Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter April 29, 2017

Biotechnology for bioenergy dedicated trees: meeting future energy demands

  • Hani Al-Ahmad EMAIL logo

Abstract

With the increase in human demands for energy, purpose-grown woody crops could be part of the global renewable energy solution, especially in geographical regions where plantation forestry is feasible and economically important. In addition, efficient utilization of woody feedstocks would engage in mitigating greenhouse gas emissions, decreasing the challenge of food and energy security, and resolving the conflict between land use for food or biofuel production. This review compiles existing knowledge on biotechnological and genomics-aided improvements of biomass performance of purpose-grown poplar, willow, eucalyptus and pine species, and their relative hybrids, for efficient and sustainable bioenergy applications. This includes advancements in tree in vitro regeneration, and stable expression or modification of selected genes encoding desirable traits, which enhanced growth and yield, wood properties, site adaptability, and biotic and abiotic stress tolerance. Genetic modifications used to alter lignin/cellulose/hemicelluloses ratio and lignin composition, towards effective lignocellulosic feedstock conversion into cellulosic ethanol, are also examined. Biotech-trees still need to pass challengeable regulatory authorities’ processes, including biosafety and risk assessment analyses prior to their commercialization release. Hence, strategies developed to contain transgenes, or to mitigate potential transgene flow risks, are discussed.

References

1. World Economic Forum. Energy Vision 2013, energy transitions: past and future, 2013. Available at: http://www3.weforum.org/docs/WEF_EN_EnergyVision_Report_2013.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

2. Asif M, Muneer T. Energy supply, its demand and security issues for developed and emerging economies. Renew Sust Energ Rev 2007;11:1388–413.10.1016/j.rser.2005.12.004Search in Google Scholar

3. Bessou C, Ferchaud F, Gabrielle B, Mary B. Biofuels, greenhouse gases and climate change. A review. Agron Sustain Dev 2011;31:1–79.10.1051/agro/2009039Search in Google Scholar

4. López-Bellido L, Wery J, López-Bellido RJ. Energy crops: prospects in the context of sustainable agriculture. Eur J Agron 2014;60:1–12.10.1016/j.eja.2014.07.001Search in Google Scholar

5. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA, et al. The path forward for biofuels and biomaterials. Science 2006;311:484–9.10.1126/science.1114736Search in Google Scholar PubMed

6. Haberl H, Beringer T, Bhattacharya SC, Erb K, Hoogwijk M. The global technical potential of bio-energy in 2050 considering sustainability constraints. Curr Opin Environ Sustain 2010;2:394–403.10.1016/j.cosust.2010.10.007Search in Google Scholar PubMed PubMed Central

7. Karp A, Richter GM. Meeting the challenge of food and energy security. J Exp Bot 2011;62:3263–71.10.1093/jxb/err099Search in Google Scholar PubMed

8. Dauber J, Brown C, Fernando AL, Finnan J, Krasuska E, Ponitka J, et al. Bioenergy from “surplus” land: environmental and socio-economic implications. BioRisk 2012;7:5–50.10.3897/biorisk.7.3036Search in Google Scholar

9. Djomo SN, El Kasmioui O, De Groote T, Broeckx LS, Verlinden MS, Berhongaray G, et al. Energy and climate benefits of bioelectricity from low-input short rotation woody crops on agricultural land over a two-year rotation. Appl Energy 2013;111:862–70.10.1016/j.apenergy.2013.05.017Search in Google Scholar

10. Hinchee M, Rottmann W, Mullinax L, Zhang C, Chang S, Cunningham M, et al. Short-rotation woody crops for bioenergy and biofuels applications. In Vitro Cell Dev Biol Plant 2009;45:619–29.10.1007/s11627-009-9235-5Search in Google Scholar PubMed PubMed Central

11. Balan V. Current challenges in commercially producing biofuels from lignocellulosic biomass. ISRN Biotechnol 2014;2014:463074.10.1155/2014/463074Search in Google Scholar PubMed PubMed Central

12. Poovaiah CR, Nageswara-Rao M, Soneji JR, Baxter HL, Stewart CN Jr. Altered lignin biosynthesis using biotechnology to improve lignocellulosic biofuel feedstocks. Plant Biotechnol J 2014;12:1163–73.10.1111/pbi.12225Search in Google Scholar PubMed

13. Welker CM, Balasubramanian VK, Petti C, Rai KM, DeBolt S, Mendu V. Engineering plant biomass lignin content and composition for biofuels and bioproducts. Energies 2015;8:7654–76.10.3390/en8087654Search in Google Scholar

14. US-DOE (U.S. Department of Energy). U.S. Billion-Ton Update: Biomass Supply for a Bioenergy and Bioproducts Industry. Perlack RD, Stokes BJ (Leads), ORNL/TM-2011/224. Oak Ridge National Laboratory, Oak Ridge, TN, USA, 2011. Available at: https://www1.eere.energy.gov/bioenergy/pdfs/billion_ton_update.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

15. Herr JR. Bioenergy from trees. The 26th New Phytol Symposium: bioenergy trees, INRA Nancy, France, 17–19 May. New Phytol 2011;192:313–5.10.1111/j.1469-8137.2011.03891.xSearch in Google Scholar PubMed

16. FAO. Global Forest Resources Assessment 2015: how are the world’s forests changing? Rome, Italy: Food and Agriculture Organization of the United Nations, 2015. Available at: http://www.fao.org/3/a-i4868e.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

17. Christersson L. Poplar plantations for paper and energy in the south of Sweden. Biomass Bioen 2008;32:997–1000.10.1016/j.biombioe.2007.12.018Search in Google Scholar

18. Rae AM, Street NR, Robenson KM, Harris N, Taylor G. Five QTL hotspots for yield in short rotation coppice bioenergy poplar: the poplar biomass loci. BMC Plant Biol 2009;9:23.10.1186/1471-2229-9-23Search in Google Scholar PubMed PubMed Central

19. Grattapaglia D, Resende MD. Genomic selection in forest tree breeding. Tree Genet Genomes 2011;7:241–55.10.1007/s11295-010-0328-4Search in Google Scholar

20. Harfouche A, Meilan R, Kirst M, Morgante M, Boerjan W, Sabatti M, et al. Accelerating the domestication of forest trees in a changing world. Trends Plant Sci 2012;17:64–72.10.1016/j.tplants.2011.11.005Search in Google Scholar PubMed

21. Burdon RD, Lstiburek M. Integrating genetically modified traits into tree improvement programmes. In: El-Kassaby YA, Prado JA, editors. Forests and genetically modified trees. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO), 2010:123–34.Search in Google Scholar

22. Walter C, Menzies M. Genetic modification as a component of forest biotechnology. In: El-Kassaby YA, Prado JA, editors. Forests and genetically modified trees. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO), 2010:3–18.Search in Google Scholar

23. Plomion C, Bastien C, Bogeat-Triboulot M-B, Bouffier L, Déjardin A, Duplessis S, et al. Forest tree genomics: 10 achievements from the past 10 years and future prospects. Ann For Sci 2016;73:77–103.10.1007/s13595-015-0488-3Search in Google Scholar

24. Abramson M, Shoseyov O, Shani Z. Plant cell wall reconstruction toward improved lignocellulosic production and processability. Plant Sci 2010;178:61–72.10.1016/j.plantsci.2009.11.003Search in Google Scholar

25. Harfouche A, Meilan R, Altman A. Tree genetic engineering and applications to sustainable forestry and biomass production. Trends Biotechnol 2011;29:9–17.10.1016/j.tibtech.2010.09.003Search in Google Scholar PubMed

26. Dubouzet JG, Strabala TJ, Wagner A. Potential transgenic routes to increase tree biomass. Plant Sci 2013;212:72–101.10.1016/j.plantsci.2013.08.006Search in Google Scholar PubMed

27. McDonnell LM, Coleman HD, French DG, Meilan R, Mansfield SD. Engineering trees with target traits. In: El-Kassaby YA, Prado JA, editors. Forests and genetically modified trees. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO), 2010:77–122.Search in Google Scholar

28. Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W. Lignin biosynthesis and structure. Plant Physiol 2010;153:895–905.10.1104/pp.110.155119Search in Google Scholar PubMed PubMed Central

29. Mansfield SD, Kang KY, Chapple C. Designed for deconstruction-poplar trees altered in cell wall lignification improve the efficacy of bioethanol production. New Phytol 2012;194:91–101.10.1111/j.1469-8137.2011.04031.xSearch in Google Scholar PubMed

30. Pauly M, Keegstra K. Plant cell wall polymers as precursors for biofuels. Curr Opin Plant Biol 2010;13:305–12.10.1016/j.pbi.2009.12.009Search in Google Scholar PubMed

31. Singh A, Pant D, Korres NE, Nizami AS, Prasad S, Murphy JD. Key issues in life cycle assessment of ethanol production from lignocellulosic biomass: challenges and perspectives. Bioresour Technol 2010;101:5003–12.10.1016/j.biortech.2009.11.062Search in Google Scholar PubMed

32. Bunn SM, Rae AM, Herbert CS, Taylor G. Leaf-level productivity traits in Populus grown in short rotation coppice for biomass energy. Forestry 2004;77:307–23.10.1093/forestry/77.4.307Search in Google Scholar

33. Sannigrahi P, Ragauskas AJ, Tuskan GA. Poplar as a feedstock for biofuels: a review of compositional characteristics. Biofuels Bioprod Bioref 2010;4:209–26.10.1002/bbb.206Search in Google Scholar

34. Kacik F, Durkovic J, Kacikova D. Chemical profiles of wood components of poplar clones for their energy utilization. Energies 2012;5:5243–56.10.3390/en5125243Search in Google Scholar

35. ORNL (Oak Ridge National Laboratory) Review. The people’s tree, 2007, Vol. 40, No. 1. Available at: http://web.ornl.gov/info/ornlreview/v40_1_07/article04.shtml. Accessed: 9 Mar 2017.Search in Google Scholar

36. Studer MH, DeMartini JD, Davis MF, Sykes RW, Davison B, Keller M, et al. Lignin content in natural Populus variants affects sugar release. Proc Natl Acad Sci USA 2011;108:6300–5.10.1073/pnas.1009252108Search in Google Scholar PubMed PubMed Central

37. Bose S, Francis R, Govender M, Bush T, Spark A. Lignin content versus syringyl to guaiacyl ratio amongst poplars. Bioresour Technol 2009;100:1628–33.10.1016/j.biortech.2008.08.046Search in Google Scholar PubMed

38. Mola-Yudego B. Regional potential yields of short rotation willow plantations on agricultural land in Northern Europe. Silva Fenn 2010;44:63–76.10.14214/sf.163Search in Google Scholar

39. Timmons D, Allen G, Damery D. Biomass energy crops: Massachusetts potential. Report prepared for Massachusetts Division of Energy Resources and Massachusetts, Department of Conservation and Recreation, 2008. Available at: http://www.mass.gov/eea/docs/doer/renewables/biomass/bio-ma-potential-crop.pdf. Last accessed: 9 Mar 2017Search in Google Scholar

40. Wickham J, Rice B, Finnan J, McConnon R. A review of past and current research on short rotation coppice in Ireland and abroad. COFORD, Dublin, 2010. Available at: http://www.coford.ie/media/coford/content/publications/projectreports/SRC.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

41. Verwijst T, Lundkvist A, Edelfeldt S, Albertsson J. Development of sustainable willow short rotation forestry in northern Europe. In: Matovic MD, editor. Biomass now – sustainable growth and use. Rijeka, Croatia, EU: InTech, 2013:481–502.Search in Google Scholar

42. Volk TA, Abrahamson LP, Cameron KD, Castellano P, Corbin T, Fabio E, et al. Yields of willow biomass crops across a range of sites in North America. Asp Appl Biol 2011;112:67–74.Search in Google Scholar

43. Guidi W, Pitre FE, Labrecque M. Short-rotation coppice of willows for the production of biomass in eastern Canada. In: Matovic MD, editor. Biomass now – sustainable growth and use. Rijeka, Croatia, EU: InTech, 2013:421–48.Search in Google Scholar

44. Volk TA, Buford M, Bergeson B, Caputo J, Eaton J, Perdue J, et al. Woody feedstocks – management and regional differences. In: Braun P, Karlen D, Johnson D, editors. Sustainable alternative feedstock opportunities, challenges and roadmap for 6 US regions. Soil Water Conserv Soc 2010:99–20.Search in Google Scholar

45. Ray M, Brereton NB, Shield I, Karp A, Murphy R. Variation in cell wall composition and accessibility in relation to biofuel potential of short rotation coppice willows. Bioenergy Res 2012;5:685–98.10.1007/s12155-011-9177-8Search in Google Scholar

46. Serapiglia MJ, Humiston MC, Xu H, Hogsett DA, de Orduña RM, Stipanovic AJ, et al. Enzymatic saccharification of shrub willow genotypes with differing biomass composition for biofuel production. Front Plant Sci 2013;4:57.10.3389/fpls.2013.00057Search in Google Scholar PubMed PubMed Central

47. Serapiglia M, Cameron K, Stipanovic A, Abrahamson L, Volk T, Smart L. Yield and woody biomass traits of novel shrub willow hybrids at two contrasting sites. Bioenergy Res 2013;6:533–46.10.1007/s12155-012-9272-5Search in Google Scholar

48. Budsberg E, Rastogi M, Puettmann ME, Caputo J, Balogh S, Volk TA, et al. Life-cycle assessment for the production of bioethanol from willow biomass crops via biochemical conversion. Forest Prod J 2012;62:305–13.10.13073/FPJ-D-12-00022.1Search in Google Scholar

49. Keoleian GA, Volk TA. Renewable energy from willow biomass crops: life cycle energy, environmental and economic performance. Crit Rev Plant Sci 2005;24:385–406.10.1080/07352680500316334Search in Google Scholar

50. Dougherty D, Wright J. Silviculture and economic evaluation of eucalypt plantations in the southern US. BioResources 2012;7:1994–2001.10.15376/biores.7.2.1994-2001Search in Google Scholar

51. Gonzalez R, Treasure T, Wright J, Saloni D, Phillips R, Abt R, et al. Exploring the potential for eucalyptus for energy production in the southern United States: financial analysis of delivered biomass. Part I. Biomass Bioen 2011;35:755–66.10.1016/j.biombioe.2010.10.011Search in Google Scholar

52. Stricker J, Rockwood D, Segrest S, Alker G, Prine G, Carter D. Short rotation woody crops for Florida. Paper presented to Third Biennial Conference, Short Rotation Woody Crops Operations Working Group, State University of New York, Syracuse, 2000. Available at: http://sfrc.ufl.edu/facultysites/rockwood/trees/SRWC-Syracuse%20NY.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

53. Dutt D, Tyagi CH. Comparison of various Eucalyptus species for their morphological, chemical, pulp and paper making characteristics. Ind J Chemical Technology 2011;18:145–51.Search in Google Scholar

54. Gonzalez R, Treasure T, Phillips R, Jameel H, Saloni D, Abt R, et al. Converting eucalyptus biomass into ethanol: financial and sensitivity analysis in a co-current dilute acid process. Part II. Biomass Bioen 2011;35:767–72.10.1016/j.biombioe.2010.10.025Search in Google Scholar

55. Hinchee MA, Mullinax LN, Rottmann WH. Woody biomass and purpose-grown trees as feedstocks for renewable energy. In: Mascia PN, Scheffran J, Widholm JM, editors. Plant biotechnology for sustainable production of energy and co-products, biotechnology in agriculture and forestry. Germany: Springer-Verlag, Berlin Heidelberg, Vol. 66, 2010:155–208.10.1007/978-3-642-13440-1_7Search in Google Scholar

56. Mercker D. Short rotation woody crops for biofuels. University of Tennessee Agricultural Experiment Station, 2007. Available at: https://extension.tennessee.edu/publications/Documents/SP702-C.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

57. Frederick WJ Jr, Lien SJ, Courchene CE, DeMartini NA, Ragauskas AJ, Iisa K. Production of ethanol from carbohydrates from loblolly pine: a technical and economic assessment. Bioresour Technol 2008;99:5051–7.10.1016/j.biortech.2007.08.086Search in Google Scholar PubMed

58. Gonzalez R, Treasure T, Phillips R, Jameel H, Saloni D. Economics of cellulosic ethanol production: Green liquor pretreatment for softwood and hardwood, greenfield and repurpose scenarios. BioResources 2011;6:2551–67.Search in Google Scholar

59. Lu S, Li L, Zhou G. Genetic modification of wood quality for second-generation biofuel production. GM Crops 2010;1:230–6.10.4161/gmcr.1.4.13486Search in Google Scholar PubMed

60. Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, et al. Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 2007;315:804–7.10.1126/science.1137016Search in Google Scholar PubMed

61. Li L, Lu S, Chiang V. A genomic and molecular view of wood formation. Crit Rev Plant Sci 2006;25:215–33.10.1080/07352680600611519Search in Google Scholar

62. Shi R, Sun YH, Li Q, Heber S, Sederoff R, Chiang VL. Towards a systems approach for lignin biosynthesis in Populus trichocarpa: transcript abundance and specificity of the mololignol biosynthetic genes. Plant Cell Physiol 2010;51:144–63.10.1093/pcp/pcp175Search in Google Scholar PubMed

63. Alvira P, Tomás-Pejó E, Ballesteros M, Negro MJ. Pretreatment technologies for an efficient bioethanol production process based on enzymatic hydrolysis: areview. Bioresour Technol 2010;101:4851–61.10.1016/j.biortech.2009.11.093Search in Google Scholar PubMed

64. Polle A, Janz D, Teichmann T, Lipka V. Poplar genetic engineering: promoting desirable wood characteristics and pest resistance. Appl Microbiol Biotechnol 2013;97:5669–79.10.1007/s00253-013-4940-8Search in Google Scholar PubMed

65. Vanholme R, Morreel K, Darrah C, Oyarce P, Grabber JH, Ralph J, et al. Metabolic engineering of novel lignin in biomass crops. New Phytol 2012;196:978–1000.10.1111/j.1469-8137.2012.04337.xSearch in Google Scholar PubMed

66. Van Acker R, Leplé JC, Aerts D, Storme V, Goeminne G, Ivens B, et al. Improved saccharification and ethanol yield from field-grown transgenic poplar deficient in cinnamoyl-CoA reductase. Proc Natl Acad Sci USA 2014;111:845–50.10.1073/pnas.1321673111Search in Google Scholar PubMed PubMed Central

67. Petrus L, Noordermeer MA. Biomass to biofuels, a chemical perspective. Green Chem 2006;8:861–7.10.1039/b605036kSearch in Google Scholar

68. Jansson M, Berglin N, Olm L. Second generation ethanol through alkaline fractionation of pine and aspen wood. Cellulose Chem Technol 2010;44:47–52.Search in Google Scholar

69. Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F, Davis MF, et al. Lignin valorization: improving lignin processing in the biorefinery. Science 2014;344:1246843.10.1126/science.1246843Search in Google Scholar PubMed

70. Henry RJ. Genomics for bioenergy production. In: Kole C, Joshi CP, Shonnard DR, editors. Handbook of bioenergy crop plants. Boca-Raton: CRC Press, 2012:21–9.10.1201/b11711-4Search in Google Scholar

71. Grattapaglia D, Plomion C, Kirst M, Sederoff RR. Genomics of growth traits in forest trees. Curr Opin Plant Biol 2009;12:148–56.10.1016/j.pbi.2008.12.008Search in Google Scholar PubMed

72. Neale DB, Kremer A. Forest tree genomics: growing resources and applications. Nature Rev Genet 2011;12:111–21.10.1038/nrg2931Search in Google Scholar

73. Neale D, Langley C, Salzberg S, Wegrzyn J. Open access to tree genomes: the path to a better forest. Genome Biol 2013;14:120.10.1186/gb-2013-14-6-120Search in Google Scholar PubMed

74. Hallingbäck H, Fogelqvist J, Powers S, Turrion-Gomez J, Rossiter R, Amey J, et al. Association mapping in Salix viminalis L. (Salicaceae) – identification of candidate genes associated with growth and phenology. Glob Change Biol Bioenergy 2016;8:670–85.10.1111/gcbb.12280Search in Google Scholar PubMed

75. Liberloo M, Luyssaert S, Bellassen V, Njakou Djomo S, Lukac M, Carlo Calfapietra C, et al. Bio-energy retains its mitigation potential under elevated CO2. PLoS One 2010;5:e11648.10.1371/journal.pone.0011648Search in Google Scholar PubMed

76. Tamm Ü. Populus tremula L. In: Schütt P, Weisgerber H, Schuck HJ, Lang UM, Stimm B, Roloff A, editors. Enzyklopädie der Laubbäume. Hamburg: Nikol, 2006:405–14.Search in Google Scholar

77. Kauter D, Lewandowski I, Claupein W. Quantity and quality of harvestable biomass from Populus short rotation coppice for solid fuel use – a review of the physiological basis and management influences. Biomass Bioen 2003;24:411–27.10.1016/S0961-9534(02)00177-0Search in Google Scholar

78. Somerville C, Youngs H, Taylor C, Davis SC, Long SP. Feedstocks for lignocellulosic biofuels. Science 2010;329:790–2.10.1126/science.1189268Search in Google Scholar PubMed

79. Ye X, Busov V, Zhao N, Meilan R, McDonnell LM, Coleman HD, et al. Transgenic Populus trees for forest products, bioenergy, and functional genomics. Crit Rev Plant Sci 2011;30:415–34.10.1080/07352689.2011.605737Search in Google Scholar

80. Xue LJ, Alabady MS, Mohebbi M, Tsai CJ. Exploiting genome variation to improve next-generation sequencing data analysis and genome editing efficiency in Populus tremula × alba 717-1B4. Tree Genet Genomes 2015;11:82.10.1007/s11295-015-0907-5Search in Google Scholar

81. Zhou X, Jacobs TB, Xue L-J, Harding SA, Tsai C-J. Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate: CoA ligase specificity and redundancy. New Phytol 2015;208:298–301.10.1111/nph.13470Search in Google Scholar PubMed

82. Kim YH, Kim MD, Choi YI, Park SC, Yun DJ, Noh EW, et al. Transgenic poplar expressing Arabidopsis NDPK2 enhances growth as well as oxidative stress tolerance. Plant Biotechnol J 2011;9:334–47.10.1111/j.1467-7652.2010.00551.xSearch in Google Scholar PubMed

83. Song J, Lu S, Chen ZZ, Lourenco R, Chiang VL. Genetic transformation of Populus trichocarpa genotype Nisqually-1: a functional genomic tool for woody plants. Plant Cell Physiol 2006;47:1582–89.10.1093/pcp/pcl018Search in Google Scholar PubMed

84. Jansson S, Douglas CJ. Populus: a model system for plant biology. Annu Rev Plant Biol 2007;58:435–58.10.1146/annurev.arplant.58.032806.103956Search in Google Scholar PubMed

85. Tuskan G, DiFazio S, Hellsten U, Jansson S, Rombauts S, Putnam N, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 2006;313:1596–604.10.1126/science.1128691Search in Google Scholar PubMed

86. Tuskan GA, DiFazio SP, Teichmann T. Poplar genomics is getting popular: the impact of the poplar genome project on tree research. Plant Biol 2004;6:2–4.10.1055/s-2003-44715Search in Google Scholar PubMed

87. Ralph SG, Chun HJ, Cooper D, Kirkpatrick R, Kolosova N, Gunter L, et al. Analysis of 4664 high-quality sequence-finished poplar full-length cDNA clones and their utility for the discovery of genes responding to insect feeding. BMC Genomics 2008;9:57.10.1186/1471-2164-9-57Search in Google Scholar PubMed PubMed Central

88. Yevtushenko DP, Misra S. Efficient Agrobacterium-mediated transformation of commercial hybrid poplar Populus nigra L. × P. maximowiczii A. Henry. Plant Cell Rep 2010;29:211–21.10.1007/s00299-009-0806-zSearch in Google Scholar PubMed

89. Han X, Ma S, Kong X, Takano T, Liu S. Efficient Agrobacterium-mediated transformation of hybrid poplar Populus davidiana Dode × Populus bollena Lauche. Int J Mol Sci 2013;14:2515–28.10.3390/ijms14022515Search in Google Scholar PubMed PubMed Central

90. Zhou J, Wang J, Bi Y, Wang L, Tang L, Yu X, et al. Overexpression of PtSOS2 enhances salt tolerance in transgenic poplars. Plant Mol Biol Rep 2014;32:185–97.10.1007/s11105-013-0640-xSearch in Google Scholar PubMed

91. Movahedi A, Zhang J, Gao P, Yang Y, Wang L, Yin T, et al. Expression of the chickpea CarNAC3 gene enhances salinity and drought tolerance in transgenic poplars. Plant Cell Tiss Organ Cult 2015;120:141–54.10.1007/s11240-014-0588-zSearch in Google Scholar

92. Benedict C, Skinner JS, Meng R, Chang Y, Bhalerao R, Huner NP, et al. The CBF1-dependent low temperature signaling pathway, regulon and increase in freeze tolerance are conserved in Populus spp. Plant Cell Environ 2006;29:1259–72.10.1111/j.1365-3040.2006.01505.xSearch in Google Scholar PubMed

93. Klocko AL, Meilan R, James RR, Viswanath V, Ma C, Payne P, et al. Bt-Cry3Aa transgene expression reduces insect damage and improves growth in field-grown hybrid poplar. Can J For Res 2014;44:28–35.10.1139/cjfr-2013-0270Search in Google Scholar

94. James C. Global Status of Commercialized Biotech/GM Crops: 2015. ISAAA Brief No. 51. Ithaca, New York: ISAAA, 2015.Search in Google Scholar

95. Man HM, Boriel R, El-Khatib R, Kirby EG. Characterization of transgenic poplar with ectopic expression of pine cytosolic glutamine synthetase under conditions of varying nitrogen availability. New Phytol 2005;167:31–9.10.1111/j.1469-8137.2005.01461.xSearch in Google Scholar PubMed

96. Pascual MB, Jing ZP, Kirby EG, Cánovas FM, Gallardo F. Response of transgenic poplar overexpressing cytosolic glutamine synthetase to phosphinothricin. Phytochemistry 2008;69:382–9.10.1016/j.phytochem.2007.07.031Search in Google Scholar PubMed

97. Bernard SM, Habash DZ. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 2009;182:608–20.10.1111/j.1469-8137.2009.02823.xSearch in Google Scholar PubMed

98. Coleman HD, Cánovas FM, Man H, Kirby EG, Mansfield SD. Enhanced expression of glutamine synthetase (GS1a) confers altered fiber and wood chemistry in field grown hybrid poplar (Populus tremula × alba) (717-1B4). Plant Biotechnol J 2012;10:883–9.10.1111/j.1467-7652.2012.00714.xSearch in Google Scholar

99. Park YW, Baba K, Furuta Y, Iida I, Sameshima K, Arai M, et al. Enhansement of growth and cellulose accumulation by overexpression of xyloglucanase in poplar. FEBS Lett 2004;564:183–7.10.1016/S0014-5793(04)00346-1Search in Google Scholar PubMed

100. Taniguchi T, Konagaya K, Kurita M, Takata N, Ishii K, Kondo T, et al. Growth and root sucker ability of field-grown transgenic poplars overexpressing xyloglucanase. J Wood Sci 2012;58:550–6.10.1007/s10086-012-1281-7Search in Google Scholar

101. Funahashi F, Ohta S, Taniguchi T, Kurita M, Konagaya K, Hayashi T. Architectural and physiological characteristics related to the depressed growth of poplars overexpressing xyloglucanase in a field study. Trees 2014;28:65–76.10.1007/s00468-013-0930-9Search in Google Scholar

102. Shani Z, Dekel M, Tsabary G, Goren R, Shoseyov O. Growth enhancement of transgenic poplar plants by over expression of Arabidopsis thaliana endo-1, 4-β-glucanase (cel1). Mol Breed 2004;14:321–30.10.1023/B:MOLB.0000049213.15952.8aSearch in Google Scholar

103. Gray-Mitsumune M, Blomquist K, McQueen-Mason S, Teeri TT, Sundberg B, Mellerowicz EJ. Ectopic expression of a wood-abundant expansin PttEXPA1 promotes cell expansion in primary and secondary tissues in aspen. Plant Biotechnol J 2008;6:62–72.10.1111/j.1467-7652.2007.00295.xSearch in Google Scholar PubMed

104. Sakamoto S, Takata N, Oshima Y, Yoshida K, Taniguchi T, Mitsuda N. Wood reinforcement of poplar by rice NAC transcription factor. Sci Rep 2016;6:19925.10.1038/srep19925Search in Google Scholar PubMed PubMed Central

105. Elias AA, Busov VB, Kosola KR, Ma C, Etherington E, Shevchenko O, et al. Green revolution trees: semidwarfism transgenes modify gibberellins, promote root growth, enhance morphological diversity, and reduce competitiveness in hybrid poplar. Plant Physiol 2012;160:1130–44.10.1104/pp.112.200741Search in Google Scholar PubMed PubMed Central

106. Hu WJ, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, et al. Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nature Biotechnol 1999;17:808–12.10.1038/11758Search in Google Scholar PubMed

107. Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J, et al. Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci USA 2003;100:4939–44.10.1073/pnas.0831166100Search in Google Scholar PubMed PubMed Central

108. Voelker SL, Lachenbruch B, Meinzer FC, Jourdes M, Ki C, Patten AM, et al. Antisense down-regulation of 4CL expression alters lignification, tree growth, and saccharification potential of field-grown poplar. Plant Physiol 2010;154:874–86.10.1104/pp.110.159269Search in Google Scholar PubMed PubMed Central

109. Stout A, Davis AA, Domec JC, Yang C, Shi R, King JS. Growth under field conditions affects lignin content and productivity in transgenic Populus trichocarpa with altered lignin biosynthesis. Biomass Bioen 2014;68:228–39.10.1016/j.biombioe.2014.06.008Search in Google Scholar

110. Leplé J-C, Dauwe R, Morreel K, Storme V, Lapierre C, Pollet B, et al. Downregulation of cinnamoyl-coenzyme A reductase in poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 2007;19:3669–91.10.1105/tpc.107.054148Search in Google Scholar PubMed PubMed Central

111. Jouanin L, Goujon T, de Nadaï V, Martin M-T, Mila I, Vallet C, et al. Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity. Plant Physiol 2000;123:1363–73.10.1104/pp.123.4.1363Search in Google Scholar PubMed PubMed Central

112. Humphreys JM, Hemm MR, Chapple C. New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc Natl Acad Sci USA 1999;96:10045–50.10.1073/pnas.96.18.10045Search in Google Scholar PubMed PubMed Central

113. Franke R, McMichael CM, Meyer K, Shirley AM, Cusumano JC, Chapple C. Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J 2000;22:223–34.10.1046/j.1365-313x.2000.00727.xSearch in Google Scholar PubMed

114. Huntley SK, Ellis D, Gilbert M, Chapple C, Mansfield SD. Significant increases in pulping efficiency in C4H-F5H-transformed poplars: improved chemical savings and reduced environmental toxins. J Agric Food Chem 2003;51:6178–83.10.1021/jf034320oSearch in Google Scholar PubMed

115. Stewart JJ, Akiyama T, Chapple C, Ralph J, Mansfield SD. The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol 2009;150: 621–35.10.1104/pp.109.137059Search in Google Scholar PubMed PubMed Central

116. Coleman HD, Park JY, Nair R, Chapple C, Mansfield SD. RNAi-mediated suppression of p-coumaroyl-CoA 3′-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc Natl Acad Sci USA 2008;105:4501–6.10.1073/pnas.0706537105Search in Google Scholar PubMed PubMed Central

117. Biswal AK, Hao Z, Pattathil S, Yang X, Winkeler K, Collins C, et al. Downregulation of GAUT12 in Populus deltoides by RNA silencing results in reduced recalcitrance, increased growth and reduced xylan and pectin in a woody biofuel feedstock. Biotechnol. Biofuels 2015;8:41.10.1186/s13068-015-0218-ySearch in Google Scholar PubMed PubMed Central

118. Bryan AC, Jawdy S, Gunter L, Gjersing E, Sykes R, Hinchee MA, et al. Knockdown of a laccase in Populus deltoides confers altered cell wall chemistry and increased sugar release. Plant Biotechnol J 2016;14:2010–20.10.1111/pbi.12560Search in Google Scholar PubMed PubMed Central

119. Tolbert AK, Ma T, Kalluri UC, Ragauskas AJ. Determining the syringyl/guaiacyl lignin ratio in the vessel and fiber cell walls of transgenic Populus plants. Energ Fuel 2016;30:5716–20.10.1021/acs.energyfuels.6b00560Search in Google Scholar

120. Kalluri UC, Payyavula R, Labbé J, Engle N, Bali G, Jawdy SS, et al. Down-regulation of KORRIGAN-like endo-β-1,4-glucanase genes impacts carbon partitioning, mycorrhizal colonization and biomass production in Populus. Front Plant Sci 2016;7:1455.10.3389/fpls.2016.01455Search in Google Scholar PubMed PubMed Central

121. Hjältén J, Lindau A, Wennström A, Blomberg P, Witzell J, Hurry V, et al. Unintentional changes of defense traits in GM trees can influence plant-herbivore interactions. Basic Appl Ecol 2007;8:434–43.10.1016/j.baae.2006.09.001Search in Google Scholar

122. Smith RA, Gonzales-Vigil E, Karlen SD, Park J-Y, Lu F, Wilkerson CG, et al. Engineering monolignol p-coumarate conjugates into poplar and arabidopsis lignins. Plant Physiol 2015;169:2992–3001.10.1104/pp.15.00815Search in Google Scholar PubMed PubMed Central

123. Karlen SD, Zhang C, Peck ML, Smith RA, Padmakshan D, Helmich KE, et al. Monolignol ferulate conjugates are naturally incorporated into plant lignins. Sci Adv 2016;2:e1600393.10.1126/sciadv.1600393Search in Google Scholar PubMed PubMed Central

124. Wilkerson CG, Mansfield SD, Lu F, Withers S, Park J-Y, Karlen SD, et al. Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 2014;344:90–3.10.1126/science.1250161Search in Google Scholar PubMed

125. Cai Y, Zhang K, Kim H, Hou G, Zhang X, Yang H, et al. Enhancing digestibility and ethanol yield of Populus wood via expression of an engineered monolignol 4-O-methyltransferase. Nat Commun 2016;7:11989.10.1038/ncomms11989Search in Google Scholar PubMed PubMed Central

126. Argus GW. Infrageneric classification of Salix (Salicaceae) in the New World. Syst Bot Monogr 1997;52:1–121.10.2307/25096638Search in Google Scholar

127. Kuzovkina YA, Weih M, Romero MA, Charles J, Hurst S, McIvor I, et al. Salix: botany and global horticulture. Hortic Rev 2008;34:447–89.10.1002/9780470380147.ch8Search in Google Scholar

128. Karp A, Hanley SJ, Trybush SO, Macalpine W, Pei M, Shield I. Genetic improvement of willow for bioenergy and biofuels. J Integr Plant Biol 2011;53:151–65.10.1111/j.1744-7909.2010.01015.xSearch in Google Scholar PubMed

129. Hanley SJ, Karp A. Genetic strategies for dissecting complex traits in biomass willows (Salix spp.). Tree Physiol 2013;34:1167–80.10.1093/treephys/tpt089Search in Google Scholar PubMed

130. Perdereau AC, Douglas GC, Hodkinson TR, Kelleher CT. High levels of variation in Salix lignocellulose genes revealed using poplar genomic resources. Biotechnol Biofuels 2013;6:114.10.1186/1754-6834-6-114Search in Google Scholar PubMed PubMed Central

131. Serapiglia MJ, Gouker FE, Hart JF, Unda F, Mansfield SD, Stipanovic AJ, et al. Ploidy level affects important biomass traits of novel shrub willow (Salix) hybrids. Bioenergy Res 2015;8:259–69.10.1007/s12155-014-9521-xSearch in Google Scholar

132. Fabio ES, Volk TA, Miller RO, Serapiglia MJ, Gauch HG, Van Rees KC, et al. Genotype x environment interactions analysis of North American shrub willow yield trials confirms superior performance of triploid hybrids. Glob Change Biol Bioenergy 2017;9:445–59.10.1111/gcbb.12344Search in Google Scholar

133. Stephenson AL, Dupree P, Scott SA, Dennis JS. The environmental and economic sustainability of potential bioethanol from willow in the UK. Bioresour Technol 2010;101:9612–23.10.1016/j.biortech.2010.07.104Search in Google Scholar PubMed

134. Brereton NJ, Pitre FE, Ray MJ, Karp A, Murphy RJ. Investigation of tension wood formation and 2,6-dichlorbenzonitrile application in short rotation coppice willow composition and enzymatic saccharification. Biotechnol Biofuels 2011;4:13.10.1186/1754-6834-4-13Search in Google Scholar PubMed

135. Berlin S, Ghelardini L, Bonosi L, Weih M, Rönnberg-Wästljung AC. QTL mapping of biomass and nitrogen economy traits in willows (Salix spp.) grown under contrasting water and nutrient conditions. Mol Breed 2014;34:1987–2003.10.1007/s11032-014-0157-5Search in Google Scholar

136. Németh AV, Dudits D, Molnár-Láng M, Linc G. Molecular cytogenetic characterisation of Salix viminalis L. using repetitive DNA sequences. J Appl Genetics 2013;54:265–9.10.1007/s13353-013-0153-1Search in Google Scholar

137. Berlin S, Lagercrantz U, von Arnold S, Öst T, Rönnberg-Wästljung AC. High-density linkage mapping and evolution of paralogs and orthologs in Salix and Populus. BMC Genomics 2010;11:129.10.1186/1471-2164-11-129Search in Google Scholar PubMed

138. Grönroos L, Von Arnold S. Eriksson T. Callus production and somatic embryogenesis from floral explants of basket willow (Salix viminalis L.). J Plant Physiol 1989;134:558–66.10.1016/S0176-1617(89)80147-6Search in Google Scholar

139. Vahala T, Stabel P, Eriksson T. Genetic transformation of willows (Salixs spp.) by Agrobacterium tumefaciens. Plant Cell Rep 1989;8:55–8.10.1007/BF00716837Search in Google Scholar PubMed

140. Vahala T, Eriksson T, Tillberg E, Nicander B. Expression of a cytokinin synthesis gene from Agrobacterium tumefaciens T-DNA basket willow (Salix viminalis). Physiol Plant 1993;88:439–45.10.1111/j.1399-3054.1993.tb01357.xSearch in Google Scholar

141. Park SY, Kim YW, Moon HK, Murthy HN, Choi YH, Cho HM. Micropropagation of Salix pseudolasiogyne from nodal explants. Plant Cell Tiss Organ Cult 2008;93:341–6.10.1007/s11240-008-9362-4Search in Google Scholar

142. Skálová D, Navrátilová B, Richterová L, Knitl M, Sochor M, Vašut RJ. Biotechnological methods of in vitro propagation in willows (Salix spp.). Cent Eur J Biol 2012;7:931–40.10.2478/s11535-012-0069-5Search in Google Scholar

143. Yang J, Yi J, Yang C, Li C. Agrobacterium tumefaciens-mediated genetic transformation of Salix matsudana Koidz. using mature seeds. Tree Physiol 2013;33:628–39.10.1093/treephys/tpt038Search in Google Scholar PubMed

144. Henry RJ, Kole C. Genetics, genomics and breeding of eucalypts. Boca Raton: CRC Press, 2015:206.10.1201/b17154Search in Google Scholar

145. Trabedo GI, Wilshermann D. Eucalyptus Universalis. Global Cultivated Eucalypt Forests Map 2009. Available at: http://git-forestry.com/download_git_eucalyptus_map.htm. Last accessed: 9 Mar 2017.Search in Google Scholar

146. Rockwood DL, Rudie AW, Ralph SA, Zhu JY, Winandy JE. Energy product options for eucalyptus species grown as short rotation woody crops. Int J Mol Sci 2008;9:1361–78.10.3390/ijms9081361Search in Google Scholar PubMed PubMed Central

147. Teulieres C, Marque C. Eucalyptus. In: Pua EC, Davey MR, editors. Biotechnology in agriculture and forestry, Transgenic Crops V. New York: Springer, Vol. 60, 2007:387–402.Search in Google Scholar

148. Gonzalez R, Wright J, Saloni D. The business of growing eucalyptus for biomass. Biomass Magazine 2010;4:52–6.Search in Google Scholar

149. Domingues RM, Patinha DJ, Sousa GD, Villaverde JJ, Silva CM, Freire CS, et al. Eucalyptus biomass residues from agro-forest and pulping industries as sources of high-value triterpenic compounds. Cellulose Chem Technol 2011;45:475–81.Search in Google Scholar

150. Healey AL, Lee DJ, Furtado A, Simmons BA, Henry RJ. Efficient eucalypt cell wall deconstruction and conversion for sustainable lignocellulosic biofuels. Front Bioeng Biotechnol 2015;3:190.10.3389/fbioe.2015.00190Search in Google Scholar PubMed PubMed Central

151. Rezende GD, de Resende MD, de Assis TF. Eucalyptus breeding for clonal forestry. In: Fenning T, editor. Challenges and opportunities for the world’s forests in the 21st century, forestry sciences. Netherlands: Springer, Vol. 81, 2014:393–424.Search in Google Scholar

152. Pinto G, Araújo C, Santos C, Neves L. Plant regeneration by somatic embryogenesis in Eucalyptus spp.: current status and future perspectives. South For 2013;75:59–69.10.2989/20702620.2013.785115Search in Google Scholar

153. Girijashankar V. Genetic transformation of Eucalyptus. Physiol Mol Biol Plants 2011;17:9–23.10.1007/s12298-010-0048-0Search in Google Scholar PubMed PubMed Central

154. Carocha V, Soler M, Hefer CA, Cassan-Wang H, Fevereiro P, Myburg AA, et al. Genome-wide analysis of the lignin toolbox of Eucalyptus grandis. New Phytol 2015;206:1297–313.10.1111/nph.13313Search in Google Scholar PubMed

155. Plasencia A, Soler M, Dupas A, Ladouce N, Silva-Martins G, Martinez Y, et al. Eucalyptus hairy roots, a fast, efficient and versatile tool to explore function and expression of genes involved in wood formation. Plant Biotechnol J 2016;14:1381–93.10.1111/pbi.12502Search in Google Scholar PubMed

156. Grattapaglia D, Kirst M. Eucalyptus applied genomics: from gene sequences to breeding tools. New Phytol 2008;179:911–29.10.1111/j.1469-8137.2008.02503.xSearch in Google Scholar PubMed

157. Bartholomé J, Mandrou E, Mabiala A, Jenkins J, Nabihoudine I, Klopp C, et al. High-resolution genetic maps of Eucalyptus improve Eucalyptus grandis genome assembly. New Phytol 2015;206:1283–96.10.1111/nph.13150Search in Google Scholar PubMed

158. Ribeiro T, Barrela RM, Bergès H, Marques C, Loureiro J, Morais-Cecilio L, et al. Advancing Eucalyptus genomics: cytogenomics reveals conservation of Eucalyptus genomes. Front Plant Sci 2016;7:510.10.3389/fpls.2016.00510Search in Google Scholar PubMed PubMed Central

159. Shani Z, Dekel M, Cohen B, Barimboim N, Kolosovski N, Safranuvitch A, et al. Cell wall modification for the enhancement of commercial Eucalyptus species. In: Sundberg B, editor. Proceedings of the Conference on IUFRO Tree biotechnology. Umea, Sweden: Umea Plant Science Center, 2003:S10–26.Search in Google Scholar

160. Shani Z, Dekel M, Cohen B, Barimboim N, Cohen O, Halay T, et al. Eucalyptus in the changing world. In: Borralho N, editor. Proceedings of the International IUFRO conference. Aveiro, Portugal: The International Union of Forest Research Organizations (IUFRO), 2004:668.Search in Google Scholar

161. Sonoda T, Koita H, Nakamoto-Ohta S, Kondo K, Suezaki T, Kato T, et al. Increasing fiber length and growth in transgenic tobacco plants overexpressing a gene encoding the Eucalyptus camaldulensis HD-Zip class II transcription factor. Plant Biotechnol 2009;26:115–20.10.5511/plantbiotechnology.26.115Search in Google Scholar

162. Ledford H. Brazil considers transgenic trees. Nature 2014;512:357.10.1038/512357aSearch in Google Scholar PubMed

163. Harcourt RL, Kyozuka J, Floyd RB, Bateman KS, Tanaka H, Decroocq V, et al. Insect- and herbicide-resistant transgenic eucalypts. Mol Breed 2000;6:307–15.10.1023/A:1009676214328Search in Google Scholar

164. Nambiar-Veetil M, Sangeetha M, Rani KS, Aravinthakumar V, Selvakesavan RK, Balasubramanian A, et al. Identification of insect-specific target genes for development of RNAi based control of the Eucalyptus gall pest Leptocybe invasa Fisher & La Salle (Hymenoptera: Eulophidae). BMC Proc 2011;5:98.10.1186/1753-6561-5-S7-P98Search in Google Scholar

165. Shao Z, Chen W, Luo H, Ye X, Zhan J. Studies on the introduction of cecropin D gene into Eucalyptus urophylla to breed the resistant varieties to Pseudomonas solaniacearum. Sci Silvae Sin 2002;38:92–7.Search in Google Scholar

166. Yamada-Watanabe K, Kawaoka A, Matsunaga K, Nanto K, Sugita K, Endo S, et al. Molecular breeding of Eucalyptus: analysis of salt stress tolerance in transgenic Eucalyptus camaldulensis that over-expressed choline oxidase gene (codA). In: Sundberg B, editor. IUFRO Tree Biotechnology. Umea, Sweden: Umea Plant Science Centre, 2003:S7–9.Search in Google Scholar

167. Yu X, Kikuchi A, Matsunaga E, Morishita Y, Nanto K, Sakurai N, et al. Establishment of the evaluation system of salt tolerance on transgenic woody plants in the special netted-house. Plant Biotechnol 2009;26:135–41.10.5511/plantbiotechnology.26.135Search in Google Scholar

168. Kawazu T, Susuki Y, Wada T, Kondo K, Koyama H. Over expression of a plant mitochondrial citrate synthase in eucalyptus trees improved growth when cultured by alphosphate as a sole phosphate source. Plant Cell Physiol 2003;44:S91.Search in Google Scholar

169. Navarro M, Ayax C, Martinez Y, Laur J, El Kayal W, Marque C, et al. Two EguCBF1 genes overexpressed in Eucalyptus display a different impact on stress tolerance and plant development. Plant Biotechnol J 2011;9:50–63.10.1111/j.1467-7652.2010.00530.xSearch in Google Scholar PubMed

170. Chen ZZ, Chang SH, Ho CK, Chen YC, Tsai JB, Chiang VL. Plant production of transgenic Eucalyptus camaldulensis carrying the Populus tremuloides cinnamate 4-hydroxylase gene. Taiwan J For Sci 2001;16:249–58.Search in Google Scholar

171. Sykes RW, Gjersing EL, Foutz K, Rottmann WH, Kuhn SA, Foster CE, et al. Down-regulation of p-coumaroyl quinate/shikimate 3′-hydroxylase (C3′H) and cinnamate 4-hydroxylase (C4H) genes in the lignin biosynthetic pathway of Eucalyptus urophylla × E. grandis leads to improved sugar release. Biotechnol Biofuels 2015;8:128.10.1186/s13068-015-0316-xSearch in Google Scholar PubMed PubMed Central

172. Tournier V, Grat S, Marque C, El Kayal W, Penchel R, Andrade DG, et al. An efficient procedure to stably introduce genes into an economically important pulp tree (Eucalyptus grandis × Eucalyptus urophylla). Trans Res 2003;12:403–11.10.1023/A:1024217910354Search in Google Scholar

173. Valerio L, Carter D, Rodrigues JC, Tournier V, Gominho J, Marque C, et al. Down regulation of cinnamyl alcohol dehydrogenase, a lignification enzyme, in Eucalyptus camaldulensis. Mol Breed 2003;12:157–67.10.1023/A:1026070725107Search in Google Scholar

174. Kawaoka A, Nanto K, Ishii K, Ebinuma H. Reduction of lignin content by suppression of expression of the LIM domain transcription factor in Eucalyptus camaldulensis. Silvae Genet 2006;55:269–77.10.1515/sg-2006-0035Search in Google Scholar

175. Gernandt DS, Lopez GG, Garcia SO, Liston A. Phylogeny and classification of Pinus. Taxon 2005;54:29–42.10.2307/25065300Search in Google Scholar

176. Peter GF. Southern pines: a resource for bioenergy. In: Vermerris W, editor. Genetic improvement of bioenergy crops. New York: Springer, 2008:397–419.Search in Google Scholar

177. Trontin JF, Walter C, Klimaszewska K, Park YS, Lelu-Walter MA. Recent progress in genetic transformation of four Pinus spp. Transgenic Plant J 2007;1:314–29.Search in Google Scholar

178. Nehra NS, Becwar MR, Rottmann WH, Pearson L, Chowdhury K, Chang S, et al. Forest biotechnology: innovative methods, emerging opportunities. In Vitro Cell and Dev Biol Plant 2005;41:701–17.10.1079/IVP2005691Search in Google Scholar

179. Lev-Yadun S, Sederoff R. Pines as model gymnosperms to study evolution, wood formation, and perennial growth. J Plant Growth Regul 2000;19:290–305.10.1007/s003440000045Search in Google Scholar

180. Papa G, Kirby J, Konda NV, Tran K, Singh S, Keasling J, et al. Development of an integrated approach for α-pinene recovery and sugar production from loblolly pine using ionic liquids. Green Chem 2017;19:1117–27.10.1039/C6GC02637KSearch in Google Scholar

181. English BC, De La Torre, Ugarte DG, Jensen K, Hellwinckel C, Menard J, et al. 25% Renewable energy for the United States by 2025: agricultural and economic impacts. University of Tennessee Agricultural Economics, 2006. Available at: http://beag.ag.utk.edu/pub/Report%2025X25nov142006.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

182. Connett-Porceddu MB, Gladfelter HJ, Gulledge JE, McCormack RR. Enhanced transformation and regeneration of transformed embryogenic pine tissue. Patent N° 7,157,620 B2, USA, 2007.Search in Google Scholar

183. Li B, McKeand S, Weir R. Tree improvement and sustainable forestry-impact of two cycles of loblolly pine breeding in the U.S.A. For Genet 1999;6:229–34.Search in Google Scholar

184. Neale D, Wegrzyn J, Stevens K, Zimin A, Puiu D, Crepeau M, et al. Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol 2014;15:R59.10.1186/gb-2014-15-3-r59Search in Google Scholar PubMed PubMed Central

185. Zimin A, Stevens KA, Crepeau MW, Holtz-Morris A, Koriabine M, Marcais G, et al. Sequencing and assembly of the 22-gb loblolly pine genome. Genetics 2014;196:875–90.10.1534/genetics.113.159715Search in Google Scholar PubMed PubMed Central

186. González-Martínez SC, Wheeler NC, Ersoz E, Nelson CD, Neale DB. Association genetics in Pinus taeda L. I. Wood property traits. Genetics 2007;175:399–409.10.1534/genetics.106.061127Search in Google Scholar PubMed PubMed Central

187. Neves LG, Davis JM, Barbazuk WB, Kirst M. A high-density gene map of loblolly pine (Pinus taeda L.) based on exome sequence capture genotyping. G3 (Bethesda) 2014;4:29–37.10.1534/g3.113.008714Search in Google Scholar PubMed PubMed Central

188. Alvarez JM, Ordás RJ. Stable Agrobacterium-mediated transformation of maritime pine based on kanamycin selection. ScientificWorldJ 2013;2013:681792.10.1155/2013/681792Search in Google Scholar PubMed PubMed Central

189. Tang W, TianY. Transgenic loblolly pine (Pinus taeda L.) plants expressing a modified δ-endotoxin gene of Bacillus thuringiensis with enhanced resistance to Dendrolimus punctatus Walker and Crypyothelea formosicola Staud. J Exp Bot 2003;54:835–44.10.1093/jxb/erg071Search in Google Scholar PubMed

190. Grace LJ, Charity JA, Gresham B, Kay N, Walter C. Insect resistance transgenic Pinus radiata. Plant Cell Rep 2005;24:103–11.10.1007/s00299-004-0912-xSearch in Google Scholar PubMed

191. Osakabe Y, Kawaoka A, Nishikubo N, Osakabe K. Responses to environmental stresses in woody plants: key to survive and longevity. J Plant Res 2012;125:1–10.10.1007/s10265-011-0446-6Search in Google Scholar PubMed

192. Harfouche A, Meilan R, Altman A. Molecular and physiological responses to abiotic stress in forest trees and their relevance to tree improvement. Tree Physiol 2014;34:1181–98.10.1093/treephys/tpu012Search in Google Scholar PubMed

193. Tang W, Newton RJ, Li C, Charles TM. Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis. Plant Cell Rep 2007;26:115–24.10.1007/s00299-006-0228-0Search in Google Scholar PubMed

194. Bonawitz ND, Chapple C. The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 2010;44:337–63.10.1146/annurev-genet-102209-163508Search in Google Scholar PubMed

195. Wagner A, Donaldson L, Ralph J. Lignification and lignin manipulations in Conifers. In: Jouanin L, Lapierre C, editors. Advances in botanical research. Burlington, VT: Academic Press, Vol. 61, 2012:37–76.Search in Google Scholar

196. Wu RL, Remington DL, MacKay JJ, McKeand SE, O’Malley DM. Average effect of a mutation in lignin biosynthesis in loblolly pine. Theor Appl Genet 1999;99:705–10.10.1007/s001220051287Search in Google Scholar PubMed

197. Yu Q, Li B, Nelson CD, McKeand SE, Batista VB, Mullin TJ. Association of the cad-n1 allele with increased stem growth and wood density in full-sib families of loblolly pine. Tree Genet Genomes 2006;2:98–108.10.1007/s11295-005-0032-ySearch in Google Scholar

198. IBSS Quarter 3 Report. Southeastern partnership for integrated biomass supply systems, USA, 2014. Available at: http://www.se-ibss.org/publications-and-patents/accomplishment-reports/ibss-quarter-3-2014-report. Last accessed: 9 Mar 2017.Search in Google Scholar

199. IBSS Quarter 2 Report. Southeastern partnership for integrated biomass supply systems, USA, 2015. Available at: http://www.se-ibss.org/publications-and-patents/accomplishment-reports/ibss-quarter-2-2015-report. Last accessed: 9 Mar 2017.Search in Google Scholar

200. Custers R, Bartsch D, Fladung M, Nilsson O, Pilate G, Sweet J, et al. EU regulations impede market introduction of GM forest trees. Trends Plant Sci 2016;21:283–5.10.1016/j.tplants.2016.01.015Search in Google Scholar PubMed

201. Häggman H, Raybould A, Borem A, Fox T, Handley L, Hertzberg M, et al. Genetically engineered trees for plantation forests: key considerations for environmental risk assessment. Plant Biotechnol J 2013;11:785–98.10.1111/pbi.12100Search in Google Scholar PubMed PubMed Central

202. Robledo-Arnuncio JJ, González-Martínez SC, Smouse PE. Theoretical and practical considerations of gene flow. In: El-Kassaby YA, Prado JA, editors. Forests and genetically modified trees. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO), 2010:147–62.Search in Google Scholar

203. FAO. Forests and genetically modified trees. Rome, Italy: Food and Agriculture Organization of the United Nations, 2010. Available at: http://www.fao.org/docrep/013/i1699e/i1699e.pdf. Last accessed: 9 Mar 2017.Search in Google Scholar

204. van Frankenhuyzen K, Beardmore T. Current status and environmental impact of transgenic forest trees. Can J For Res 2004;34:1163–80.10.1139/x04-024Search in Google Scholar

205. Meilan R, Brunner A, Skinner J, Strauss S. Modification of flowering in transgenic trees. In: Komamine A, Morohoshi N, editors. Molecular breeding of woody plants, progress in biotechnology series. Amsterdam, The Netherlands: Elsevier Science BV, 2001:247–56.Search in Google Scholar

206. Gressel J, Al-Ahmad H. Transgenic plants for mitigating introgression of genetically engineered genetic traits. Patent N° 7,612,255 B2, USA, 2009.Search in Google Scholar

207. Brunner AM, Li J, DiFazio SP, Shevchenko O, Montgomery BE, Mohamed R, et al. Genetic containment of forest plantations. In: El-Kassaby YA, Prado JA, editors. Forests and genetically modified trees. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO), 2010:35–75.Search in Google Scholar

208. Kausch AP, Hague J, Oliver M, Li Y, Daniell H, Mascia P, et al. Transgenic perennial biofuel feedstocks and strategies for bioconfinement. Biofuels 2010;1:163–76.10.4155/bfs.09.11Search in Google Scholar

209. Mariani C, De Beuckeleer M, Trueltner J, Leemans J, Goldberg RB. Induction of male sterility in plants by a chimeric ribonuclease gene. Nature 1990;347:737–41.10.1038/347737a0Search in Google Scholar

210. Skinner JS, Meilan R, Ma C, Strauss SH. The Populus PTD promoter imparts floral-predominant expression and enables high levels of floral-organ ablation in Populus, Nicotiana and Arabidopsis. Mol Breed 2003;12:119–32.10.1023/A:1026044927910Search in Google Scholar

211. Moon HS, Li Y, Stewart CN Jr. Keeping the genie in the bottle: transgene biocontainment by excision in pollen. Trends Biotechnol 2010;28:3–8.10.1016/j.tibtech.2009.09.008Search in Google Scholar PubMed

212. Somleva MN, Xu CA, Ryan KP, Thilmony R, Peoples O, Snel KD, et al. Transgene autoexcision in switchgrass pollen mediated by the Bxb1 recombinase. BMC Biotechnol 2014;14:79.10.1186/1472-6750-14-79Search in Google Scholar PubMed PubMed Central

213. Gressel J, Al-Ahmad H. Transgenic mitigation of transgene dispersal by pollen and seed. In: Oliver MJ, Li Y, editors. Plant Gene Containment. Ames, IA: Wiley-Blackwell, 2012:125–46.10.1002/9781118352670.ch9Search in Google Scholar

Received: 2016-9-19
Revised: 2017-3-14
Accepted: 2017-3-26
Published Online: 2017-4-29
Published in Print: 2018-1-26

©2018 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 29.3.2024 from https://www.degruyter.com/document/doi/10.1515/znc-2016-0185/html
Scroll to top button