood production - integration of ecological effects and economic perspectives. Front Bioeng Biotechnol 3:72PubMedPubMedCentralCrossRefGoogle Scholar
  13. Brereton NJB, Pitre FE, Hanley SJ et al (2010) QTL mapping of enzymatic saccharification in short rotation coppice willow and its independence from biomass yield. Bioenergy Res 3:251–261CrossRefGoogle Scholar
  14. Brondani RPV, Williams ER, Brondani C, Grattapaglia D (2006) A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus. BMC Plant Biol 6:20PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bungart R (1999) Erzeugung von Biomasse zur energetischen Nutzung durch den Anbau schnellwachsender Baumarten auf Kippsubstraten des Lausitzer Braunkohlereviers unter besonderer Beru¨ cksichtigung der Na¨ hrelementversorgung und des Wasserhaushaltes. Cottbuser Schr Bodenschutz Rekult 7:159Google Scholar
  16. Bungart R, Hüttl 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. Eur J For Res 123:105–115Google Scholar
  17. Carmona R, Nuñez T, Alonso MF (2015) Biomass yield and quality of an energy dedicated crop of poplar (Populus spp.) clones in the Mediterranean zone of Chile. Biomass and Bioenergy 74:96–102CrossRefGoogle Scholar
  18. Cervera M, Ivens B, Gusma J et al (2001) Dense genetic linkage maps of three populus species (populus deltoides, P. Nigra and P. Trichocarpa) based on AFLP and microsatellite markers. Genetics 158:787–809PubMedPubMedCentralGoogle Scholar
  19. David K, Ragauskas AJ (2010) Switchgrass as an energy crop for biofuel production: A review of its ligno-cellulosic chemical properties. Energy Environ Sci 3:1182CrossRefGoogle Scholar
  20. Davis SC, Boddey RM, Alves BJR et al (2013) Management swing potential for bioenergy crops. GCB Bioenergy 5:623–638CrossRefGoogle Scholar
  21. de Andrade TCGR, de Barros NF, Dias LE, Azevedo MIR (2013) Biomass yield and calorific value of six clonal stands of Eucalyptus urophylla ST Blake cultivated in Northeastern Brazil. Cern Lavras 19:467–472CrossRefGoogle Scholar
  22. Dillen SY, Djomo SN, Al Afas N et al (2013) Biomass yield and energy balance of a short-rotation poplar coppice with multiple clones on degraded land during 16 years. Biomass and Bioenergy 56:157–165CrossRefGoogle Scholar
  23. Don A, Osborne B, Hastings A et al (2012) Land-use change to bioenergy production in Europe: implications for the greenhouse gas balance and soil carbon. GCB Bioenergy 4:372–391CrossRefGoogle Scholar
  24. Drost DR, Puranik S, Novaes E et al (2015) Genetical genomics of Populus leaf shape variation. BMC Plant Biol 15:166PubMedPubMedCentralCrossRefGoogle Scholar
  25. Fan D, Liu T, Li C et al (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in populus in the first generation. Sci Rep 5:12217PubMedPubMedCentralCrossRefGoogle Scholar
  26. Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374PubMedCrossRefGoogle Scholar
  27. Fortier J, Gagnon D, Truax B, Lambert F (2010) Biomass and volume yield after 6 years in multiclonal hybrid poplar riparian buffer strips. Biomass and Bioenergy 34:1028–1040CrossRefGoogle Scholar
  28. Freeman JS, Whittock SP, Potts BM, Vaillancourt RE (2009) QTL influencing growth and wood properties in Eucalyptus globulus. Tree Genet Genomes 5:713–722CrossRefGoogle Scholar
  29. Freeman JS, Potts BM, Downes GM et al (2013) Stability of quantitative trait loci for growth and wood properties across multiple pedigrees and environments in Eucalyptus globulus. New Phytol 198:1121–1134PubMedCrossRefGoogle Scholar
  30. Fuss S, Canadell JG, Peters GP et al (2014) Betting on negative emissions. Nat Clim Chang 4:850–853CrossRefGoogle Scholar
  31. FuturaGene (2015) FuturaGene’s eucalyptus is approved for commercial use in BrazilGoogle Scholar
  32. Gaj T, Gersbach CA, Barbas CF (2013) ZFN, TALEN and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405PubMedPubMedCentralCrossRefGoogle Scholar
  33. Gamal El-Dien O, Ratcliffe B, Klápště J et al (2015) Prediction accuracies for growth and wood attributes of interior spruce in space using genotyping-by-sequencing. BMC Genomics 16:1–16CrossRefGoogle Scholar
  34. Gaut BS, Long AD (2003) The lowdown on linkage disequilibrium. Plant Cell 15:1502–1506PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gehan MA, Greenham K, Mockler TC, McClung CR (2015) Transcriptional networks-crops, clocks, and abiotic stress. Curr Opin Plant Biol 24:39–46PubMedCrossRefGoogle Scholar
  36. Geraldes A, Pang J, Thiessen N et al (2011) SNP discovery in black cottonwood (Populus trichocarpa) by population transcriptome resequencing. Mol Ecol Resour 11:81–92PubMedCrossRefGoogle Scholar
  37. Geraldes A, Difazio SP, Slavov GT et al (2013) A 34K SNP genotyping array for populus trichocarpa: design, application to the study of natural populations and transferability to other populus species. Mol Ecol Resour 13:306–323PubMedCrossRefGoogle Scholar
  38. Gomez LD, Steele-King CG, McQueen-Mason SJ (2008) Sustainable liquid biofuels from biomass: the writing’s on the walls. New Phytol 178:473–485PubMedCrossRefGoogle Scholar
  39. Grattapaglia D, Resende MDV (2010) Genomic selection in forest tree breeding. Tree Genet Genomes 7:241–255CrossRefGoogle Scholar
  40. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedPubMedCentralGoogle Scholar
  41. Grobkinsky DK, Pieruschka R, Svensgaard J et al (2015) Phenotyping in the fields: dissecting the genetics of quantitative traits and digital farming. New Phytol 207:950–952CrossRefGoogle Scholar
  42. Guerra FP, Wegrzyn JL, Sykes R et al (2013) Association genetics of chemical wood properties in black poplar (Populus nigra). New Phytol 197:162–176PubMedCrossRefGoogle Scholar
  43. Guo LB, Sims REH, Horne DJ (2006) Biomass production and nutrient cycling in Eucalyptus short rotation energy forests in New Zealand: II. Litter fall and nutrient return. Biomass and Bioenergy 30:393–404CrossRefGoogle Scholar
  44. Hamanishi ET, Barchet GL, Dauwe R et al (2015) Poplar trees reconfigure the transcriptome and metabolome in response to drought in a genotype- and time-of-day-dependent manner. BMC Genomics 16:329PubMedPubMedCentralCrossRefGoogle Scholar
  45. Hanley SJ, Karp A (2014) Genetic strategies for dissecting complex traits in biomass willows (Salix spp.). Tree Physiol 34:1167–1180PubMedCrossRefGoogle Scholar
  46. Hanley SJ, Pei MH, Powers SJ et al (2011) Genetic mapping of rust resistance loci in biomass willow. Tree Genet Genomes 7:597–608CrossRefGoogle Scholar
  47. Harfouche A, Meilan R, Altman A (2011) Tree genetic engineering and applications to sustainable forestry and biomass production. Trends Biotechnol 29:9–17PubMedCrossRefGoogle Scholar
  48. Harfouche A, Meilan R, Kirst M et al (2012) Accelerating the domestication of forest trees in a changing world. Trends Plant Sci 17:64–72PubMedCrossRefGoogle Scholar
  49. Harris ZM, Spake R, Taylor G (2015) Land use change to bioenergy: a meta-analysis of soil carbon and GHG emissions. Biomass and Bioenergy 82:27–39CrossRefGoogle Scholar
  50. Hefer CA, Mizrachi E, Myburg AA et al (2015) Comparative interrogation of the developing xylem transcriptomes of two wood-forming species: Populus trichocarpa and Eucalyptus grandis. New Phytol 206:1391–1405PubMedCrossRefGoogle Scholar
  51. Hennig A, Kleinschmit JRG, Schoneberg S et al (2015) Water consumption and biomass production of protoplast fusion lines of poplar hybrids under drought stress. Front Plant Sci 6:330PubMedPubMedCentralCrossRefGoogle Scholar
  52. Herrero C, Juez L, Tejedor C et al (2014) Importance of root system in total biomass for Eucalyptus globulus in northern Spain. Biomass and Bioenergy 67:212–222CrossRefGoogle Scholar
  53. Hinchee M, Rottmann W, Mullinax L et al (2009) Short-rotation woody crops for bioenergy and biofuels applications. In Vitro Cell Dev Biol Plant 45:619–629PubMedPubMedCentralCrossRefGoogle Scholar
  54. Hudson CJ, Freeman JS, Kullan AR et al (2012) A reference linkage map for Eucalyptus. BMC Genomics 13:240PubMedPubMedCentralCrossRefGoogle Scholar
  55. Ingvarsson PK, Street NR (2010) Association genetics of complex traits in plants. New Phytol 189:909–922PubMedCrossRefGoogle Scholar
  56. Jia X, Zhao M, Zhao C et al (2011) Populus biomass protein-protein interactions and their functions. BMC ProcGoogle Scholar
  57. Joosen RVL, Ligterink W, Hilhorst HWM, Keurentjes JJB (2009) Advances in genetical genomics of plants. Curr Genomics 10:540–549PubMedPubMedCentralCrossRefGoogle Scholar
  58. Joosen RVL, Arends D, Li Y et al (2013) Identifying genotype-by-environment interactions in the metabolism of germinating Arabidopsis seeds using generalized genetical genomics. Plant Physiol 162:553–566PubMedPubMedCentralCrossRefGoogle Scholar
  59. Jørgensen U (2011) Benefits versus risks of growing biofuel crops: the case of Miscanthus. Curr Opin Environ Sustain 3:24–30CrossRefGoogle Scholar
  60. Jung SK, Parisutham V, Jeong SH, Lee SK (2012) Heterologous expression of plant cell wall degrading enzymes for effective production of cellulosic biofuels. J Biomed Biotechnol 2012:405842PubMedPubMedCentralCrossRefGoogle Scholar
  61. Karp A, Hanley SJ, Trybush SO et al (2011) Genetic improvement of willow for bioenergy and biofuels. J Integr Plant Biol 53:151–165PubMedCrossRefGoogle Scholar
  62. Kassie BT, Van Ittersum MK, Hengsdijk H et al (2014) Climate-induced yield variability and yield gaps of maize (Zea mays L.) in the Central Rift Valley of Ethiopia. F Crop Res 160:41–53CrossRefGoogle Scholar
  63. Kim S, Kim Y, Ee YL et al (2012) The transgenic poplar as an efficient bioreactor system for the production of xylanase. Biosci Biotechnol Biochem 76:1140–1145PubMedCrossRefGoogle Scholar
  64. Kopp RF, Abrahamson LP, White EH et al (2001) Willow biomass production during ten successive annual harvests. Biomass and Bioenergy 20:1–7CrossRefGoogle Scholar
  65. La Mantia J, Klápště J, El-Kassaby YA et al (2013) Association analysis identifies melampsora × columbiana poplar leaf rust resistance SNPs. PLoS One 8, e78423PubMedPubMedCentralCrossRefGoogle Scholar
  66. Labrecque M, Teodorescu TI (2003) High biomass yield achieved by Salix clones in SRIC following two 3-year coppice rotations on abandoned farmland in southern Quebec, Canada. Biomass and Bioenergy 25:135–146CrossRefGoogle Scholar
  67. Labrecque M, Teodorescu T (2005) Field performance and biomass production of 12 willow and poplar clones in short-rotation coppice in southern Quebec (Canada). Biomass and Bioenergy 29:1–9CrossRefGoogle Scholar
  68. Lamb A, Green R, Bateman I et al (2016) The potential for land sparing to offset greenhouse gas emissions from agriculture. Nat Clim Chang 1Google Scholar
  69. Ledford H (2014) Brazil considers transgenic trees. Nature 512:357PubMedCrossRefGoogle Scholar
  70. Licker R, Johnston M, Foley JA et al (2010) Mind the gap: how do climate and agricultural management explain the “yield gap” of croplands around the world? Glob Ecol Biogeogr 19:769–782CrossRefGoogle Scholar
  71. Liesebach M, Naujoks G (2004) Approaches on vegetative propagation of difficult-to-root Salix caprea. Plant Cell Tissue Organ Cult 79:239–247CrossRefGoogle Scholar
  72. Liu P, Wang C, Li L et al (2011) Mapping QTLs for oil traits and eQTLs for oleosin genes in jatropha. BMC Plant Biol 11:132PubMedPubMedCentralCrossRefGoogle Scholar
  73. Liu J, Yin T, Ye N et al (2013) Transcriptome analysis of the differentially expressed genes in the male and female shrub willows (Salix suchowensis). PLoS One 8, e60181PubMedPubMedCentralCrossRefGoogle Scholar
  74. Majewski J, Pastinen T (2011) The study of eQTL variations by RNA-seq: From SNPs to phenotypes. Trends Genet 27:72–79PubMedCrossRefGoogle Scholar
  75. Manning P, Taylor GE, Hanley M (2015) Bioenergy, food production and biodiversity - an unlikely alliance? GCB Bioenergy 7:570–576CrossRefGoogle Scholar
  76. Mardis ER (2011) A decade’s perspective on DNA sequencing technology. Nature 470:198–203PubMedCrossRefGoogle Scholar
  77. Marroni F, Pinosio S, Di Centa E et al (2011) Large-scale detection of rare variants via pooled multiplexed next-generation sequencing: towards next-generation Ecotilling. Plant J 67:736–745PubMedCrossRefGoogle Scholar
  78. McElroy GH, Dawson WM (1986) Biomass from short-rotation coppice willow on marginal land. Biomass 10:225–240CrossRefGoogle Scholar
  79. McKown AD, Guy RD, Quamme L et al (2014a) Association genetics, geography, and ecophysiology link stomatal patterning in Populus trichocarpa with carbon gain and disease resistance trade-offs. Mol Ecol 23:5771–5790PubMedCrossRefGoogle Scholar
  80. McKown AD, Klápště J, Guy RD et al (2014b) Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa. New Phytol 203:535–553PubMedCrossRefGoogle Scholar
  81. Meilan R, Auerbach DJ, Ma C et al (2002) Stability of herbicide resistance and GUS expression in transgenic hybrid poplars (Populus sp.) during four years of field trials and vegetative propagation. HortScience 37:277–280Google Scholar
  82. Miedaner T, Korzun V (2012) Marker-assisted selection for disease resistance in wheat and barley breeding. Phytopathology 102:560–566PubMedCrossRefGoogle Scholar
  83. Milner S, Holland RA, Lovett A et al (2015) Potential impacts on ecosystem services of land use transitions to second generation bioenergy crops in GB. GCB Bioenergy 8:317–333PubMedPubMedCentralCrossRefGoogle Scholar
  84. Minhas PS, Yadav RK, Lal K, Chaturvedi RK (2015) Effect of long-term irrigation with wastewater on growth, biomass production and water use by Eucalyptus (Eucalyptus tereticornis Sm.) planted at variable stocking density. Agric Water Manag 152:151–160CrossRefGoogle Scholar
  85. Missiaggia AA, Piacezzi AL, Grattapaglia D (2005) Genetic mapping of Eef1, a major effect QTL for early flowering in Eucalyptus grandis. Tree Genet Genomes 1:79–84CrossRefGoogle Scholar
  86. Mueller ND, Gerber JS, Johnston M et al (2012) Closing yield gaps through nutrient and water management. Nature 490:254–257PubMedCrossRefGoogle Scholar
  87. Müller MD, Filho AAT, Vale RS, do Couto L (2005) Biomass yield and energetic content in Agroforestry Systems with Eucalypt in Vazante-MG. Biomassa Energ 2:125–132Google Scholar
  88. Muscolo A, Junker A, Klukas C et al (2015) Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions. J Exp Bot 66:5467–5480PubMedPubMedCentralCrossRefGoogle Scholar
  89. Myburg A, Grattapaglia D, Tuskan G et al (2011) The Eucalyptus grandis Genome Project: Genome and transcriptome resources for comparative analysis of woody plant biology. BMC Proc 5:I20PubMedCentralCrossRefGoogle Scholar
  90. Nassi O Di Nasso N, Guidi W, Ragaglini G et al (2010) Biomass production and energy balance of a 12-year-old short-rotation coppice poplar stand under different cutting cycles. GCB Bioenergy 2:89–97Google Scholar
  91. Navarro M, Ayax C, Martinez Y et al (2011) Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnol J 9:50–63PubMedCrossRefGoogle Scholar
  92. Neale DB, Kremer A (2011) Forest tree genomics: growing resources and applications. Nat Rev Genet 12:111–122PubMedCrossRefGoogle Scholar
  93. Nielsen UB, Madsen P, Hansen JK et al (2014) Production potential of 36 poplar clones grown at medium length rotation in Denmark. Biomass and Bioenergy 64:99–109CrossRefGoogle Scholar
  94. Nonhebel S (2002) Energy yields in intensive and extensive biomass production systems. Biomass and Bioenergy 22:159–167CrossRefGoogle Scholar
  95. Novaes E, Osorio L, Drost DR et al (2009) Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol 182:878–890PubMedCrossRefGoogle Scholar
  96. Polle A, Chen S (2015) On the salty side of life: molecular, physiological and anatomical adaptation and acclimation of trees to extreme habitats. Plant Cell Environ 38:1794–1816PubMedCrossRefGoogle Scholar
  97. Polle A, Janz D, Teichmann T, Lipka V (2013) Poplar genetic engineering: promoting desirable wood characteristics and pest resistance. Appl Microbiol Biotechnol 97:5669–5679PubMedCrossRefGoogle Scholar
  98. Pontailler JY, Ceulemans R, Guittet J (1999) Biomass yield of poplar after five 2-year coppice rotations. Forestry 72:157–163Google Scholar
  99. Porth I, Klapšte J, Skyba O et al (2013a) Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. New Phytol 200:710–726PubMedCrossRefGoogle Scholar
  100. Porth I, Klápště J, Skyba O et al (2013b) Network analysis reveals the relationship among wood properties, gene expression levels and genotypes of natural Populus trichocarpa accessions. New Phytol 200:727–742PubMedCrossRefGoogle Scholar
  101. Powlson DS, Gregory PJ, Whalley WR et al (2011) Soil management in relation to sustainable agriculture and ecosystem services. Food Policy 36:S72–S87CrossRefGoogle Scholar
  102. Prado JR, Segers G, Voelker T et al (2014) Biotech crop development: from idea to product. Annu Rev Plant Biol 65:769–790PubMedCrossRefGoogle Scholar
  103. Rae AM, Pinel MPC, Bastien C et al (2007) QTL for yield in bioenergy Populus: identifying G × E interactions from growth at three contrasting sites. Tree Genet Genomes 4:97–112CrossRefGoogle Scholar
  104. Rae AM, Street NR, Robinson KM et al (2009) Five QTL hotspots for yield in short rotation coppice bioenergy poplar: the Poplar Biomass Loci. BMC Plant Biol 9:23PubMedPubMedCentralCrossRefGoogle Scholar
  105. Ray DK, Ramankutty N, Mueller ND et al (2012) Recent patterns of crop yield growth and stagnation. Nat Commun 3:1293PubMedCrossRefGoogle Scholar
  106. Resende MFR, Muñoz P, Acosta JJ et al (2012) Accelerating the domestication of trees using genomic selection: accuracy of prediction models across ages and environments. New Phytol 193:617–624PubMedCrossRefGoogle Scholar
  107. Rocha R, Barros E, Cruz C et al (2007) Mapping of QTLS related with wood quality and developmental characteristics in hybrids (Eucalyptus Grandis X Eucalyptus mapping of QTLS related with wood quality and developmental Characteristics In Hybrids (Eucalyptus Grandis X Madeira E Crescimento EM. Rev Arvore 31:13–24CrossRefGoogle Scholar
  108. Salmon J, Ward SP, Hanley SJ et al (2014) Functional screening of willow alleles in Arabidopsis combined with QTL mapping in willow (Salix) identifies SxMAX4 as a coppicing response gene. Plant Biotechnol J 12:480–491PubMedPubMedCentralCrossRefGoogle Scholar
  109. Samils B, Rönnberg-Wästljung AC, Stenlid J (2011) QTL mapping of resistance to leaf rust in Salix. Tree Genet Genomes 7:1219–1235CrossRefGoogle Scholar
  110. Scaracia-Mugnozza GE, Ceulemans R, Heilman PE et al (1997) Species and their hybrids grown under short rotation. II. Biomass components and harvest index of hybrid and parental species clones. Can J For Res 27:285–294CrossRefGoogle Scholar
  111. Schilling MP, Wolf PG, Duffy AM et al (2014) Genotyping-by-sequencing for populus population genomics: an assessment of genome sampling patterns and filtering approaches. PLoS One 9, e95292PubMedPubMedCentralCrossRefGoogle Scholar
  112. Schulte RPO, Creamer RE, Donnellan T et al (2014) Functional land management: a framework for managing soil-based ecosystem services for the sustainable intensification of agriculture. Environ Sci Policy 38:45–58CrossRefGoogle Scholar
  113. Serapiglia MJ, Cameron KD, Stipanovic AJ, Smart LB (2011) Correlations of expression of cell wall biosynthesis genes with variation in biomass composition in shrub willow (Salix spp.) biomass crops. Tree Genet Genomes 8:775–788CrossRefGoogle Scholar
  114. Serapiglia MJ, Cameron KD, Stipanovic AJ et al (2013) Yield and woody biomass traits of novel shrub willow hybrids at two contrasting sites. Bioenergy Res 6:533–546CrossRefGoogle Scholar
  115. Shankhwar AK, Srivastava RK (2015) Biomass production through grey water fertigation in eucalyptus hybrid and its economic significance. Environ Prog Sustain Energy 34:222–226CrossRefGoogle Scholar
  116. Shvaleva AL, Costa E, Silva F, Breia E et al (2006) Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiol 26:239–248PubMedCrossRefGoogle Scholar
  117. Silva-Junior OB, Grattapaglia D (2015) Genome-wide patterns of recombination, linkage disequilibrium and nucleotide diversity from pooled resequencing and single nucleotide polymorphism genotyping unlock the evolutionary history of Eucalyptus grandis. New Phytol 208:830–845PubMedCrossRefGoogle Scholar
  118. Silva-Junior OB, Faria DA, Grattapaglia D (2015) A flexible multi-species genome-wide 60K SNP chip developed from pooled resequencing of 240 Eucalyptus tree genomes across 12 species. New Phytol 206:1527–1540PubMedCrossRefGoogle Scholar
  119. Sims REH, Senelwa K, Maiava T, Bullock BT (1999) Eucalyptus species for biomass energy in New Zealand - part II: Coppice performance. Biomass and Bioenergy 17:333–343CrossRefGoogle Scholar
  120. Sims REH, Hastings A, Schlamadinger B et al (2006) Energy crops: current status and future prospects. Glob Chang Biol 12:2054–2076CrossRefGoogle Scholar
  121. Slavov GT, Difazio SP, Martin J et al (2012) Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 196:713–725PubMedCrossRefGoogle Scholar
  122. Somerville C, Youngs H, Taylor C et al (2010) Feedstocks for lignocellulosic biofuels. Science 329:790–792PubMedCrossRefGoogle Scholar
  123. Stape JL, Binkley D, Ryan MG (2008) Production and carbon allocation in a clonal Eucalyptus plantation with water and nutrient manipulations. For Ecol Manage 255:920–930CrossRefGoogle Scholar
  124. Steane DA, Nicolle D, Sansaloni CP et al (2011) Population genetic analysis and phylogeny reconstruction in Eucalyptus (Myrtaceae) using high-throughput, genome-wide genotyping. Mol Phylogenet Evol 59:206–224PubMedCrossRefGoogle Scholar
  125. Stewart JJ, Akiyama T, Chapple C et al (2009) The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol 150:621–635PubMedPubMedCentralCrossRefGoogle Scholar
  126. Stolarski MJ, Szczukowski S, Tworkowski J, Klasa A (2011) Willow biomass production under conditions of low-input agriculture on marginal soils. For Ecol Manage 262:1558–1566CrossRefGoogle Scholar
  127. Stolarski MJ, Szczukowski S, Tworkowski J, Klasa A (2013) Yield, energy parameters and chemical composition of short-rotation willow biomass. Ind Crops Prod 46:60–65CrossRefGoogle Scholar
  128. Street NR, Skogström O, Sjödin A et al (2006) The genetics and genomics of the drought response in Populus. Plant J 48:321–341PubMedCrossRefGoogle Scholar
  129. Studer MH, Demartini JD, Davis MF et al (2011) Lignin content in natural Populus variants affects sugar release. Proc Natl Acad Sci U S A 108:6300–6305PubMedPubMedCentralCrossRefGoogle Scholar
  130. Takagi H, Abe A, Yoshida K et al (2013) QTL-seq: Rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183PubMedCrossRefGoogle Scholar
  131. Teare MD (2011) Candidate gene association studies. In: Teare MD (ed) Genetic epidemeology. Humana Press, Totowa, NJ, pp 105–117CrossRefGoogle Scholar
  132. Terpstra IR, Snoek LB, Keurentjes JJB et al (2010) Regulatory network identification by genetical genomics: signaling downstream of the Arabidopsis receptor-like kinase ERECTA. Plant Physiol 154:1067–1078PubMedPubMedCentralCrossRefGoogle Scholar
  133. Thavamanikumar S, Tibbits J, McManus L et al (2011) Candidate gene-based association mapping of growth and wood quality traits in Eucalyptus globulus Labill. BMC Proc 5:O15PubMedCentralCrossRefGoogle Scholar
  134. Thavamanikumar S, McManus LJ, Ades PK et al (2014) Association mapping for wood quality and growth traits in Eucalyptus globulus ssp. globulus Labill identifies nine stable marker-trait associations for seven traits. Tree Genet Genomes 10:1661–1678CrossRefGoogle Scholar
  135. Tilman D, Balzer C, Hill J, Befort BL (2011) Global food demand and the sustainable intensification of agriculture. Proc Natl Acad Sci U S A 108:20260–20264PubMedPubMedCentralCrossRefGoogle Scholar
  136. Truax B, Gagnon D, Fortier J, Lambert F (2012) Yield in 8 year-old hybrid poplar plantations on abandoned farmland along climatic and soil fertility gradients. For Ecol Manage 267:228–239CrossRefGoogle Scholar
  137. Tullus A, Rytter L, Tullus T et al (2012) Short-rotation forestry with hybrid aspen (Populus tremula L. × P. tremuloides Michx.) in Northern Europe. Scand J Forensic Res 27:10–29CrossRefGoogle Scholar
  138. Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604PubMedCrossRefGoogle Scholar
  139. United Nations (2015) Adoption of the Paris AgreementGoogle Scholar
  140. Van Acker R, Leplé JC, Aerts D et al (2014) Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase. Proc Natl Acad Sci U S A 111:845–850PubMedCrossRefGoogle Scholar
  141. Van Ittersum MK, Cassman KG, Grassini P et al (2013) Yield gap analysis with local to global relevance: a review. Field Crop Res 143:4–17CrossRefGoogle Scholar
  142. Vanholme R, Storme V, Vanholme B et al (2012) A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24:3506–3529PubMedPubMedCentralCrossRefGoogle Scholar
  143. Verlinden MS, Broeckx LS, Ceulemans R (2015) First vs. Second rotation of a poplar short rotation coppice: above-ground biomass productivity and shoot dynamics. Biomass and Bioenergy 73:174–185CrossRefGoogle Scholar
  144. Vining K, Romanel E, Jones R et al (2015) The floral transcriptome of Eucalyptus grandis. New Phytol 206:1406–1422PubMedCrossRefGoogle Scholar
  145. Virlet N, Costes E, Martinez S et al (2015) Multispectral airborne imagery in the field reveals genetic determinisms of morphological and transpiration traits of an apple tree hybrid population in response to water deficit. J Exp Bot 66:5453–5465PubMedPubMedCentralCrossRefGoogle Scholar
  146. Volk TA, Abrahamson LP, Cameron KD et al (2011) Yields of willow biomass crops across a range of sites in North America. Asp Appl Biol 112:67–74Google Scholar
  147. Wang Y, Zhang B, Sun X et al (2011) Comparative genome mapping among Populus adenopoda, P. alba, P. deltoides, P. euramericana and P. trichocarpa. Genes Genet Syst 86:257–268PubMedCrossRefGoogle Scholar
  148. Wegrzyn JL, Eckert AJ, Choi M et al (2010) Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol 188:515–532PubMedCrossRefGoogle Scholar
  149. Weltecke K, Gaertig T (2012) Influence of soil aeration on rooting and growth of the Beuys-trees in Kassel, Germany. Urban For Urban Green 11:329–338CrossRefGoogle Scholar
  150. Wilkerson CG, Mansfield SD, Lu F et al (2014) Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 344(80):90–93PubMedCrossRefGoogle Scholar
  151. Wullschleger SD, Yin TM, Difazio SP et al (2005) Phenotypic variation in growth and biomass distribution for two advanced-generation pedigrees of hybrid poplar. Can J For Res 35:1779–1789CrossRefGoogle Scholar
  152. Xing Z, Maynard C (1995) Producing transgenic shining willow (Salix lucida Muhl.) shoots from stem segments via Agrobacterium tumefaciens transformation. Vitr Cell Dev Biol Plant 31:221–226Google Scholar
  153. Yin T, Zhang X, Huang M et al (2002) Molecular linkage maps of the Populus genome. Genome 45:541–555PubMedCrossRefGoogle Scholar
  154. Yu A, Gallagher T (2015) Analysis on the growth rhythm and cold tolerance of five-year old eucalyptus benthamii plantation for bioenergy. Open J For 5:585–592Google Scholar
  155. Yu S, Liao F, Wang F et al (2012) Identification of rice transcription factors associated with drought tolerance using the ecotilling method. PLoS One 7:1–9CrossRefGoogle Scholar
  156. Yu X, Kikuchi A, Matsunaga E et al (2013) Environmental biosafety assessment on transgenic Eucalyptus globulus harboring the choline oxidase (codA) gene in semi-confined condition. Plant Biotechnol 30:73–76CrossRefGoogle Scholar
  157. Zanchi G, Pena N, Bird N (2012) Is woody bioenergy carbon neutral? A comparative assessment of emissions from consumption of woody bioenergy and fossil fuel. GCB Bioenergy 4:761–772CrossRefGoogle Scholar
  158. Zhou X, Jacobs T, Xue L et al (2015) Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate : CoA ligase specificity and redundancy. New Phytol 208:298–301PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • G. Taylor
    • 1
    Email author
  • M. R. Allwright
    • 1
  • H. K. Smith
    • 1
  • A. Polle
    • 2
  • H. Wildhagen
    • 2
  • M. Hertzberg
    • 3
  • R. Bhalerao
    • 4
  • J. J. B. Keurentjes
    • 5
  • S. Scalabrin
    • 6
  • D. Scaglione
    • 6
  • M. Morgante
    • 7
  1. 1.Centre for Biological Sciences, Life Sciences Building, University of SouthamptonSouthamptonUK
  2. 2.Department of Forest Botany and Tree PhysiologyBüsgen Institute, Georg-August-UniversityGöttingenGermany
  3. 3.SweTree Technologies ABUmeåSweden
  4. 4.Department of Forest Genetics and Plant PhysiologyUmeå Plant Science Center, Swedish University of Agricultural SciencesUmeåSweden
  5. 5.Laboratory of GeneticsWageningen UniversityWageningenThe Netherlands
  6. 6.IGA Technology ServicesUdineItaly
  7. 7.Università Di Udine, Istituto die Genomica ApplicataUdineItaly

Personalised recommendations