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Zeitschrift für Naturforschung C

A Journal of Biosciences

Editor-in-Chief: Seibel, Jürgen

Editorial Board: Aigner , Achim / Boland, Wilhelm / Bornscheuer, Uwe / Hoffmann, Klaus

12 Issues per year

IMPACT FACTOR 2017: 0.882
5-year IMPACT FACTOR: 0.912

CiteScore 2017: 0.92

SCImago Journal Rank (SJR) 2017: 0.288
Source Normalized Impact per Paper (SNIP) 2017: 0.448

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Volume 73, Issue 1-2


Biotechnology for bioenergy dedicated trees: meeting future energy demands

Hani Al-Ahmad
Published Online: 2017-04-29 | DOI: https://doi.org/10.1515/znc-2016-0185


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.

Keywords: bioenergy; Eucalyptus; genetic modification; Populus; short-rotation trees


  • 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.

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 7.

    Karp A, Richter GM. Meeting the challenge of food and energy security. J Exp Bot 2011;62:3263–71.CrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.PubMedCrossrefGoogle Scholar

  • 11.

    Balan V. Current challenges in commercially producing biofuels from lignocellulosic biomass. ISRN Biotechnol 2014;2014:463074.PubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.

  • 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.Google Scholar

  • 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.

  • 17.

    Christersson L. Poplar plantations for paper and energy in the south of Sweden. Biomass Bioen 2008;32:997–1000.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 19.

    Grattapaglia D, Resende MD. Genomic selection in forest tree breeding. Tree Genet Genomes 2011;7:241–55.CrossrefGoogle 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.CrossrefGoogle Scholar

  • 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.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.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.CrossrefGoogle Scholar

  • 24.

    Abramson M, Shoseyov O, Shani Z. Plant cell wall reconstruction toward improved lignocellulosic production and processability. Plant Sci 2010;178:61–72.CrossrefGoogle 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.PubMedCrossrefGoogle Scholar

  • 26.

    Dubouzet JG, Strabala TJ, Wagner A. Potential transgenic routes to increase tree biomass. Plant Sci 2013;212:72–101.PubMedCrossrefGoogle Scholar

  • 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.Google Scholar

  • 28.

    Vanholme R, Demedts B, Morreel K, Ralph J, Boerjan W. Lignin biosynthesis and structure. Plant Physiol 2010;153:895–905.PubMedCrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 30.

    Pauly M, Keegstra K. Plant cell wall polymers as precursors for biofuels. Curr Opin Plant Biol 2010;13:305–12.PubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefGoogle 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.

  • 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.CrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 38.

    Mola-Yudego B. Regional potential yields of short rotation willow plantations on agricultural land in Northern Europe. Silva Fenn 2010;44:63–76.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 2017

  • 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.

  • 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.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.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.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.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.CrossrefGoogle 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.PubMedGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefGoogle Scholar

  • 50.

    Dougherty D, Wright J. Silviculture and economic evaluation of eucalypt plantations in the southern US. BioResources 2012;7:1994–2001.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.CrossrefGoogle 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.

  • 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.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.CrossrefGoogle 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.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.

  • 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.PubMedCrossrefGoogle Scholar

  • 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.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.PubMedCrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 61.

    Li L, Lu S, Chiang V. A genomic and molecular view of wood formation. Crit Rev Plant Sci 2006;25:215–33.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 67.

    Petrus L, Noordermeer MA. Biomass to biofuels, a chemical perspective. Green Chem 2006;8:861–7.CrossrefGoogle 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.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.PubMedCrossrefGoogle Scholar

  • 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.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.PubMedCrossrefGoogle Scholar

  • 72.

    Neale DB, Kremer A. Forest tree genomics: growing resources and applications. Nature Rev Genet 2011;12:111–21.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.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.CrossrefGoogle Scholar

  • 78.

    Somerville C, Youngs H, Taylor C, Davis SC, Long SP. Feedstocks for lignocellulosic biofuels. Science 2010;329:790–2.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 84.

    Jansson S, Douglas CJ. Populus: a model system for plant biology. Annu Rev Plant Biol 2007;58:435–58.PubMedCrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 94.

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

  • 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.PubMedCrossrefGoogle Scholar

  • 97.

    Bernard SM, Habash DZ. The importance of cytosolic glutamine synthetase in nitrogen assimilation and recycling. New Phytol 2009;182:608–20.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefGoogle 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.PubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.PubMedCrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle 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.PubMedGoogle Scholar

  • 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.CrossrefGoogle 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.PubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 126.

    Argus GW. Infrageneric classification of Salix (Salicaceae) in the New World. Syst Bot Monogr 1997;52:1–121.CrossrefGoogle 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.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.CrossrefPubMedGoogle Scholar

  • 129.

    Hanley SJ, Karp A. Genetic strategies for dissecting complex traits in biomass willows (Salix spp.). Tree Physiol 2013;34:1167–80.PubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle Scholar

  • 139.

    Vahala T, Stabel P, Eriksson T. Genetic transformation of willows (Salixs spp.) by Agrobacterium tumefaciens. Plant Cell Rep 1989;8:55–8.CrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.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.PubMedCrossrefGoogle Scholar

  • 144.

    Henry RJ, Kole C. Genetics, genomics and breeding of eucalypts. Boca Raton: CRC Press, 2015:206.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.

  • 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.PubMedCrossrefGoogle Scholar

  • 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.Google Scholar

  • 148.

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

  • 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.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.Google Scholar

  • 153.

    Girijashankar V. Genetic transformation of Eucalyptus. Physiol Mol Biol Plants 2011;17:9–23.PubMedCrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 156.

    Grattapaglia D, Kirst M. Eucalyptus applied genomics: from gene sequences to breeding tools. New Phytol 2008;179:911–29.CrossrefPubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.PubMedGoogle Scholar

  • 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.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.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.CrossrefGoogle Scholar

  • 162.

    Ledford H. Brazil considers transgenic trees. Nature 2014;512:357.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.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.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.CrossrefGoogle 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.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.PubMedCrossrefGoogle Scholar

  • 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.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.CrossrefGoogle Scholar

  • 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.CrossrefGoogle 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.CrossrefGoogle 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.Google Scholar

  • 175.

    Gernandt DS, Lopez GG, Garcia SO, Liston A. Phylogeny and classification of Pinus. Taxon 2005;54:29–42.CrossrefGoogle 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.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.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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefGoogle 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.

  • 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.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.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.CrossrefPubMedGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.PubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 188.

    Alvarez JM, Ordás RJ. Stable Agrobacterium-mediated transformation of maritime pine based on kanamycin selection. ScientificWorldJ 2013;2013:681792.Google Scholar

  • 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.CrossrefGoogle Scholar

  • 190.

    Grace LJ, Charity JA, Gresham B, Kay N, Walter C. Insect resistance transgenic Pinus radiata. Plant Cell Rep 2005;24:103–11.PubMedCrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.PubMedCrossrefGoogle Scholar

  • 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.PubMedGoogle Scholar

  • 194.

    Bonawitz ND, Chapple C. The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 2010;44:337–63.CrossrefPubMedGoogle Scholar

  • 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.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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefGoogle 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.

  • 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.

  • 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.PubMedCrossrefGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.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.

  • 204.

    van Frankenhuyzen K, Beardmore T. Current status and environmental impact of transgenic forest trees. Can J For Res 2004;34:1163–80.CrossrefGoogle 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.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.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.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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefGoogle 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.CrossrefPubMedGoogle Scholar

  • 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.CrossrefPubMedGoogle Scholar

  • 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.Google Scholar

About the article

Received: 2016-09-19

Revised: 2017-03-14

Accepted: 2017-03-26

Published Online: 2017-04-29

Published in Print: 2018-01-26

Citation Information: Zeitschrift für Naturforschung C, Volume 73, Issue 1-2, Pages 15–32, ISSN (Online) 1865-7125, ISSN (Print) 0939-5075, DOI: https://doi.org/10.1515/znc-2016-0185.

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