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Genetic engineering of trees: progress and new horizons

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Abstract

Genetic engineering of trees to improve productivity, wood quality, and resistance to biotic and abiotic stresses has been the primary goal of the forest biotechnology community for decades. We review the extensive progress in these areas and their current status with respect to commercial applications. Examples include novel methods for lignin modification, solutions for long-standing problems related to pathogen resistance, modifications to flowering onset and fertility, and drought and freeze tolerance. There have been numerous successful greenhouse and field demonstrations of genetically engineered trees, but commercial application has been severely limited by social and technical considerations. Key social factors are costly and uncertain regulatory hurdles and sweeping market barriers in the form of forest certification systems that disallow genetically modified trees. These factors limit and, in many cases, preclude field research and commercial adoption. Another challenge is the high cost and uncertainty in transformation efficiency that is needed to apply genetic engineering and gene editing methods to most species and genotypes of commercial importance. Recent advances in developmental gene-based transformation systems and gene editing, if combined with regulatory and certification system reform, could provide the foundation for genetic engineering to become a significant tool for coping with the increasing environmental and biological stresses on planted and wild forests.

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References

  • Ali Z, Abul-faraj A, Li L, Ghosh N, Piatek M, Mahjoub A, Aouida M, Piatek A, Baltes NJ, Voytas DF, Dinesh-Kumar S, Mahfouz MM (2015) Efficient virus-mediated genome editing in plants using the CRISPR/Cas9 system. Mol Plant 8:1288–1291

    Article  PubMed  CAS  Google Scholar 

  • Álvarez R, Alonso P, Cortizo M, Celestino C, Hernández I, Toribio M, Ordás RJ (2014) Genetic transformation of selected mature cork oak (Quercus suber L.) trees. Plant Cell Rep 23:218–223

    Article  CAS  Google Scholar 

  • Álvarez R, Álvarez JM, Humara JM, Revilla A, Ordás RJ (2009) Genetic transformation of cork oak (Quercus suber L.) for herbicide resistance. Biotechnol Lett 31:1477–1483

    Article  PubMed  CAS  Google Scholar 

  • Álvarez R, Ordás RJ (2007) Improved genetic transformation protocol for cork oak (Quercus suber L.). Plant Cell Tissue Organ Cult 91:45–52

    Article  CAS  Google Scholar 

  • Álvarez R, Toribio M, Cortizo M, Fernández R-JO (2006) Cork oak trees (Quercus suber L.). In: Wang K (ed) Methods in molecular biology, vol 344, Agrobacterium protocols, vol 2, 2nd edn. Humana Press Inc., Totowa, pp 113–123

    Chapter  Google Scholar 

  • Amerson HV, Nelson CD, Kubisiak TL, Kuhlman EG, Garcia SA (2015) Identification of nine pathotype-specific genes conferring resistance to fusiform rust in loblolly pine (Pinus taeda L.). Forests 6:2739–2761

    Article  Google Scholar 

  • Anacker BL, Rank NE, Hüberli D, Garbelotto M, Gordon S, Harnik T, Whitkus R, Meentemeyer R (2008) Susceptibility to Phytophthora ramorum in a key infectious host: landscape variation in host genotype, host phenotype, and environmental factors. New Phytol 177:756–766

    Article  PubMed  Google Scholar 

  • Anagnostakis SL (1987) Chestnut blight: the classical problem of an introduced pathogen. Mycologia 79:23–37

    Article  Google Scholar 

  • Anagnostakis SL (2012) Chestnut breeding in the United States for disease and insect resistance. Plant Dis 96:1392–1403

    Article  Google Scholar 

  • Andrade GM, Nairn CJ, Le HT, Merkle SA (2009) Sexually mature transgenic American chestnut trees via embryogenic suspension-based transformation. Plant Cell Rep 28:1385–1397

    Article  PubMed  CAS  Google Scholar 

  • Anonymous (2015) Brazil approves transgenic eucalyptus. Nat Biotechnol 33:577

    Google Scholar 

  • Araji S, Grammer TA, Gertzen R, Anderson SD, Mikulic-Petkovsek M, Veberic R, Phu ML, Solar A, Leslie CA, Dandekar AM, Escobar MA (2014) Novel roles for the polyphenol oxidase enzyme in secondary metabolism and the regulation of cell death in walnut. Plant Physiol 164:1191–1203

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Argout X, Salse J, Aury J-M, Guiltinan MJ, Droc G, Gouzy J, Allegre M, Chaparro C, Legavre T, Maximova SN, Abrouk M, Murat F, Fouet O, Poulain J, Ruiz M, Roguet Y, Rodier-Goud M, Barbosa-Neto JF, Sabot F, Kudrna D, Ammiraju JSS, Schuster SC, Carlson JE, Sallet E, Schiex T, Dievart A, Kramer M, Gelley L, Shi Z, Bérard A, Viot C, Boccara M, Risterucci AM, Guignon V, Sabau X, Axtell MJ, Ma Z, Zhang Y, Brown S, Bourge M, Golser W, Song X, Clement D, Rivallan R, Tahi M, Akaza JM, Pitollat B, Gramacho K, D'Hont A, Brunel D, Infante D, Kebe I, Costet P, Wing R, McCombie WR, Guiderdoni E, Quetier F, Panaud O, Wincker P, Bocs S, Lanaud C (2011) The genome of Theobroma cacao. Nat Genet 14:101–108

    Article  CAS  Google Scholar 

  • Ariani A, Francini A, Andreucci A, Sebastiani L (2016) Over-expression of AQUA1 in Populus alba Villafranca clone increases relative growth rate and water use efficiency, under Zn excess condition. Plant Cell Rep 35:289–301

    Article  PubMed  CAS  Google Scholar 

  • Arrillaga I, Segura J, Merkle SA (2008) Black locust. In: Kole C, Hall TC (eds) Compendium of transgenic crop plants, Transgenic forest tree species, vol 9. Wiley-Blackwell, Chichester, pp 293–307

    Chapter  Google Scholar 

  • Attílio LB, Martins PK, Gómez-Krapp LM, Machado MA, Freitas-Astúa J (2014) Genetic transformation of sweet oranges to over-express SABP2 gene. BMC Proc 8:P109

    Article  PubMed Central  Google Scholar 

  • Baird RE (1991) Growth and stromata production of hypovirulent and virulent strains of Cryphonectria parasitica on dead Quercus rubra and Acer rubrum. Mycologia 83:158–162

    Article  Google Scholar 

  • Baldoni E, Genga A, Cominelli E (2015) Plant MYB transcription factors: their role in drought response mechanisms. Int J Mol Sci 16:15811–15851

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Balestrazzi A, Bonadei M, Carbonera D (2007) Nuclease-producing bacteria in soil cultivated with herbicide resistant transgenic white poplars. Ann Microbiol 57:531–536

    Article  CAS  Google Scholar 

  • Balestrazzi A, Bonadei M, Zelasco S, Giorcelli A, Gennaro M, Calligari P, Mattivi F, Quattrini E, Carbonera D (2011) Seasonal and tissue-specific transgene expression and resveratrol-3-glucoside (piceid) accumulation in genetically modified white poplars carrying the grapevine StSy gene. Plant Cell Tissue Organ Cult 105:1–8

    Article  CAS  Google Scholar 

  • Balestrazzi A, Botti S, Zelasco S, Biondi S, Franchin C, Calligari P, Racchi M, Turchi A, Lingua G, Berta G, Carbonera D (2009) Expression of the PsMT A1 gene in white poplar engineered with the MAT system is associated with heavy metal tolerance and protection against 8-hydroxy-2′-deoxyguanosine mediated-DNA damage. Plant Cell Rep 28:1179–1192

    Article  PubMed  CAS  Google Scholar 

  • Betti M, Bauwe H, Busch FA, Fernie AR, Keech O, Levey M, Ort DR, Parry MAJ, Sage R, Timm S, Walker B, Webber APM (2016) Manipulation photorespiration to increase plant productivity: recent advances and perspectives for crop improvement. J Exp Bot 67:2977–2988

    Article  PubMed  CAS  Google Scholar 

  • Birol I, Raymond A, Jackman SD, Pleasance S, Coope R, Taylor GA, Yuen MMS, Keeling CI, Brand D, Vandervalk BP, Kirk H, Pandoh P, Moore RA, Zhao Y, Mungall AJ, Jaquish B, Yanchuk A, Ritland C, Boyle B, Bousquet J, Ritland K, Mackay J, Bohlmann J, Jones SJM (2013) Assembling the 20 Gb white spruce (Picea glauca) genome from whole-genome shotgun sequencing data. Bioinformatics 29:1492–1497

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Biswal AK, Hao Z, Pattathil S, Yang X, Winkeler K, Collins C, Mohanty SS, Richardson EA, Gelineo-Albersheim I, Hunt K, Ryno D, Sykes RW, Turner GB, Ziebell A, Gjersing E, Lukowitz W, Davis MF, Decker SR, Hahn MG, Mohnen D (2015) 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 8:41

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Biswal AK, Soeno K, Gandla ML, Immerzeel P, Pattathil S, Lucenius J, Serimaa R, Hahn MG, Moritz T, Jönsson LJ, Israelsson-Nordström M, Mellerowicz EJ (2014) Aspen pectate lyase PtxtPL1-27 mobilizes matrix polysaccharides from woody tissues and improves saccharification yield. Biotechnol Biofuels 7:11

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bjurhager I, Olsso A-M, Zhang B, Gerber L, Kumar M, Berglund LA, Burgert I, Sundberg B, Salmén L (2010) Ultrastructure and mechanical properties of Populus wood with reduced lignin content caused by transgenic down-regulation of cinnamate 4-hydroxylase. Biomacromolecules 11:2359–2365

    Article  PubMed  CAS  Google Scholar 

  • Boeckler GA, Towns M, Unsicker SB, Mellway RD, Yip L, Hilke I, Gershenzon J, Constabel CP (2014) Transgenic upregulation of the condensed tannin pathway in poplar leads to a dramatic shift in leaf palatability for two tree-feeding Lepidoptera. J Chem Ecol 40:150–158

    Article  PubMed  CAS  Google Scholar 

  • Bogdanove AJ, Voytas DF (2011) TAL effectors: customizable proteins for DNA testing. Science 333:1843–1846

    Article  PubMed  CAS  Google Scholar 

  • Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043

    Article  PubMed  CAS  Google Scholar 

  • Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JEK, Blais S, Trembley L, Morency M-J, Pavy N, Grima-Pettenati J, Séquin A, MacKay J (2008) Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot 59:3925–3939

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bonawitz ND, Chapple C (2013) Can genetic engineering of lignin deposition be accomplished without an unacceptable yield penalty? Curr Opin Biotechnol 24:336–343

    Article  PubMed  CAS  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu C-M, van Lammeren AAM, Miki BLA, Custers JBM, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Brunner AM, Li J, DiFazio SP, Shevchenko O, Montgomery BE, Mohamed R, Wei H, Ma C, Elias AA, VanWormer K, Strauss SH (2007) Genetic containment of forest plantations. Tree Genet Genomes 3:75–100

    Article  Google Scholar 

  • Burnworth E (2002) A brief history of the efforts of Stronghold, Inc to restore the American chestnut: 1969 to present. Stronghold, Inc., Dickerson, Maryland

  • Butt HI, Yang Z, Gong Q, Chen E, Wang X, Zhao G, Ge X, Zhang X, Li F (2017) GaMYB85, an R2R3 MYB gene, in transgenic Arabidopsis plays an important role in drought tolerance. BMC Plant Biol 17:142

    Article  PubMed  PubMed Central  Google Scholar 

  • Campbell MM, Brunner AM, Jones HM, Strauss SH (2003) Forestry’s fertile crescent: the application of biotechnology to forest trees. Plant Biotechnol J 1:141–154

    Article  PubMed  CAS  Google Scholar 

  • Carraway DT, Wilde HD, Merkle SA (1994) Somatic embryogenesis and gene transfer in American chestnut. J Am Chest Found 8:29–33

    Google Scholar 

  • Castellanos-Hernández OA, Rodríguez-Sahagún A, Acevedo-Hernández GJ, Herrera-Estrella LR (2011) Genetic transformation of forest trees. In: Alvarez M (ed) Genetic transformation. InTechOpen, London, pp 191–214

  • Celedon JM, Yuen MMS, Chiang A, Henderson H, Reid KE, Bohlmann J (2017) Cell-type- and tissue-specific transcriptomes of the white spruce (Picea glauca) bark unmask fine-scale spatial patterns of constitutive and induced conifer defense. Plant J 92:710–726

    Article  PubMed  CAS  Google Scholar 

  • Chandler JW (2012) Floral meristem initiation and emergence in plants. Cell Mol Life Sci 69:3807–3818

    Article  PubMed  CAS  Google Scholar 

  • Chauhan RD, Veale A, Ma C, Strauss SH, Myburg AA (2014) Genetic transformation of Eucalyptus—challenges and future prospects. In: Ramawat KG, Mérillon J-M, Ahuja MR (eds) Tree biotechnology. CRC Press, Boca Raton, pp 392–445

    Google Scholar 

  • Che D, Meagher RB, Rugh CL, Kim T, Heaton ACP, Merkle SA (2006) Expression of organomercurial lyase in eastern cottonwood enhances organomercury resistance. In Vitro Cell Dev Biol Plant 42:228–234

    Article  CAS  Google Scholar 

  • Chinnusamy V, Ohta M, Kanrar S, Lee B-h, Hong X, Agarwal M, Zhu J-K (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann KA (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J 26:573–582

    Article  PubMed  CAS  Google Scholar 

  • Coleman HD, Canam T, Kang K-Y, Ellis DD, Mansfield SD (2007) Over-expression of UDP-glucose pyrophosphorylase in hybrid poplar affects carbon allocation. J Exp Bot 58:4257–4268

    Article  PubMed  CAS  Google Scholar 

  • Coleman HD, Cánovas FM, Man H, Kirby EG, Mansfield SD (2012) 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 10:883–889

    Article  PubMed  CAS  Google Scholar 

  • Coleman HD, Park J-Y, Nair R, Chapple C, Mansfield SD (2008a) RNAi-mediated suppression of p-coumaroyl-CoA 3′-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism. Proc Natl Acad Sci U S A 105:4501–4506

    Article  PubMed  PubMed Central  Google Scholar 

  • Coleman HD, Samuels AL, Guy RD, Mansfield SD (2008b) Perturbed lignification impacts tree growth in hybrid poplar—a function of sink strength, vascular integrity, and photosynthetic assimilation. Plant Physiol 148:1229–1237

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Coleman HD, Yan J, Mansfield SD (2009) Sucrose synthase affects carbon partitioning to increase cellulose production and altered cell wall ultrastructure. Proc Natl Acad Sci U S A 106:13118–13123

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Confalonieri M, Balestrazzi A, Bisoffi S, Carbonera D (2003) In vitro culture and genetic engineering of Populus spp.: synergy for forest tree improvement. Plant Cell Tissue Organ Cult 72:109–138

    Article  CAS  Google Scholar 

  • Cooke BJ, Carroll AL (2017) Predicting the risk of mountain pine beetle spread to eastern pine forests: considering uncertainty in uncertain times. For Ecol Manag 396:11–25

  • Corbesier L, Vincent C, Jang S, Fornara F, Fan Q, Searle I, Giakountis A, Farrona S, Gissot L, Turnbull C, Coupland G (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033

    Article  PubMed  CAS  Google Scholar 

  • Corredoira E, San-José MC, Ballester A, Vietiez AM (2005) Genetic transformation of Castanea sativa Mill. by Agrobacterium tumefaciens. Acta Hortic 693:387–393

    Article  Google Scholar 

  • Corredoira E, San José MC, Vieitez AM, Allona I, Aragoncillo C, Ballester A (2016) Agrobacterium-mediated transformation of European chestnut somatic embryos with a Castanea sativa (Mill.) endochitinase gene. New For 47:669–684

    Article  Google Scholar 

  • Corredoira E, San-José MC, Vietiez AM, Ballester A (2007) Improving genetic transformation of European chestnut and cryopreservation of transgenic lines. Plant Cell Tissue Organ Cult 91:281–288

    Article  CAS  Google Scholar 

  • Corredoira E, Valladares S, Allona I, Aragoncillo C, Vieitez AM, Ballester A (2012) Genetic transformation of European chestnut somatic embryos with a native thaumatin-like protein (CsTL1) gene isolated from Castanea sativa seeds. Tree Physiol 32:1389–1402

    Article  PubMed  CAS  Google Scholar 

  • Corredoira E, Valladares S, Vieitez AM, Ballester A (2015) Chestnut, European (Castanea sativa). In: Wang K (ed) Agrobacterium protocols, vol 2, Methods in molecular biology, vol 1224. Springer Sci Bus Media, New York, pp 163–176

    Google Scholar 

  • Cowling E, Young C (2013) Narrative history of the resistance screening center: it’s origins, leadership and partial list of public benefits and scientific contributions. Forests 4:666–692

    Article  Google Scholar 

  • da Silva ALL, de Oliveira Y, da Luz Costa J, de Souza Mudry C, Procopiuk M, Scheidt GN, Brondani GE (2011) Preliminary results for genetic transformation of shoot tip of Eucalyptus saligna Sm. via Agrobacterium tumefaciens. J Biotechnol Biodiv 2:1–6

    Google Scholar 

  • da Silva ALL, de Oliveira Y, Procopiuk M, de Souza Mudry C, Brondani GE, da Luz Costa J, Scheidt GN (2013) Transient expression of uidA gene in leaf explants of Eucalyptus saligna Sm. transformed via Agrobacterium tumefaciens. Biosci J (Uberlândia) 29:1–7

    Google Scholar 

  • Dai X, Xu Y, Ma Q, Xu W, Wang T, Xue Y, Chong K (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol 143:1739–1751

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dandekar AM, Fisk HJ, McGranahan GH, Uratsu SL, Bains H, Leslie CA, Escobar TM, Labavitch J, Grieve C, Gradziel T, Vail PV, Tebbets SJ, Sassa H, Tao R, Viss W, Driver J, James D, Passey A, Teo G (2002) Different genes for different folks in tree crops: what works and what does not. HortScience 37:281–286

    CAS  Google Scholar 

  • Dandekar AM, McGranahan GH, Vail PV, Uratsu SL, Leslie CA, Tebbets JS (1998) High levels of expression of full-length cryIA(c) gene from Bacillus thuringiensis in transgenic somatic walnut embryos. Plant Sci 131:181–193

    Article  CAS  Google Scholar 

  • Davis DD, Torsello ML, McClenahen JR (1997) Influence of Cryphonectria parasitica basal cankers on radial growth of scarlet oak in Pennsylvania. Plant Dis 81:369–373

    Article  Google Scholar 

  • de la Torre F, Rodríquez R, Jorge G, Villar B, Álvarez-Otero R, Grima-Pettenati J, Gallego PP (2014) Genetic transformation of Eucalyptus globulus using the vascular-specific EgCCR as an alternative to the constitutive CaMV35S promoter. Plant Cell Tissue Organ Cult 117:77–84

    Article  CAS  Google Scholar 

  • Del Rio JC, Marques G, Rencoret J, Martínez AT, Gutiérrez A (2007) Occurrence of naturally acetylated lignin units. J Agric Food Chem 55:5461–5468

    Article  PubMed  CAS  Google Scholar 

  • Deng W, Luo K, Li Z, Yang Y (2009) A novel method for induction of plant regeneration via somatic embryogenesis. Plant Sci 177:43–48

    Article  CAS  Google Scholar 

  • Derba-Maceluch M, Awano T, Takahashi J, Lucenius J, Ratke C, Kontro I, Kallas Å, Busse-Wicher M, Kosik O, Tanaka R, Winzéll A, Kallas A, Leśniewska J, Berthold F, Immerzeel P, Teeri TT, Ezcurra I, Dupree P, Serimaa R, Mellerowicz EJ (2015) Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood. New Phytol 205:666–681

    Article  PubMed  CAS  Google Scholar 

  • Dietz A (1978) The use of ionizing radiation to develop a blight resistant American chestnut, Castanea dentata, through induced mutations. In: MacDonald WL, Cech FC, Luchok J, Smith C (eds) Proc American chestnut symposium, West Virginia University Press, Morgantown, pp 17–20

  • Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32:278–289

    Article  PubMed  CAS  Google Scholar 

  • Doherty CJ, Van Buskirk HA, Myers SJ, Thomashow MF (2009) Roles for Arabidopsis CAMTA transcription factors in cold-regulated gene expression and freezing tolerance. Plant Cell 21:972–984

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Du J, Mansfield SD, Groover AT (2009) The Populus homeobox gene ARBORKNOX2 regulates cell differentiation during secondary growth. Plant J 60:1000–1014

    Article  PubMed  CAS  Google Scholar 

  • Du N, Liu X, Li Y, Chen S, Zhang J, Ha D, Deng W, Sun C, Zhang Y, Pijut PM (2012) Genetic transformation of Populus tomentosa to improve salt tolerance. Plant Cell Tissue Organ Cult 108:181–189

    Article  CAS  Google Scholar 

  • Du N, Pijut PM (2009) Agrobacterium-mediated transformation of Fraxinus pennsylvanica hypocotyls and plant regeneration. Plant Cell Rep 28:915–923

    Article  PubMed  CAS  Google Scholar 

  • Dubouzet JG, Strabala TJ, Wagner A (2013) Potential transgenic routes to increase tree biomass. Plant Sci 212:72–101

    Article  PubMed  CAS  Google Scholar 

  • Dutt M, Barthe G, Irey M, Grosser J (2015) Transgenic citrus expressing an Arabidopsis NPR1 gene exhibit enhanced resistance against Huanglongbing (HLB; citrus greening). PLoS One 10:e0137134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dutt M, Omar A, Orbovic V, Barthe G, Gmittier J, Vasconcellos M, Dunning C, Grosser JW (2008) Combating Huanglongbing and canker via genetic engineering of citrus. Proc Fla State Hort Soc 121:124–129

    Google Scholar 

  • Elias AA, Busov VB, Kosola KR, Ma C, Etherington E, Shevchenko O, Gandhi H, Pearce DW, Rood SB, Strauss SH (2012) Green revolution trees: semidwarfism transgenes modify gibberellins, promote root growth, enhance morphological diversity, and reduce competitiveness in hybrid poplar. Plant Physiol 160:1130–1144

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Elorriaga E, Klocko AL, Ma C, Strauss S (2016) Asexual gene drive in Populus? Results from CRISPR/Cas9 mutagenesis of floral genes for genetic containment. Plant and Animal Genomes Conference, San Diego https://pag.confex.com/pag/xxiv/webprogram/Paper19742.html

    Google Scholar 

  • Elorriaga E, Klocko AL, Ma C, Strauss SH (2018) Variation in mutation spectra among CRISPR/Cas9 mutagenized poplars. Front Plant Sci 9(2018):594

    Article  PubMed  PubMed Central  Google Scholar 

  • Elorriaga E, Meilan R, Ma C, Skinner JS, Etherington E, Brunner A, Strauss SH (2014) A tapetal ablation transgene induces stable male sterility and slows field growth in Populus. Tree Genet Genomes 10:1583–1593

    Article  Google Scholar 

  • Eriksson ME, Israelsson M, Olsson O, Moritz T (2000) Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat Biotechnol 18:784–788

    Article  PubMed  CAS  Google Scholar 

  • Etchells JP, Mishra LS, Kumar M, Campbell L, Turner SR (2015) Wood formation in trees is increased by manipulating PXY-regulated cell division. Curr Biol 25:1050–1055

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Etchells JP, Turner SR (2010) The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137:767–774

    Article  PubMed  CAS  Google Scholar 

  • Eudes A, George A, Mukerjee P, Kim JS, Pollet B, Benke PI, Yang F, Mitra P, Sun L, Çetinkol O, Chabout S, Mouille G, Soubigou-Taconnat L, Balzergue S, Singh S, Holmes BM, Mukhopadhyay A, Keasling JD, Simmons BA, Lapierre C, Ralph J, Loque D (2012) Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification. Plant Biotechnol 10:609–620

    Article  CAS  Google Scholar 

  • Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, Luo K (2015) Efficient CRISPR/Cas9-mediated targeted mutagenesis in Populus in the first generation. Sci Rep 5:12217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fang H, Wang G (2000) Somatic embryogenesis of Juglans nigra L. and establishment of gene transformation system of walnut. Acta Hort Sin 27:406–411

    Google Scholar 

  • FAO (2010) Forests and genetically modified trees. Food and Agriculture Organization of the United Nations, Rome

  • Fauser F, Roth N, Pacher M, Ilg G, Sánchez-Fernández R, Biesgen C, Puchta H (2012) In planta gene targeting. Proc Natl Acad Sci U S A 109:7535–7540

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernando DD, Richards JL, Kikkert JR (2006) In vitro germination and transient GFP expression of American chestnut (Castanea dentata) pollen. Plant Cell Rep 25:450–456

    Article  PubMed  CAS  Google Scholar 

  • Fernando SC, Goodger JQD, Gutierrez SS, Johnson AAT, Woodrow IE (2016) Plant regeneration through indirect organogenesis and genetic transformation of Eucalyptus polybractea R.T. Baker. Ind Crop Prod 86:73–78

    Article  CAS  Google Scholar 

  • Ferreira SA, Pitz KY, Manshardt R, Zee F, Fitch M (2002) Virus coat protein transgenic papaya provides practical control of papaya ringspot virus in Hawaii. Plant Dis 86:101–105

    Article  Google Scholar 

  • Fillatti JJ, Sellmer J, McCown B, Haissig B, Comai L (1987) Agrobacterium mediated transformation and regeneration of Populus. Mol Gen Genet 206:192–199

    Article  CAS  Google Scholar 

  • Flachowsky H, Hanke M-V, Peil A, Strauss SH, Fladung M (2009) A review on transgenic approaches to accelerate breeding of woody plants. Plant Breed 128:217–226

    Article  CAS  Google Scholar 

  • Flachowsky H, Peil A, Sopanen T, Elo A, Hanke V (2007) Overexpression of BpMADS4 from silver birch (Betula pendula Roth.) induces early-flowering in apple (Malus × domestica Borkh.). Plant Breed 126:137–145

    Article  CAS  Google Scholar 

  • Flachowsky H, Szankowski I, Waidmann S, Peil A, Tränkner C, Hanke M-V (2012) The MdTFL1 gene of apple (Malus × domestica Borkh.) reduces vegetative growth and generation time. Tree Physiol 32:1288–1301

    Article  PubMed  CAS  Google Scholar 

  • Fladung M, Becker D (2010) Targeted integration and removal of transgenes in hybrid aspen (Populus tremula L. × P. tremuloides Michx.) using site-specific recombination systems. Plant Biol 12:334–340

    Article  PubMed  CAS  Google Scholar 

  • Florez SL, Erwin RL, Maximova SN, Guiltinan MJ, Curtis WR (2015) Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biol 15:121

    Article  PubMed  PubMed Central  Google Scholar 

  • Franke R, McMichael CM, Meyer K, Shirley AM, Cusumano JC, Chapple C (2000) Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J 22:223–234

    Article  PubMed  CAS  Google Scholar 

  • Freiman A, Shlizerman L, Golobovitch S, Yablovitz Z, Korchinsky R, Cohen Y, Samach A, Chevreau E, Le Roux P-M, Patocchi A, Flaishman MA (2012) Development of a transgenic early flowering pear (Pyrus communis L.) genotype by RNAi silencing of PcTFL1-1 and PcTFL1-2. Planta 235:1239–1251

    Article  PubMed  CAS  Google Scholar 

  • Frigimelica G, Faccoli M (1999) Preliminary report on the occurrence of Cryphonectria parasitica (Murrill) Barr on different tree species in Friuli Venezia-Giulia (Italy). Acta Hortic 494:467–472

    Article  Google Scholar 

  • Fry SC (2004) Primary cell wall metabolism: tracking the careers of wall polymers in living plant cells. New Phytol 161:641–675

    Article  CAS  Google Scholar 

  • Gallardo F, Fu J, Cantón FR, Garcia-Gutiérrez A, Cánovas FM, Kirby EG (1999) Expression of a conifer glutamine synthetase gene in transgenic poplar. Planta 210:19–26

    Article  PubMed  CAS  Google Scholar 

  • Gerber L, Zhang B, Roach M, Rende U, Gorzsás A, Kumar M, Burgert I, Niittylä T, Sundberg B (2014) Deficient sucrose synthase activity in developing wood does not specifically affect cellulose biosynthesis, but causes an overall decrease in cell wall polymers. New Phytol 203:1220–1230

    Article  PubMed  CAS  Google Scholar 

  • Gonsalves D (1998) Control of papaya ringspot virus in papaya: a case study. Annu Rev Phytopathol 36:415–437

    Article  PubMed  CAS  Google Scholar 

  • Gordon-Kamm WJ, Spencer TM, Mangano ML, Adams TR, Daines RJ, Start WG, O'Brien JV, Chambers SA, Adams WR Jr, Willetts NG, Rice TB, Mackey CJ, Krueger RW, Kausch AP, Lemaux PG (1990) Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell 2:603–618

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gou J, Ma C, Kadmiel M, Gai Y, Strauss S, Jiang X, Busov V (2011) Tissue-specific expression of Populus C19 GA 2-oxidases differentially regulate above- and below-ground biomass growth through control of bioactive GA concentrations. New Phytol 192:626–639

    Article  PubMed  CAS  Google Scholar 

  • Grace LJ, Charity JA, Gresham B, Kay N, Walter C (2005) Insect-resistant transgenic Pinus radiata. Plant Cell Rep 24:103–111

    Article  PubMed  CAS  Google Scholar 

  • Guo C-H, Zhao S-T, Ma Y, Hu J-J, Han X-J, Chen J, Lu M-Z (2012) Bacillus thuringiensis Cry3Aa fused to a cellulase-binding peptide shows increased toxicity against the longhorned beetle. Appl Microbiol Biotechnol 93:1249–1256

    Article  PubMed  CAS  Google Scholar 

  • Guo L, Xu W, Zhang Y, Zhang J, Wei Z (2017) Inducing triploids and tetraploids with high temperatures in Populus sect. Tacamahaca. Plant Cell Rep 36:313–326

    Article  PubMed  CAS  Google Scholar 

  • Haberman A, Bakhshian O, Cerezo-Medina S, Paltiel J, Adler C, Ben-Ari G, Mercado JA, Pliego-Alfaro F, Lavee S, Samach A (2017) A possible role for flowering locus T-encoding genes in interpreting environmental and internal cues affecting olive (Olea europaea L.) flower induction. Plant Cell Environ 40:1263–1280

    Article  PubMed  CAS  Google Scholar 

  • Häggman H, Sutela S, Fladung M (2016) Genetic engineering contribution to forest tree breeding efforts. In: Vettori C, Gallardo F, Häggman H, Kazana V, Migliacci F, Pilate G, Fladung M (eds) Biosafety of forest transgenic trees. Springer, Dordrecht, pp 11–29

    Chapter  Google Scholar 

  • Hajeri S, Killiny N, El-Mohtar C, Dawson WO, Gowda S (2014) Citrus tristeza virus-based RNAi in citrus plants induces gene silencing in Daiphorina citri, a phloem-sap sucking insect vector of citrus greening disease (Huanglongbing). J Biotechnol 176:42–49

    Article  PubMed  CAS  Google Scholar 

  • Hammerbacher A, Paetz C, Wright LP, Fischer TC, Bohlmann J, Davis AJ, Fenning TM, Gershenzon J, Schmidt A (2014) Flavan-3-ols in Norway spruce: biosynthesis, accumulation, and function in response to attack by the bark beetle-associated fungus Ceratocystis polonica. Plant Physiol 164:2107–2122

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Han KM, Dharmawardhana P, Arias RS, Ma C, Busov V, Strauss SH (2011) Gibberellin-associated cisgenes modify growth, stature and wood properties in Populus. Plant Biotechnol J 9:162–178

    Article  PubMed  CAS  Google Scholar 

  • Harcourt RL, Kyozuka J, Floyd RB, Bateman KS, Tanaka H, Decroocq V, Llewellyn DJ, Zhu X, Peacock WJ, Dennis ES (2000) Insect- and herbicide-resistant transgenic eucalypts*. Mol Breed 6:307–315

    Article  CAS  Google Scholar 

  • Havir EA, Anagnostakis SL (1983) Oxalate production by virulent but not by hypovirulent strains of Endothia parasitica. Physiol Plant Pathol 23:369–376

    Article  CAS  Google Scholar 

  • Helliwell EE, Vega-Arreguín J, Shi Z, Bailey B, Xiao S, Maximova SN, Tyler BM, Guiltinan MJ (2016) Enhanced resistance in Theobroma cacao against oomycete and fungal pathogens by secretion of phosphatidylinositol-3-phosphate-binding proteins. Plant Biotechnol J 14:875–886

    Article  PubMed  CAS  Google Scholar 

  • Hertzberg M, Bhalerao R, Jonsén D, Möller L, Jonsson P (2015a) Woody plants having improved growth characteristics and methods for making the same using transcription factors. US Patent 8937219 B2

  • Hertzberg M, Sandberg G, Schrader J, Jonsén CD (2015b) Woody plants having improved growth characteristics and methods for making the same. US Patent 9018448 B2

  • Himmel ME, Ding S-Y, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315:804–807

    Article  PubMed  CAS  Google Scholar 

  • Hinchee M, Rottmann W, Mullinax L, Zhang C, Chang S, Cunnigham M, Pearson L, Nehra N (2009) Short-rotation woody crops for bioenergy and biofuels applications. In Vitro Cell Dev Biol Plant 45:619–629

    Article  PubMed  PubMed Central  Google Scholar 

  • Hinchee M, Zhang C, Chang S, Cunningham M, Hammond W, Nehra N (2011) Biotech Eucalyptus can sustainably address society’s need for wood: the example of freeze tolerant Eucalyptus in the southeastern U.S. BMC Proc 5:124

    Article  Google Scholar 

  • Hinchee MAW, Connor-Ward DV, Newell CA, McDonell RE, Sato SJ, Gasser CS, Fischhoff DA, Re DB, Fraley RT, Horsch RB (1988) Production of transgenic soybean plants using Agrobacterium-mediated DNA transfer. BioTechnol 6:915–922

    CAS  Google Scholar 

  • Hoenicka H, Lehnhardt D, Briones V, Nilsson O, Fladung M (2016) Low temperatures are required to induce the development of fertile flowers in transgenic male and female early flowering poplar (Populus tremula L.). Tree Physiol 36:667–677

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hu J, Wang L, Yan D, Lu M-Z (2014) Research and application of transgenic poplar in China. In: Fenning T (ed) Challenges and opportunities for the world’s forests in the 21st century. Springer, Netherlands, pp 567–584

    Chapter  Google Scholar 

  • Hu JJ, Liu QY, Wang KS, Zhang BE, Tian YC, Han YF (1999) Field test on insect resistance of transgenic plants (Populus nigra) transformed with Bt toxin gene. For Res 12:202–205

    Google Scholar 

  • Hu JJ, Tian YC, Han YF, Li L, Zhang BE (2001) Field evaluation of insect-resistant transgenic Populus nigra trees. Euphytica 121:123–127

    Article  Google Scholar 

  • Humphreys JM, Chapple C (2002) Rewriting the lignin roadmap. Curr Opin Plant Biol 5:224–229

    Article  PubMed  CAS  Google Scholar 

  • Huntley SK, Ellis D, Gilbert M, Chapple C, Mansfield SD (2003) Significant increases in pulping efficiency in C4H-F5H transformed poplars: improved chemical savings and reduced environmental toxins. J Agric Food Chem 51:6178–6183

    Article  PubMed  CAS  Google Scholar 

  • Hussey SG, Mizrachi E, Spokevicius AV, Bossinger G, Berger DK, Myburg AA (2011) SND2, a NAC transcription factor gene, regulates genes involved in secondary cell wall development in Arabidopsis fibres and increases fibre cell area in Eucalyptus. BMC Plant Biol 11:173

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106

    Article  PubMed  CAS  Google Scholar 

  • James C (2015) 20th Anniversary (1996 to 2015) of the global commercialization of biotech crops and biotech crop highlights in 2015. ISAAA Brief No. 51. ISAAA, Ithaca

    Google Scholar 

  • Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environ 7:153–164

    CAS  Google Scholar 

  • Jeon H-W, Cho J-S, Park E-J, Han K-H, Choi Y-I, Ko J-H (2016) Developing xylem-preferential expression of PdGA20ox1, a gibberellin 20-oxidase 1 from Pinus densiflora, improves woody biomass production in a hybrid poplar. Plant Biotechnol J 14:1161–1170

    Article  PubMed  CAS  Google Scholar 

  • Jia C, Zhao H, Wang H, Xing Z, Du K, Song Y, Wei J (2004) Obtaining the transgenic poplars with low lignin content through down-regulation of 4CL. Chin Sci Bull 49:905–909

    CAS  Google Scholar 

  • Jia H, Orbovic V, Jones JB, Wang N (2016) Modification of the PthA4 effector binding elements in type I CsLOB1 promoter using Cas9/sgRNA to produce transgenic Duncan grapefruit alleviating XccΔpthA4:dCsLOB1.3 infection. Plant Biotechnol J 14:1291–1301

    Article  PubMed  CAS  Google Scholar 

  • Jia H, Zhang Y, Orbovic V, Xu J, White FF, Jones JB, Wang N (2017) Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnol J 15:817–823

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jin Y-L, Tang R-J, Wang H-H, Jiang C-M, Bao Y, Yang Y, Liang M-X, Sun Z-C, Kong F-J, Li B, Zhang H-X (2017) Overexpression of Populus trichocarpa CYP85A3 promotes growth and biomass production in transgenic trees. Plant Biotechnol J 15:1309–1321

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821

    Article  PubMed  CAS  Google Scholar 

  • Jing ZP, Gallardo F, Pascual MB, Sampalo R, Romero J, de Navarra AT, Cánovas FM (2004) Improved growth in a field trial of transgenic hybrid poplar overexpressing glutamine synthetase. New Phytol 164:137–145

    Article  CAS  Google Scholar 

  • John E, Maqbool A, Malik KA (2014) Optimization of Agrobacterium tumefaciens mediated transformation in Populus deltoides. Pak J Bot 46:1079–1086

    CAS  Google Scholar 

  • Johnson LPV (1939) The breeding of forest trees. For Chron 15:139–151

    Article  Google Scholar 

  • Joshi CP, Thammannagowda S, Fujino T, Gou J-Q, Avci U, Haigler CH, McDonnell LM, Mansfield SD, Mengesha B, Carpita NC, Harris D, Debolt S, Peter GF (2011) Perturbation of wood cellulose synthesis causes pleiotropic effects in transgenic aspen. Mol Plant 4:331–345

    Article  PubMed  CAS  Google Scholar 

  • Kania T, Russenberger D, Peng S, Apel K, Melzer S (1997) FPF1 promotes flowering in Arabidopsis. Plant Cell 9:1327–1338

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Karel TH, Man G.(2017) Major forest insect and disease conditions in the United States: 2015. Forest Service, United States Department Agriculture, Forest Health Protection, Washington

  • Karlen SD, Zhang C, Peck ML, Smith RA, Padmakshan D, Helmich KE, Free HCA, Lee S, Smith BG, Lu F, Sedbrook JC, Sibout R, Grabber JH, Runge TM, Mysore KS, Harris PJ, Bartley LE, Ralph J (2016) Monolignol ferulate conjugates are naturally incorporated into plant lignins. Sci Adv 2:e1600393

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Karvelis T, Gasiunas G, Young J, Bigelyte G, Silanskas A, Cigan M, Siksnys V (2015) Rapid characterization of CRISPR-Cas9 protospacer adjacent motif sequence elements. Genome Biol 16:253

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kawaoka A, Matsunaga E, Endo S, Kondo S, Yoshida K, Shinmyo A, Ebinuma H (2003) Ectopic expression of a horseradish peroxidase enhances growth rate and increases oxidative stress resistance in hybrid aspen. Plant Physiol 132:1177–1185

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim Y-G, Cha J, Chandrasegaran S (1996) Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proc Natl Acad Sci U S A 93:1156–1160

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kim Y-H, Kim MD, Choi YI, Park S-C, Yun D-J, Noh EW, Lee H-S, Kwak S-S (2011) Transgenic poplar expressing Arabidopsis NDPK2 enhances growth as well as oxidative stress tolerance. Plant Biotechnol J 9:334–347

    Article  PubMed  CAS  Google Scholar 

  • Kirst M (2014) Material and methods to increase plant growth and yield. US Patent Application US 20140201867 A1

  • Kleczkowski LA (1994) Glucose activation and metabolism through UDP-glucose pyrophosphorylase in plants. Phytochemistry 37:1507–1515

    Article  CAS  Google Scholar 

  • Kleinstiver BP, Prew MS, Tsai SQ, Topkar VV, Nguyen NT, Zheng Z, Gonzales APW, Li Z, Peterson RT, Yeh J-RJ, Aryee MJ, Joung JK (2015) Engineered CRISPR-Cas9 nucleases with altered PAM specificities. Nature 523:481–485

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klintenäs M, Pin PA, Benlloch R, Ingvarsson PK, Nilsson O (2012) Analysis of conifer FLOWERING LOCUS T/TERMINAL FLOWER1-like genes provides evidence for dramatic biochemical evolution in the angiosperm FT lineage. New Phytol 196:1260–1273

    Article  PubMed  CAS  Google Scholar 

  • Klocko AL, Borejsza-Wysocka E, Brunner AM, Shevchenko O, Aldwinckle H, Strauss SH (2016c) Transgenic suppression of AGAMOUS genes in apple reduces fertility and increases floral attractiveness. PLoS One 11:e0159421

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Klocko AL, Brunner AM, Huang J, Meilan R, Lu H, Ma C, Morel A, Zhao D, Ault K, Dow M, Howe G, Shevchenko O, Strauss SH (2016b) Containment of transgenic trees by suppression of LEAFY. Nat Biotechnol 34:918–922

    Article  PubMed  CAS  Google Scholar 

  • Klocko AL, Ma C, Robertson S, Esfandiari E, Nilsson O, Strauss SH (2016a) FT overexpression induces precocious flowering and normal reproductive development in Eucalyptus. Plant Biotechnol J 14:808–819

    Article  PubMed  CAS  Google Scholar 

  • Klocko AL, Meilan R, James RR, Viswanath V, Ma C, Payne P, Miller L, Skinner JS, Oppert B, Cardineau GA, Strauss SH (2013) Bt-Cry3Aa transgene expression reduces insect damage and improves growth in field-grown hybrid poplar. Can J For Res 44:28–35

  • Koester RP, Skoneczka JA, Cary TR, Diers BW, Ainsworth EA (2014) Historical gains in soybean (Glycine max Merr.) seed yield are driven by linear increases in light interception, energy conversion, and partitioning efficiencies. J Exp Bot 65:3311–3321

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kong L, Holtz CT, Nairn CJ, Houke H, Powell WA, Baier K, Merkle SA (2014) Application of airlift bioreactors to accelerate genetic transformation in American chestnut. Plant Cell Tissue Organ Cult 117:39–50

    Article  CAS  Google Scholar 

  • Kontunen-Soppela S, Sillanpää M, Tuhkanen E-M, Sutinen S, Kangasjärvi J, Vapaavuori E, Häggman H (2010) Photosynthetic characteristics in genetically modified sense-RbcS silver birch lines. J Plant Physiol 167:820–828

    Article  PubMed  CAS  Google Scholar 

  • Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698

    Article  PubMed  CAS  Google Scholar 

  • Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:857–861

    Article  PubMed  CAS  Google Scholar 

  • Kumar M, Turner S (2015) Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 112:91–99

    Article  PubMed  CAS  Google Scholar 

  • Lachance D, Hamel L-P, Pelletier F, Valéro J, Bernier-Cardou M, Chapman K, van Frankenhuyzen K, Séguin A (2007) Expression of a Bacillus thuringiensis cry1Ab gene in transgenic white spruce and its efficacy against the spruce budworm (Choristoneura fumiferana). Tree Genet Genomes 3:153–167

    Article  Google Scholar 

  • Lane BG (1994) Oxalate, germin, and the extracellular matrix of higher plants. FASEB J 8:294–301

    Article  PubMed  CAS  Google Scholar 

  • Leplé J-C, Dauwe R, Morreel K, Storme V, Lapierre C, Pollet B, Naumann A, Kang K-Y, Kim H, Ruel K, Lefèbvre A, Josseleau J-P, Grima-Pettenati J, De Rycke R, Andersson-Gunnerás S, Erban A, Fehrle I, Petit-Conil M, Kopka J, Polle A, Messens E, Sundberg B, Mansfield SD, Ralph J, Pilate G, Boerjan W (2007) Downregulation of cinnamoyl-coenzyme a reductase in poplar: multiple-level phenotyping reveals effects on cell wall polymer metabolism and structure. Plant Cell 19:3669–3691

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lebedev V, Faskhiev V, Shestibratov K (2015) Lack of correlation between ammonium accumulation and survival of transgenic birch plants with pine cytosolic glutamine synthetase gene after “Basta” herbicide treatment. J Bot 2015:749356

    Google Scholar 

  • Lebedev VG, Schestibratov KA, Shadrina TE, Bulatova IV, Abramochkin DG, Miroshnikov AI (2010) Cotransformation of aspen and birch with three T-DNA regions from two different replicons in one Agrobacterium tumefaciens strain. Russ J Genet 46:1282–1289

    Article  CAS  Google Scholar 

  • LeBlanc MS, Lima A, Montello P, Kim T, Meagher RB, Merkle SA (2011) Enhanced arsenic tolerance of transgenic eastern cottonwood plants expressing gamma-glutamylcysteine synthetase. Int J Phytoremediation 13:657–673

    Article  PubMed  CAS  Google Scholar 

  • Lee C, Teng Q, Huang W, Zhong R, Ye Z-H (2009) Down-regulation of PoGT47C expression in poplar results in a reduced glucuronoxylan content and an increased wood digestibility by cellulase. Plant Cell Physiol 50:1075–1089

    Article  PubMed  CAS  Google Scholar 

  • Lemmetyinen J, Järvinen P, Pasonen H-L, Keinonen K, Lännenpää M, Keinänen M (2008) Birches. In: Kole C, Hall TC (eds) Compendium of transgenic crop plants, Transgenic forest tree species, vol 9. Blackwell Publishing Ltd, West Sussex, pp 193–218

    Chapter  Google Scholar 

  • Leslie CA, Uratsu SL, McGranahan G, Dandekar AM (2006) Walnut (Juglans). In: Wang K (ed) Methods in molecular biology, vol 344, Agrobacterium protocols, vol 2. Humana Press, Totowa, pp 297–307

    Chapter  Google Scholar 

  • Li D, Song S, Xia X, Yin W (2012) Two CBL genes from Populus euphratica confer multiple stress tolerance in transgenic triploid white poplar. Plant Cell Tissue Organ Cult 109:477–489

    Article  CAS  Google Scholar 

  • Li H, Wu D, Wang Z, Liu F, Liu G, Jiang J (2016a) BpMADS12 mediates endogenous hormone signaling: effect on plant development Betula platyphylla. Plant Cell Tissue Organ Cult 124:169–180

    Article  CAS  Google Scholar 

  • Li H, Ye K, Shi Y, Cheng J, Zhang X, Yang S (2017) BZR1 positively regulates freeze tolerance via CBF-dependent and CBF-independent pathways in Arabidopsis. Mol Plant 10:545–559

    Article  PubMed  CAS  Google Scholar 

  • Li L, Zhou Y, Cheng X, Sum J, Marita JM, Ralph J, Chiang VL (2003) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci U S A 100:4939–4944

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li M, Li H, Jiang H, Wu G (2008) Establishment of a highly efficient Agrobacterium tumefaciens-mediated leaf disc transformation method for Broussonetia papyrifera. Plant Cell Tissue Organ Cult 93:249–255

    Article  CAS  Google Scholar 

  • Li M-R, Li Y, Li H-Q, Wu G-J (2011a) Ectopic expression of FaDREB2 enhances osmotic tolerance in paper mulberry. J Integr Plant Biol 53:951–960

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Min D, Wang JP-Y, Peszlen I, Horvath L, Horvath B, Nishimura Y, Jameel H, Chang H-M, Chiang VL (2011b) Down-regulation of glycosyltransferase 8D genes in Populus trichocarpa caused reduced mechanical strength and xylan content in wood. Tree Physiol 31:226–236

    Article  PubMed  CAS  Google Scholar 

  • Li T, Huang S, Jiang WZ, Wright D, Spalding MH, Weeks DP, Yang B (2010) TAL nucleases (TALNs): hybrid proteins composed of TAL effectors and FokI DNA-cleavage domain. Nucleic Acids Res 39:359–372

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Li W, Hu W, Fang C, Chen L, Zhuang W, Katin-Grazzini L, McAvoy RJ, Guillard K, Li Y (2016b) An AGAMOUS intron-driven cytotoxin leads to flowerless tobacco and produces no detrimental effects on vegetative growth of either tobacco or poplar. Plant Biotechnol J 14:2276–2287

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liang H, Frost CJ, Wei X, Brown NR, Carlson JE, Tien M (2008) Improved sugar release from lignocellulosic material by introducing a tyrosine-rich cell wall peptide gene in poplar. Clean 36:662–668

    CAS  Google Scholar 

  • Liang H, Maynard CA, Allen RD, Powell WA (2001) Increased Septoria musiva resistance in transgenic hybrid poplar leaves expressing a wheat oxalate oxidase gene. Plant Mol Biol 45:619–629

    Article  PubMed  CAS  Google Scholar 

  • Liang Q (2011) Forward. In: Shu QY, Forster BP, Nakagawa H (eds) Plant mutation breeding and biotechnology, joint FAO. IAEA, Vienna Austria, p 1

    Google Scholar 

  • Liang Z, Chen K, Li T, Zhang Y, Wang Y, Zhao Q, Liu J, Zhang H, Liu C, Ran Y, Gao C (2017) Efficient DNA-free genome editing of bread wheat using CRISPR/Cas9 ribonucleoprotein complexes. Nat Commun 8:14261

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci U S A 103:6398–6403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lima MD, Eloy NB, Siqueira JA, Inze D, Hemerly AS, Ferreira PC (2017) Molecular mechanisms of biomass increase in plants. Biotechnol Res Innov 1:14–25

    Article  Google Scholar 

  • Lin C-Y, Li Q, Tunlaya-Anukit S, Shi R, Sun H-Y, Wang JP, Liu J, Loziuk P, Edmunds CW, Miller ZD, Peszlen I, Muddiman DC, Sederoff RR, Chiang VL (2016) A cell wall-bound anionic peroxidase, PtrPO21, is involved in lignin polymerization in Populus trichocarpa. Tree Genet Genomics 12:22

    Article  Google Scholar 

  • Lin M-K, Belanger H, Lee Y-J, Varkonyi-Gasic E, Taoka K-I, Miura E, Xoconostle-Cázares B, Gendler K, Jorgensen RA, Phinney B, Lough TJ, Lucas WJ (2007) FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19:1488–1506

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin Y-C, Li W, Sun Y-H, Kumari S, Wei H, Li Q, Tunlaya-Anukit S, Sederoff RR, Chiang VL (2013) SND1 transcription factor-directed quantitative functional hierarchical genetic regulatory network in wood formation in Populus trichocarpa. Plant Cell 25:4324–4341

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu FH, Sun ZX, Cui DC, Du BX, Wang CR, Chen SY (2000) Cloning of E.coli mtl-D gene and its expression in transgenic Balizhuangyang (Populus). Acta Genet Sin 27:428–433

    PubMed  CAS  Google Scholar 

  • Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu X, Pijut PM (2010) Agrobacterium-mediated transformation of mature Prunus serotina (black cherry) and regeneration of transgenic shoots. Plant Cell Tissue Organ Cult 101:49–57

    Article  CAS  Google Scholar 

  • Lotan T, Ohto M-a, Yee KM, West MAL, Lo R, Kwong RL, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    Article  PubMed  CAS  Google Scholar 

  • Lowe K, Hoerster G, Sun X, Rasco-Gaunt S, Lazerri P, Abbitt S, Glassman K, Gordon-Kamm B (2002) Maize LEC1 improves transformation in both maize and wheat. In: Vasil IK (ed) Plant biotechnology 2002 and beyond. Kluwer Academic Publishers, Dordrecht, pp 255–258

    Google Scholar 

  • Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho M-J, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, Rudrappa B, Shamseer PM, Bruce W, Newman L, Shen B, Zheng P, Bidney D, Falco C, Register J, Zhao Z-Y, Xy D, Jones T, Gordon-Kamm W (2016) Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell 28:1998–2015

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lu F, Marita JM, Lapierre C, Jouanin L, Morreel K, Boerjan W, Ralph J (2010) Sequencing around 5-hydroxyconiferyl alcohol-derived units in caffeic acid O-methlytransferase-deficient poplar lignins. Plant Physiol 153:569–579

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu H, Klocko AL, Dow M, Ma C, Amarasinghe V, Strauss SH (2016) Low frequency of zinc-finger nuclease-induced mutagenesis in Populus. Mol Breed 36:121

    Article  CAS  Google Scholar 

  • Lu H, Viswanath V, Ma C, Etherington E, Dharmawardhana P, Shevchenko O, Strauss SH, Pearce DW, Rood SB, Busov V (2015) Recombinant DNA modification of gibberellin metabolism alters growth rate and biomass allocation in Populus. Tree Genet Genomes 11:127

    Article  Google Scholar 

  • Lu M, Zhang P, Wang J, Kang X, Wu J, Wang X, Chen Y (2014) Induction of tetraploidy using high temperature exposure during the first zygote division in Populus adenopoda Maxim. Plant Growth Regul 72:279–287

    Article  CAS  Google Scholar 

  • Lu S, Li Q, Wei H, Chang M-J, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun Y-H, Yuan L, Yeh T-F, Peszlen I, Ralph J, Sederoff RR, Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci U S A 110:10848–10853

    Article  PubMed  PubMed Central  Google Scholar 

  • Lyyra S, Meagher RB, Kim T, Heaton A, Montello P, Balish RS, Merkle SA (2007) Coupling two mercury resistance genes in eastern cottonwood enhances the processing of organomercury. Plant Biotechnol J 5:254–262

    Article  PubMed  CAS  Google Scholar 

  • Maheshwari P, Kovalchuk I (2016) Agrobacterium-mediated stable genetic transformation of Populus angustifolia and Populus balsamifera. Front Plant Sci 7:296

    Article  PubMed  PubMed Central  Google Scholar 

  • Mallón R, Valladares S, Corredoira E, Vieitez AM, Vidal N (2014) Overexpression of the chestnut CsTL1 gene coding for a thaumatin-like protein in somatic embryos of Quercus robur. Plant Cell Tiss Org Cult 116:141–151

  • Mallón R, Vieitez AM, Vidal N (2013) High-efficiency Agrobacterium-mediated transformation in Quercus robur: selection by use of a temporary immersion system and assessment by quantitative PCR. Plant Cell Tissue Organ Cult 114:171–185

    Article  CAS  Google Scholar 

  • Maloney VJ, Mansfield SD (2010) Characterization and varied expression of a membrane-bound endo-β-1, 4-glucanase in hybrid poplar. Plant Biotechnol J 8:294–307

    Article  PubMed  CAS  Google Scholar 

  • Maloney VJ, Park J-Y, Unda F, Mansfield SD (2015) Sucrose phosphate synthase and sucrose phosphate phosphatase interact in planta and promote plant growth and biomass accumulation. J Exp Bot 66:4383–4394

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Maloney VJ, Samuels AL, Mansfield SD (2012) The endo-1, 4-β-glucanase Korrigan exhibits functional conservation between gymnosperms and angiosperms and is required for proper cell wall formation in gymnosperms. New Phytol 193:1076–1087

    Article  PubMed  CAS  Google Scholar 

  • Mansfield SD (2009) Solutions for dissolution – engineering cell walls for deconstruction. Curr Opin Biotechnol 20:286–294

    Article  PubMed  CAS  Google Scholar 

  • Mansfield SD, Kang K-Y, Chapple C (2012) Designed for deconstruction—poplar trees altered in cell wall lignification improve the efficacy of bioethanol production. New Phytol 194:91–101

    Article  PubMed  CAS  Google Scholar 

  • Marita JM, Ralph J, Lapierre C, Jouanin L, Boerjan W (2001) NMR characterization of lignins from transgenic poplars with suppressed caffeic acid O-methyltransferase activity. J Chem Soc Perkin Trans 1:2939–2945

    Article  CAS  Google Scholar 

  • Maruyama TE, Hosoi Y (2015) Somatic embryogenesis in Japanese black pine (Pinus thunbergii Parl.). In: Mujib A (ed) Somatic embryogenesis in ornamentals and its applications. Springer, India, pp 27–39

    Google Scholar 

  • Matsson M, Schjoerring JK (1997) Ammonia exchange between plants and the atmosphere: effects of ammonium supply to the roots, dark-induced senescence and reduced GS activity. In: Ando T, Fujita M, Mae T, Matsumoto H, Mori S, Sekiya J (eds) Plant nutrition for sustainable food production and environment, developments in plant and soil sciences, vol 78. Springer, Dordrecht, pp 827–831

    Chapter  Google Scholar 

  • Matsunaga E, Nanto K, Oishi M, Ebinuma H, Morishita Y, Sakurai N, Suzuki H, Shibata D, Shimada T (2012) Agrobacterium-mediated transformation of Eucalyptus globulus using explants with shoot apex with introduction of bacterial choline oxidase gene to enhance salt tolerance. Plant Cell Rep 31:225–235

    Article  PubMed  CAS  Google Scholar 

  • Maynard CA, McGuigan LD, Oakes AD, Zhang B, Newhouse AE, Northern LC, Chartrand AM, Will LR, Baier KM, Powell WA (2015) Chestnut, American (Castanea dentata (Marsh.) Borkh.). In: Wang K (ed) Agrobacterium protocols, vol 2, Methods in molecular biology, vol 1224. Springer Sci Bus Media, New York, pp 143–161

    Google Scholar 

  • Maynard CA, Polin LD, LaPierre SL, Rothrock RE, Powell WA (2006) American chestnut (Castanea dentata (Marsh.) Borkh.). In: Wang K (ed) Methods in molecular biology, vol 344, Agrobacterium protocols, vol 2, 2nd edn. Humana Press Inc., Totowa, pp 239–251

    Google Scholar 

  • Maynard CA, Powell WA, Polin-McGuigan LD, Viéitez AM, Ballester A, Corredoira E, Merkle SA, Andrade GM (2008) Chestnut. In: Kole C, Hall TC (eds) Compendium of transgenic crop plants, Transgenic forest tree species, vol 9. Blackwell Publishing Ltd, West Sussex, pp 169–192

    Chapter  Google Scholar 

  • McAllister CH, Beatty PH, Good AG (2012) Engineering nitrogen use efficient crop plants: the current status. Plant Biotechnol J 10:1011–1025

    Article  PubMed  CAS  Google Scholar 

  • McKown AD, Klápště J, Guy RD, Geraldes A, Porth I, Hannemann J, Friedmann M, Muchero W, Tuskan GA, Ehlting J, Cronk QCB, El-Kassaby YA, Mansfield SD, Douglas CJ (2014) Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa. New Phytol 203:535–553

    Article  PubMed  CAS  Google Scholar 

  • McGarry RC, Klocko AL, Pang M, Strauss SH, Ayre BG (2017) Virus-induced flowering: an application of reproductive biology to benefit plant research and breeding. Plant Physiol 173:47–55

    Article  PubMed  CAS  Google Scholar 

  • Mellerowicz EJ, Baucher M, Sundberg B, Boerjan W (2001) Unravelling cell wall formation in the woody dicot stem. Plant Mol Biol 47:239–274

    Article  PubMed  CAS  Google Scholar 

  • Mellway RD, Tran LT, Prouse MB, Campbell MM, Constabel CP (2009) The wound-, pathogen-, and ultraviolet B-responsive MYB134 gene encodes and R2R3 MYB transcription factor that regulates proanthocyanidin synthesis in poplar. Plant Physiol 150:924–941

    Article  PubMed  PubMed Central  Google Scholar 

  • Mendonça EG, Stein VC, Balieiro FP, Lima CDF, Santos BR, Paiva LV (2013) Genetic transformation of Eucalyptus camaldulensis by Agrobolistic method. Rev Árvore 37:419–429

    Article  Google Scholar 

  • Merkle SA, Battle PJ (2000) Enhancement of embryogenic culture initiation from tissues of mature sweetgum trees. Plant Cell Rep 19:268–273

    Article  CAS  Google Scholar 

  • Merkle SA, Montello PM, Reece HM, Kong L (2014) Somatic embryogenesis and cryostorage of eastern hemlock and Carolina hemlock for conservation and restoration. Trees 28:1767–1776

    Article  Google Scholar 

  • Merkle SA, Narin CJ (2005) Hardwood tree biotechnology. In Vitro Cell Dev Biol Plant 41:602–619

    Article  CAS  Google Scholar 

  • Merkle SA, Neu KA, Battle PJ, Bailey RL (1998) Somatic embryogenesis and plantlet regeneration from immature and mature tissues of sweetgum (Liquidambar styraciflua). Plant Sci 132:169–178

    Article  CAS  Google Scholar 

  • Merkle SA, Wiecko AT, Watson-Pauley BA (1991) Somatic embryogenesis in American chestnut. Can J For Res 21:1698–1701

    Article  Google Scholar 

  • Meyermans H, Morreel K, Lapierre C, Pollet B, De Bruyn A, Busson R, Herdewijn P, Devreese B, Van Beeumen J, Marita JM, Ralph J, Chen C, Burrggraeve B, Van Montagu M, Messens E, Boerjan W (2000) Modification in lignin and accumulation of phenolic glucosides in poplar xylem upon down-regulation of caffeoyl-coenzyme A O-methyltransferase, an enzyme involved in lignin biosynthesis. J Biol Chem 275:36899–36909

    Article  PubMed  CAS  Google Scholar 

  • Michler CH, Pijut PM, Meilan R, Smagh G, Liang X, Woeste KE (2008) Black walnut. In: Kole C, Hall TC (eds) Compendium of transgenic crop plants, Transgenic forest tree species, vol 9. Wiley-Blackwell, Chichester, pp 263–278

    Chapter  Google Scholar 

  • Min D, Li Q, Jameel H, Chiang V, Chang H-M (2012) The cellulase-mediated saccharification on wood derived from transgenic low-lignin lines of black cottonwood (Populus trichocarpa). Appl Biochem Biotechnol 168:947–955

    Article  PubMed  CAS  Google Scholar 

  • Min D, Yang C, Shi R, Jameel H, Chiang V, Chang H (2013) The elucidation of the lignin structure effect on the cellulase-mediated saccharification by genetic engineering poplars (Populus nigra L. × Populus maximowiczii a.). Biomass Bioenergy 58:52–57

    Article  CAS  Google Scholar 

  • Min D-Y, Li Q, Chiang V, Jameel H, Chang H-M, Lucia L (2014b) The influence of lignin-carbohydrate complexes on the cellulase-mediated saccharification I: transgenic black cottonwood (western balsam poplar, California poplar) P. trichocarpa including the xylan down-regulated and the lignin down-regulated lines. Fuel 119:207–213

    Article  CAS  Google Scholar 

  • Min D-Y, Yang C, Chiang V, Jameel H, Chang H-M (2014a) The influence of lignin-carbohydrate complexes on the cellulase-mediated saccharification II: transgenic hybrid poplars (Populus nigra L. × Populus maximowiczii A.). Fuel 116:56–62

    Article  CAS  Google Scholar 

  • Mohamed R, Wang C-T, Ma C, Shevchenko O, Dye SJ, Puzey JR, Etherington E, Sheng X, Meilan R, Strauss SH, Brunner AM (2010) Populus CEN/TFL1 regulates first onset of flowering, axillary meristem identity and dormancy release in Populus. Plant J 62:674–688

    Article  PubMed  CAS  Google Scholar 

  • Morreel K, Ralph J, Kim H, Lu F, Goeminne G, Ralph S, Messens E, Boerjan W (2004) Profiling of oligolignols reveals monolignol coupling conditions in lignifying poplar xylem. Plant Physiol 136:3537–3549

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mottiar Y, Vanholme R, Boerjan W, Ralph J, Mansfield SD (2016) Designer lignins: harnessing the plasticity of lignification. Curr Opin Biotechnol 37:190–200

    Article  PubMed  CAS  Google Scholar 

  • Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, Jenkins J, Lindquist E, Tice H, Bauer D, Goodstein DM, Dubchak I, Poliakov A, Mizrachi E, Kullan ARK, Hussey SG, Pinard D, van der Merwe K, Singh P, van Jaarsveld I, Silva-Junior OB, Togawa RC, Pappas MR, Faria DA, Sansaloni CP, Petroli CD, Yang X, Ranjan P, Tschaplinski TJ, Ye C-Y, Li T, Sterck L, Vanneste K, Mutate F, Soler M, Clemente HS, Saidi N, Cassan-Wang H, Dunand C, Hefer CA, Bornberg-Bauer E, Kersting AR, Vining K, Amarasinghe V, Ranik M, Naithani S, Elser J, Boyd AE, Liston A, Spatafora JW, Dharmwardhana P, Raja R, Sullivan C, Romanel E, Alves-Ferreira M, Külheim C, Foley W, Carocha V, Paiva J, Kudrna D, Brommonschenkel SH, Pasquali G, Byrne M, Rigault P, Tibbits J, Spokevicius A, Jones RC, Steane DA, Vaillancourt RE, Potts BM, Joubert F, Barry K, Pappas GJ Jr, Strauss SH, Jaiswal P, Grima-Pettenati J, Salse J, Van de Peer Y, Rokhsar DS, Schmutz J (2014) The genome of Eucalyptus grandis. Nature 510:356–362

    Article  PubMed  CAS  Google Scholar 

  • Nardmann J, Werr W (2006) The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution. Mol Biol Evol 23:2492–2504

    Article  PubMed  CAS  Google Scholar 

  • Neale DB, McGuire PE, Wheeler VC, Stevens KA, Crepeau MW, Cardeno C, Zimin AV, Puiu D, Pertea GM, Sezen UU, Casola C, Koralewski TE, Paul R, Gonzalez-Ibeas D, Zaman S, Cronn R, Yandell M, Holt C, Langley CH, Yorke JA, Salzberg SL, Wegrzyn JL (2017) The Douglas-fir genome sequence reveals specialization of the photosynthetic apparatus in Pinaceae. Genes Genomes Genetics 7:3157–3167

    PubMed  Google Scholar 

  • Neale DB, Wegrzyn JL, Stevens KA, Zimin AV, Puiu D, Crepeau MW, Cardeno C, Koriabine M, Holtz-Morris AE, Liechty JD, Martínez-García PJ, Vasquez-Gross HA, Lin BY, Zieve JJ, Dougherty WM, Fuentes-Soriano S, Wu L-S, Gilbert D, Marçais G, Roberts M, Holt C, Yandell M, Davis JM, Smith KE, Dean JFD, Lorenz WW, Whetten RW, Sederoff R, Wheeler N, McGuire PE, Main D, Loopstra CA, Mockaitis K, deJong PJ, Yorke JA, Salzberg SL, Langley CH (2014) Decoding the massive genome of loblolly pine using haploid DNA and novel assembly strategies. Genome Biol 15:R59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nehra NS, Becwar MR, Rottmann WH, Pearson L, Chowdhury K, Chang S, Wilde HD, Kodrzycki RJ, Zhang C, Gause KC, Parks DW, Hinchee MA (2005) Forest biotechnology: innovative methods, emerging opportunities. In Vitro Cell Dev Biol Plant 41:701–717

    Article  CAS  Google Scholar 

  • Newhouse AE, Kaczmar NS, Maynard CA, Powell WA (2008) American elm. In: Kole C, Hall TC (eds) Compendium of transgenic crop plants, Transgenic forest tree species, vol 4. Wiley-Blackwell, Chichester, pp 241–262

    Chapter  Google Scholar 

  • Newhouse AE, Polin-McGuigan LD, Baier KA, Valletta KER, Rottmann WH, Tschaplinski TJ, Maynard CA, Powell WA (2014) Transgenic American chestnuts show enhanced blight resistance and transmit the trait to T1 progeny. Plant Sci 228:88–97

    Article  PubMed  CAS  Google Scholar 

  • Newhouse AE, Schrodt F, Liang H, Maynard CA, Powell WA (2007) Transgenic American elm shows reduced Dutch elm disease symptoms and normal mycorrhizal colonization. Plant Cell Rep 26:977–987

    Article  PubMed  CAS  Google Scholar 

  • Newhouse AE, Schrodt F, Maynard CA, Powell WA (2006) American elm (Ulmus americana). In: Wang K (ed) Methods in molecular biology, vol 344, Agrobacterium protocols, vol 2, 2nd edn. Humana Press Inc., Totowa, pp 99–112

    Chapter  Google Scholar 

  • Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998) A plasma membrane-bound putative endo-1, 4-β-D-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Niskanen A-M, Kärkkäinen K, Pasonen H (2011) Comparison of variation in adaptive traits between wild-type and transgenic silver birch (Betula pendula) in a field trial. Tree Genet Genomes 7:955–967

    Article  Google Scholar 

  • Niu S, Li Z, Yuan H, Fang P, Chen X, Li W (2013) Proper gibberellin localization in vascular tissue is required to regulate adventitious root development in tobacco. J Exp Bot 64:3411–3424

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nystedt B, Street NR, Wetterbom A, Zuccolo A, Lin Y-C, Scofield DG, Vezzi F, Delhomme N, Giacomello S, Alexeyenko A, Vicedomini R, Sahlin K, Sherwood E, Elfstrand M, Gramzow L, Holmberg K, Hällman J, Keech O, Klasson L, Koriabine M, Kucukoglu M, Käller M, Luthman J, Lysholm F, Niittylä T, Olson A, Rilakovic N, Ritland C, Rosselló JA, Sena J, Svensson T, Talavera-López C, Theißen G, Tuominen H, Vanneste K, Wu Z-Q, Zhang B, Zerbe P, Arvestad L, Bhalerao R, Bohlmann J, Bousquet J, Garcia Gil R, Hvidsten TR, deJong P, MacKay J, Morgante M, Ritland K, Sundberg B, Thompson SL, Van de Peer Y, Andersson B, Nilsson O, Ingvarsson PK, Lundeberg J, Jansson S (2013) The Norway spruce genome sequence and conifer genome evolution. Nature 497:579–584

    Article  PubMed  CAS  Google Scholar 

  • Okumura S, Sawada M, Park YW, Hayashi T, Shimamura M, Takase H, Tomizawa K-I (2006) Transformation of poplar (Populus alba) plastids and expression of foreign proteins in tree chloroplasts. Transgenic Res 15:637–646

    Article  PubMed  CAS  Google Scholar 

  • Ó’Maoiléidigh DS, Graciet E, Wellmer F (2014) Gene networks controlling Arabidopsis thaliana flower development. New Phytol 201:16–30

    Article  PubMed  Google Scholar 

  • Ort DR, Merchant SS, Alric J, Barkan A, Blankenship RE, Bock R, Croce R, Hanson MR, Hibberd JM, Long SP, Moore TA, Moroney J, Niyogi KK, Parry MAJ, Peralta-Yahya PP, Prince RC, Redding KE, Spalding MH, van Wijk KJ, Vermaas WFJ, von Caemmerer S, Weber APM, Yeates TO, Yuan JS, Zhu XG (2015) Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc Natl Acad Sci U S A 112:8529–8536

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Palla KJ, Pijut PM (2015) Agrobacterium-mediated genetic transformation of Fraxinus americana hypocotyls. Plant Cell Tissue Organ Cult 120:631–641

    Article  CAS  Google Scholar 

  • Pasonen H-L, Lu J, Niskanen A-M, Seppänen S-K, Rytkönen A, Raunio J, Pappinen A, Kasanin R, Timonen S (2009) Effects of sugar beet chitinase IV on root-associated fungal community of transgenic silver birch in a field trial. Planta 230:973–983

    Article  PubMed  CAS  Google Scholar 

  • Pelloux J, Rustérucci C, Mellerowicz EJ (2007) New insights into pectin methylesterase structure and function. Trends Plant Sci 12:267–277

    Article  PubMed  CAS  Google Scholar 

  • Peng A, Chen S, Lei T, Xu L, He Y, Wu L, Yao L, Zou X (2017) Engineering canker-resistant plants through CRISPR/Cas9-targeted editing of the susceptibility gene CsLOB1 promoter in citrus. Plant Biotechnol J 15:1509–1519

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Petrik DL, Karlen SD, Cass CL, Padmakshan D, Lu F, Liu S, Le Bris P, Antelme S, Santoro N, Wilkerson CG, Sibout R, Lapierre C, Ralph J, Sadbrook JC (2014) p-Coumaroyl-CoA:monolignol transferase (PMT) acts specifically in the lignin biosynthetic pathway in Brachypodium distachyon. Plant J 77:713–726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pettersen RC (1984) The chemical composition of wood. In: Rowell RM (ed) The chemistry of solid wood. Advances in chemistry series, vol 207. American Chemical Society, Washington, DC, pp 57–126

    Chapter  Google Scholar 

  • Plasencia A, Soler M, Dupas A, Ladouce N, Silva-Martins G, Martinez Y, Lapierre C, Franche C, Truchet I, Grima-Pettenati J (2016) Eucalyptus hairy roots, a fast, efficient and versatile tool to explore function and expression of genes involved in wood formation. Plant Biotechnol J 14:1381–1393

    Article  PubMed  CAS  Google Scholar 

  • Polin LD, Liang H, Rothrock RE, Nishii M, Diehl DL, Newhouse AE, Nairn CJ, Powell WA, Maynard CA (2006) Agrobacterium-mediated transformation of American chestnut (Castanea dentata (marsh.) Borkh.) somatic embryos. Plant Cell Tissue Organ Cult 84:69–79

    Article  CAS  Google Scholar 

  • Porth I, Klapšte J, Skyba O, Hannemann J, McKown AD, Guy RD, DiFazio SP, Muchero W, Ranjan P, Tuskan GA, Friedmann MC, Ehlting J, Cronk QCB, El-Kassaby YA, Douglas CJ, Mansfield SD (2013) Genome-wide association mapping for wood characteristics in Populus identifies an array of candidate single nucleotide polymorphisms. New Phytol 200:710–726

    Article  PubMed  CAS  Google Scholar 

  • Qiao G, Zhou J, Jiang J, Sun Y, Pan L, Song H, Jiang J, Zhuo R, Wang X, Sun Z (2010) Transformation of Liquidambar formosana L. via Agrobacterium tumefaciens using a mannose selection system and recovery of salt tolerant lines. Plant Cell Tissue Organ Cult 102:163–170

    Article  CAS  Google Scholar 

  • Ralph J (2010) Hydroxycinnamates in lignification. Phytochem Rev 9:65–83

    Article  CAS  Google Scholar 

  • Ralph J, Akiyama T, Coleman HD, Mansfield SD (2012) Effects on lignin structure of coumarate 3-hydroxylase downregulation in poplar. Bioenerg Res 5:1009–1019

    Article  CAS  Google Scholar 

  • Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem Rev 3:29–60

    Article  CAS  Google Scholar 

  • Rennie EA, Scheller HV (2014) Xylan biosynthesis. Curr Opin Biotechnol 26:100–107

    Article  PubMed  CAS  Google Scholar 

  • Roach M, Gerber L, Sandquist D, Gorzsás A, Hedenström M, Kumar M, Steinhauser MC, Feil R, Daniel G, Stitt M, Sundberg B, Nittylä T (2012) Fructokinase is required for carbon partitioning to cellulose in aspen wood. Plant J 70:967–977

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell 171:470–480

    Article  PubMed  CAS  Google Scholar 

  • Rogers S, Wells R, Rechsteiner M (1986) Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 234:364–368

    Article  PubMed  CAS  Google Scholar 

  • Rothrock RE, Polin-McGuigan LD, Newhouse AE, Powell WA, Maynard CA (2007) Plate flooding as an alternative Agrobacterium-mediated transformation method for American chestnut somatic embryos. Plant Cell Tissue Organ Cult 88:93–99

    Article  Google Scholar 

  • Rottmann WH, Meilan R, Sheppard LA, Brunner AM, Skinner JS, Ma C, Cheng S, Jouanin L, Pilate G, Strauss SH (2000) Diverse effects of overexpression of LEAFY and PTLF, a poplar (Populus) homolog of LEAFY/FLORICAULA, in transgenic poplar and Arabidopsis. Plant J 22:235–245

    Article  PubMed  CAS  Google Scholar 

  • Rubinelli PM, Chuck G, Li X, Meilan R (2013) Constitutive expression of the Corngrass1 microRNA in poplar affects plant architecture and stem lignin content and composition. Biomass Bioenergy 54:312–321

    Article  CAS  Google Scholar 

  • Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A, Singh SP, Krishna P (2016) Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance. Sci Rep 6:28298

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Salomon S, Puchta H (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J 17:6086–6095

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sato S, Kato T, Kakegawa K, Ishii T, Liu Y-G, Awano T, Takabe K, Nishiyama Y, Kuga S, Sato S, Nakamura Y, Tabata S, Shibata D (2001) Role of the putative membrane-bound endo-1, 4-β-glucanase KORRIGAN in cell elongation and cellulose synthesis in Arabidopsis thaliana. Plant Cell Physiol 42:251–263

    Article  PubMed  CAS  Google Scholar 

  • Schmidt A, Wächtler B, Temp U, Krekling T, Séguin A, Gershenzon J (2010) A bifunctional geranyl and geranylgeranyl diphosphate synthase is involved in terpene oleoresin formation in Picea abies. Plant Physiol 152:639–655

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt M, Schwartzberg AM, Perera PN, Weber-Bargioni A, Carroll A, Sarkar P, Bosneaga E, Urban JJ, Song J, Balakshin MY, Capanema EA, Auer M, Adams PD, Chiang VL, Schuck PJ (2009) Label-free in situ imaging of lignification in the cell wall of low lignin transgenic Populus trichocarpa. Planta 230:589–597

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Schmidt R (2003) Fusiform rust of southern pines: a major success for forest disease management. Phytopathology 93:1048–1051

    Article  PubMed  Google Scholar 

  • Schwander T, von Borzyskowski LS, Burgener S, Cortina NS, Erb TJ (2016) A synthetic pathway for the fixation of carbon dioxide in vitro. Science 354:900–904

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Scorza R, Callahan A, Dardick C, Ravelonandro M, Polak J, Malinowski T, Zagrai I, Cambra M, Kamenova I (2013) Genetic engineering of Plum pox virus resistance: ‘HoneySweet’ plum – from concept to product. Plant Cell Tissue Organ Cult 115:1–12

    Article  CAS  Google Scholar 

  • Scorza R, Ravelonandro M, Callahan A, Zagrai I, Polak J, Malinowski T, Cambra M, Levy L, Damsteegt V, Krška B, Cordts J, Gonsalves D, Dardick C (2016) HoneySweet’ (C5), the first genetically engineered Plum pox virus–resistant plum (Prunus domestica L.) cultivar. HortScience 51:601–603

    CAS  Google Scholar 

  • Seppänen S-K, Pasonen H-L, Vauramo S, Vahala J, Toikka M, Kilpeläinen I, Setälä H, Teeri TH, Timonen S, Pappinen A (2007) Decomposition of the leaf litter and mycorrhiza forming ability of silver birch with a genetically modified lignin biosynthesis pathway. Appl Soil Ecol 36:100–106

    Article  Google Scholar 

  • Shao Z, Chen W, Luo H, Ye XF, Zhang J (2002) Studies on the introduction of the cecrpin d gene into Eucalyptus urophylla to breed the resistant varieties to Pseudomonas solanacearum. Sci Silvae Sin 38:92–97

    CAS  Google Scholar 

  • Sheikh Beig Goharrizi MA, Dejahang A, Tohidfar M, Izadi Darbandi A, Carillo N, Hajirezaei MR, Vahdat K (2016) Agrobacterium mediated transformation of somatic embryos of Persian walnut using fld gene for osmotic stress tolerance. J Agric Sci Technol 18:423–435

    Google Scholar 

  • Shen J-L, Li Y, Jiang J-Z, Chen S-Y (2008) Establishment of a transgenic system in fast-growing black locust (Robinia pseudoacacia L.). For Stud China 10:243–252

    Article  CAS  Google Scholar 

  • Shi Q, Liu P, Liu M, Wang J, Zhao J, Zhao Z, Dai L (2016) In vivo fast induction of homogeneous autopolyploids via callus in sour jujube (Ziziphus acidojujuba Cheng et Liu). Hortic Plant J 2:147–153

    Article  Google Scholar 

  • Shi Q-H, Liu P, Liu M-J, Wang J-R, Xu J (2015) A novel method for rapid in vivo induction of homogeneous polyploids via calluses in a woody fruit tree (Ziziphus jujuba mill.). Plant Cell Tissue Organ Cult 121:423–433

    Article  CAS  Google Scholar 

  • Shi X-X, Du G-Q, Wang X-M, Pei D (2012) Studies on gene transformation via pollen tube pathway in walnut. Acta Hortic Sin 39:1243–1252

    CAS  Google Scholar 

  • Siedlecka A, Wiklund S, Péronne M-A, Micheli F, Leśniewska J, Sethson I, Edlund U, Richard L, Sundberg B, Mellerowicz EJ (2008) Pectin methyl esterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. Plant Physiol 146:554–565

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Siegel D, Avisar D, Abramson M, Shani Z, Hirsch S (2013) Compositions and methods for enhancing plant photosynthetic activity. US Patent Application US 20130333073 A1

  • Simkin AJ, Lopez-Calcagno PE, Davey PA, Headland LR, Lawson T, Timm S, Bauwe H, Raines CA (2017) Simultaneous stimulation of sedoheptulose 1,7-bisphosphatase, fructose 1,6-bisphophate aldolase and the photorespiratory glycine decarboxylase-H protein increases CO2 assimilation, vegetative biomass and seed yield in Arabidopsis. Plant Biotechnol J 15:805–816

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simkin AJ, McAusland L, Headland LR, Lawson T, Raines CA (2015) Multigene manipulation of photosynthetic carbon assimilation increases CO2 fixation and biomass yield in tobacco. J Exp Bot 66:4075–4090

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Smith RA, Gonzales-Vigil E, Karlen SD, Park J-Y, Lu F, Wilkerson CG, Samuels L, Ralph J, Mansfield SD (2015) Engineering monolignol p-coumarate conjugates into poplar and Arabidopsis lignins. Plant Physiol 169:2992–3001

    PubMed  PubMed Central  CAS  Google Scholar 

  • Sollars ESA, Harper AL, Kelly LJ, Sambles CM, Ramirez-Gonzalez RH, Swarbreck D, Kaithakottil G, Cooper ED, Uauy C, Havlickova L, Worswick G, Studholme DJ, Zohren J, Salmon DL, Clavijo BJ, Li Y, He Z, Fellgett A, McKinney LV, Nielsen LR, Douglas GC, Kjær ED, Downie JA, Boshier D, Lee S, Clark J, Grant M, Bancroft I, Caccamo M, Buggs RJA (2017) Genome sequence and genetic diversity of European ash trees. Nature 541:212–216

    Article  PubMed  CAS  Google Scholar 

  • Song D, Gui J, Liu C, Sun J, Li L (2016) Suppression of PtrDUF579-3 expression causes structural changes of the glucuronoxylan in Populus. Front Plant Sci 7:493

    PubMed  PubMed Central  Google Scholar 

  • Song G-Q, Sink KC, Walworth AE, Cook MA, Allison RF, Lang GA (2013) Engineering cherry rootstocks with resistance to Prunus necrotic ring spot virus through RNAi-mediated silencing. Plant Biotechnol J 11:702–708

    Article  PubMed  CAS  Google Scholar 

  • Spokevicius AV, Van Beveren KS, Bossinger G (2006) Agrobacterium-mediated transformation of dormant lateral buds in poplar trees reveals developmental patterns in secondary stem tissues. Funct Plant Biol 33:133–139

    Article  CAS  Google Scholar 

  • Srinivasan C, Dardick C, Callahan A, Scorza R (2012) Plum (Prunus domestica) trees transformed with poplar FT1 result in altered architecture, dormancy requirement, and continuous flowering. PLoS One 7:e40715

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srinivasan C, Liu Z, Heidmann I, Supena EDJ, Fukuoka H, Joosen R, Lambalk J, Angenent G, Scorza R, Custers JBM, Boutilier K (2007) Heterologous expression of the BABY BOOM AP2/ERF transcription factor enhances the regeneration capacity of tobacco (Nicotiana tabacum L.). Planta 225:341–351

    Article  PubMed  CAS  Google Scholar 

  • Steiner KC, Westbrook JW, Hebard FV, Georgi LL, Powell WA, Fitzsimmons SF (2016) Rescue of American chestnut with extraspecific genes following its destruction by a naturalized pathogen. New For 48:317–336

    Article  Google Scholar 

  • Stevens ME, Pijut PM (2014) Agrobacterium-mediated genetic transformation and plant regeneration of the hardwood tree species Fraxinus profunda. Plant Cell Rep 33:861–870

    Article  PubMed  CAS  Google Scholar 

  • Stewart JJ, Akiyama T, Chapple C, Ralph J, Mansfield SD (2009) The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar. Plant Physiol 150:621–635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stipes RJ, Hunter PP, Elkins JR, Roane MK (1978) Endothia cankers of oaks. In: Santamour Jr FS (ed) Proc 1st Conf Metropolitan Tree Improvement Alliance (METRIA), METRIA, USDA Forest Service, The National Urban and Community Forestry Council, and North Carolina State University, https://www.ces.ncsu.edu/fletcher/programs/nursery/metria/, pp 97–120

  • Stone SL, Braybrook SA, Paula SL, Kwong LW, Meuser J, Pelletier J, Hsieh T-F, Fischer RL, Goldberg RB, Harada JJ (2008) Arabidopsis LEAFY COTYLEDON2 induces maturation traits and auxin activity: implications for somatic embryogenesis. Proc Natl Acad Sci U S A 105:3151–3156

    Article  PubMed  PubMed Central  Google Scholar 

  • Stover E, Stange RR Jr, McCollum TG, Jaynes J, Mirkov E (2013) Screening antimicrobial peptides in vitro for use in developing transgenic citrus resistant to Huanglongbing and citrus canker. J Am Soc Hortic Sci 138:142–148

    CAS  Google Scholar 

  • Strauss SH, Costanza A, Séguin A (2015) Genetically engineered trees: paralysis from good intentions. Science 349:794–795

    Article  PubMed  CAS  Google Scholar 

  • Strauss SH, Jones KN, Lu H, Petit JD, Klocko AL, Betts MG, Brosi BJ, Fletcher RJ Jr, Needham MD (2017) Reproductive modification in forest plantations: impacts on biodiversity and society. New Phytol 213:1000–1021

    Article  PubMed  Google Scholar 

  • Strauss SH, Rottmann WH, Brunner AM, Sheppard LA (1995) Genetic engineering of reproductive sterility in forest trees. Mol Breed 1:5–26

    Article  CAS  Google Scholar 

  • Strauss SH, Tan H, Boerjan W, Sedjo R (2009) Strangled at birth? Forest biotech and the convention on biological diversity. Nat Biotechnol 27:519–527

    Article  PubMed  CAS  Google Scholar 

  • Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4:401–407

    Article  PubMed  CAS  Google Scholar 

  • Suárez MF, Avila C, Gallardo F, Canton FR, García-Gutiérrez A, Gonzalo Claros M, Cánovas FM (2002) Molecular and enzymatic analysis of ammonium assimilation in woody plants. J Exp Bot 53:891–904

    Article  PubMed  Google Scholar 

  • Sugden A, Fahrenkamp-Uppenbrink J, Malakoff D, Vignieri S (2015) Forest health in a changing world. Science 349:800–801

    Article  PubMed  CAS  Google Scholar 

  • Sun J, Peng X, Fan W, Tang M, Liu J, Shen S (2014) Functional analysis of BpDREB2 gene involved in salt and drought response from a woody plant Broussonetia papyrifera. Gene 535:140–149

    Article  PubMed  CAS  Google Scholar 

  • Sun ZX, Yang HH, Cui DC, Zhao CZ, Zhao SP (2002) Analysis of salt resistance on the poplar transferred with salt tolerance gene. Chin J Biotechnol 18:481–485

    CAS  Google Scholar 

  • Sutela S, Hahl T, Tilmonen H, Aronen T, Ylioja T, Laakso T, Saranpää P, Chiang V, Julkunen-Tiitto R, Häggman H (2014) Phenolic compounds and expression in 4CL genes in silver birch clones and Pt4CL1a lines. PLoS One 9:e114434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suzuki JY, Tripathi S, Gonsalves D (2007) Virus-resistant transgenic papaya: commercial development and regulatory and environmental issues. In: Punja ZK, De Boer SH, Sanfaçon H (eds) Biotechnology and plant disease management. CAB Int, Wallingford, pp 436–461

    Chapter  Google Scholar 

  • Suzuki S, Sakakibara N, Li L, Umezawa T, Chiang VL (2010) Profiling of phenylpropanoid monomers in developing xylem tissue of transgenic aspen (Populus tremuloides). J Wood Sci 56:71–76

    Article  CAS  Google Scholar 

  • Svitashev S, Schwartz C, Lenderts B, Young JK, Cigan AM (2016) Genome editing in maize directed by CRISPR-Cas9 ribonucleoprotein. Nat Commun 7:13274

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sykes RW, Gjersing EL, Foutz K, Rottmann WH, Kuhn SA, Foster CE, Ziebell A, Turner GB, Decker SR, Hinchee MAW, Davis MF (2015) 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 8:128

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Takabe T, Uchida A, Shinagawa F, Terada Y, Kajita H, Tanaka Y, Takabe T, Hayashi T, Kawai T, Takabe T (2008) Overexpression of DnaK from a halotolerant cyanobacterium Aphanothece halophytica enhances growth rate as well as abiotic stress tolerance of poplar plants. Plant Growth Regul 56:265–273

    Article  CAS  Google Scholar 

  • Takahashi N, Koshijima T (1988) Ester linkages between lignin and glucuronoxylan in a lignin-carbohydrate complex from beech (Fagus crenata) wood. Wood Sci Technol 22:231–241

    Article  CAS  Google Scholar 

  • Tang W, Charles TM, Newton RJ (2005) Overexpression of the pepper transcription factor CaPF1 in transgenic Virginia pine (Pinus virginiana Mill.) confers multiple stress tolerance and enhances organ growth. Plant Mol Biol 59:603–617

    Article  PubMed  CAS  Google Scholar 

  • Taniguchi T, Ohmiya Y, Kurita M, Tsubomura M, Kondo T, Park YW, Baba K, Hayashi T (2008) Biosafety assessment of transgenic poplars overexpressing xyloglucanase (AaXEG2) prior to field trials. J Wood Sci 54:408–413

    Article  Google Scholar 

  • Tao R, Dandekar AM, Uratsu SL, Vail PV, Tebbets JS (1997) Engineering genetic resistance against insects in Japanese persimmon using the cryIA(c) gene of Bacillus thuringiensis. J Am Soc Hortic Sci 122:764–771

    CAS  Google Scholar 

  • Taylor JG, Owen TP Jr, Koonce LT, Haigler CH (1992) Dispersed lignin in tracheary elements treated with cellulose synthesis inhibitors provides evidence that molecules of the secondary cell wall mediate wall patterning. Plant J 2:959–970

    Article  CAS  Google Scholar 

  • Teper-Bamnolker P, Samach A (2005) The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell 17:2661–2675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • The International Peach Genome Initiative (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity domestication and genome evolution. Nat Genet 45:487–494

    Article  CAS  Google Scholar 

  • Tian XM, Xie J, Zhao YL, Lu H, Liu SC, Qu L, Li JM, Gai Y, Jiang XN (2013) Sense-, antisense- and RNAi-4CL1 regulate soluble phenolic acids, cell wall components and growth in transgenic Populus tomentosa Carr. Plant Physiol Biochem 65:111–119

    Article  PubMed  CAS  Google Scholar 

  • Tian YC, Zheng JB, YU HM, Liang HY, Li CQ, Wang JM (2000) Studies of transgenic hybrid poplar 741 carrying two insect-resistant genes. Acta Bot Sin 42:263–268

    CAS  Google Scholar 

  • Timell TE (1967) Recent progress in the chemistry of wood hemicelluloses. Wood Sci Technol 1:45–70

    Article  CAS  Google Scholar 

  • Tokumoto Y, Kajiura H, Takeno S, Harada Y, Suzuki N, Hosaka T, Gyokusen K, Nakazawa Y (2016) Induction of tetraploid hardy rubber tree, Eucommia ulmoides, and phenotypic differences from diploid. Plant Biotechnol 33:51–57

    Article  CAS  Google Scholar 

  • Turgeon R, Medville R (1998) The absence of phloem loading in willow leaves. Proc Natl Acad Sci U S A 95:12055–12060

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen G-L, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Déjardin A, de Pamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjärvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leplé J-C, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouzé P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai C-J, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Tuskan GA, Kalluri UC (2016) Gene impacting biomass formation and recalcitrance and methods of use. US Patent Application US20160326602 A1

  • United States Department of Agriculture Animal and Plant Health Inspection Service (2013) Freeze tolerant Eucalyptus environmental impact statement scoping meetings. https://www.aphis.usda.gov/aphis/ourfocus/biotechnology/stakeholder-meetings/ct_freeze_tolerant_eucalyptus Accessed 13 Dec 2017

  • United States Department of Agriculture Animal and Plant Health Inspection Service (2017) Petitions for determination of nonregulated status. https://www.aphis.usda.gov/aphis/ourfocus/biotechnology/permits-notifications-petitions/petitions/petition-status Accessed 13 Dec 2017

  • USDA Forest Service (2011) Western bark beetle strategy, Human safety, recovery and resiliency. United States Department Agriculture Forest Service. https://www.fs.usda.gov/Internet/FSE_DOCUMENTS/stelprdb5338089.pdf Accessed 8 Dec 2017

  • Van Beveren KS, Spokevicius AV, Tibbits J, Wang Q, Bossinger G (2006) Transformation of cambial tissue in vivo provides an efficient means for induced somatic sector analysis and gene testing in stems of woody plant species. Funct Plant Biol 33:629–638

    Article  Google Scholar 

  • Van Doorsselaere J, Baucher M, Chognot E, Chabbert B, Tollier M-T, Petit-Conil M, Leplé J-C, Pilate G, Cornu D, Monties B, Van Montagu M, Inzé D, Boerjan W, Jouanin L (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J 8:855–864

    Article  Google Scholar 

  • Vanholme R, Morreel K, Darrah C, Oyarce P, Grabber JH, Ralph J, Boerjan W (2012) Metabolic engineering of novel lignin in biomass crops. New Phytol 196:978–1000

    Article  PubMed  CAS  Google Scholar 

  • Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11:278–285

    Article  PubMed  CAS  Google Scholar 

  • Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M, Micheletti D, Moretto M, Perazzolli M, Si-Ammour A, Vezzulli S, Zini E, Eldredge G, Fitzgerald LM, Gutin N, Lanchbury J, Macalma T, Mitchell JT, Reid J, Wardell B, Kodira C, Chen Z, Desany B, Niazi F, Palmer M, Koepke T, Jiwan D, Schaeffer S, Krishnan V, Wu C, Chu VT, King ST, Vick J, Tao Q, Mraz A, Stormo A, Stormo K, Bogden R, Ederle D, Stella A, Vecchietti A, Kater MM, Masiero S, Lasserre P, Lespinasse Y, Allan AC, Bus V, Chagné D, Crowhurst RN, Gleave AP, Lavezzo E, Fawcett JA, Proost S, Rouzé P, Sterck L, Toppo S, Lazzari B, Hellens RP, Durel C-E, Gutin A, Bumgarner RE, Gardiner SE, Skolnick M, Egholm M, Van de Peer Y, Salamini F, Viola R (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839

    Article  PubMed  CAS  Google Scholar 

  • Velázquez K, Agüero J, Vives MC, Aleza P, Pina JA, Moreno P, Navarro L, Guerri J (2016) Precocious flowering of juvenile citrus induced by a viral vector based on Citrus leaf blotch virus: a new tool for genetics and breeding. Plant Biotechnol J 14:1976–1985

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vendrame W, Wetzstein H (2005) Carya illinoinensis Pecan. In: Litz RE (ed) Biotechnology of fruit and nut crops. CAB International, Wallingford, pp 298–306

  • Vidal N, Mallón R, Valladares S, Meijomín AM, Vieitez AM (2010) Regeneration of transgenic plants by Agrobacterium-mediated transformation of somatic embryos of juvenile and mature Quercus robur. Plant Cell Rep 29:1411–1422

    Article  PubMed  CAS  Google Scholar 

  • Vihervuori L, Lyytikäinen-Saarenmaa P, Lu J, Pasonen H-L (2013) Effects on lepidopteran herbivores of feeding on leaves of transgenic birch (Betula pendula) expressing the sugar beet chitinase IV gene. Eur J Entomol 110:253–262

    Article  CAS  Google Scholar 

  • Vihervuori L, Pasonen H-L, Lyytikäinen-Saarenmaa P (2008) Density and composition of an insect population in a field trial of chitinase transgenic and wild-type silver birch (Betula pendula) clones. Environ Entomol 37:1582–1591

    Article  PubMed  CAS  Google Scholar 

  • Vining KJ, Romanel E, Jones RC, Klocko A, Alves-Ferreira M, Hefer CA, Amarasinghe V, Dharmawardhana P, Naithani S, Ranik M, Wesley-Smith J, Solomon L, Jaiswal P, Myburg AA, Strauss SH (2015) The floral transcriptome of Eucalyptus grandis. New Phytol 206:1406–1422

    Article  PubMed  CAS  Google Scholar 

  • Viswanath V, Albrectsen BR, Strauss SH (2012) Global regulatory burden for field testing of genetically modified trees. Tree Genet Genomes 8:221–226

    Article  Google Scholar 

  • Voelker SL, Lachenbruch B, Meinzer FC, Kitin P, Strauss SH (2011b) Transgenic poplars with reduced lignin show impaired xylem conductivity, growth efficiency and survival. Plant Cell Environ 34:655–668

    Article  PubMed  Google Scholar 

  • Voelker SL, Lachenbruch B, Meinzer FC, Strauss SH (2011a) Reduced wood stiffness and strength, and altered stem form, in young antisense 4CL transgenic poplars with reduced lignin contents. New Phytol 189:1096–1109

    Article  PubMed  Google Scholar 

  • Voosen P (2014) Can genetic engineering save the Florida orange? In: Natl Geogr news http://news.nationalgeographic.com/news/2014/09/140914-florida-orange-citrus-greening-gmo-environment-science/ Accessed 21 Feb 2017

  • Wadenbäck J, von Arnold S, Egertsdotter U, Walter MH, Grima-Pettenati J, Goffner D, Gellerstedt G, Gullion T, Clapham D (2008) Lignin biosynthesis in transgenic Norway spruce plants harboring an antisense construct for cinnamoyl CoA reductase (CCR). Transgenic Res 17:379–392

    Article  PubMed  CAS  Google Scholar 

  • Wagner A, Donaldson L, Kim H, Phillips L, Flint H, Steward D, Torr K, Koch G, Schmitt U, Ralph J (2009) Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol 149:370–383

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wagner A, Ralph J, Akiyama T, Flint H, Phillips L, Torr K, Nanayakkara B, Te Kiri L (2007) Exploring lignification in conifers by silencing hydroxycinnamoyl-CoA: shikimate hydroxycinnamoyltransferase in Pinus radiata. Proc Natl Acad Sci U S A 104:11856–11861

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wagner A, Tobimatsu Y, Goeminne G, Philips L, Flint H, Steward D, Torr K, Donaldson L, Boerjan W, Ralph J (2013) Suppression of CCR impacts metabolite profile and cell wall composition in Pinus radiata tracheary elements. Plant Mol Biol 81:105–117

    Article  PubMed  CAS  Google Scholar 

  • Wagner A, Tobimatsu Y, Philips L, Flint H, Geddes B, Lu F, Ralph J (2015) Syringyl lignin production in conifers: proof of concept in a pine tracheary element system. Proc Natl Acad Sci U S A 112:6218–6223

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wagner A, Tobimatsu Y, Philips L, Flint H, Torr K, Donaldson L, Pears L, Ralph J (2011) CCoAOMT suppression modifies lignin composition in Pinus radiata. Plant J 67:119–129

    Article  PubMed  CAS  Google Scholar 

  • Walawage SL, Britton MT, Leslie CA, Uratsu SL, Li YY, Dandekar AM (2013) Stacking resistance to crown gall and nematodes in walnut rootstocks. BMC Genomics 14:668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wallsgrove RM, Turner JC, Hall NP, Kendall AC, Bright SWJ (1987) Barley mutants lacking chloroplast glutamine synthetase—biochemical and genetic analysis. Plant Physiol 83:155–158

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Waltz E (2016a) Gene-edited CRISPR mushroom escapes US regulation. Nature 532:293

    Article  PubMed  CAS  Google Scholar 

  • Waltz E (2016b) CRISPR-edited crops free to enter market, skip regulation. Nat Biotechnol 34:582

    Article  PubMed  CAS  Google Scholar 

  • Wang J-W, Park MY, Wang L-J, Koo Y, Chen X-Y, Weigel D, Poethig RS (2011) miRNA control of vegetative phase change in trees. PLoS Genet 7:e1002012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Y, Pijut PM (2014a) Improvement of Agrobacterium-mediated transformation and rooting of black cherry. In Vitro Cell Dev Biol Plant 50:307–316

    Article  CAS  Google Scholar 

  • Wang Y, Pijut PM (2014b) Agrobacterium-mediated transformation of black cherry for flowering control and insect resistance. Plant Cell Tissue Organ Cult 119:107–116

    Article  CAS  Google Scholar 

  • Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500

    Article  PubMed  CAS  Google Scholar 

  • Weigl K, Wenzel S, Flachowsky H, Peil A, Hanke M-V (2015) Integration of BpMADS4 on various linkage groups improves the utilization of the rapid cycle breeding system in apple. Plant Biotechnol J 13:246–258

    Article  PubMed  CAS  Google Scholar 

  • Welch AJ, Stipanovic AJ, Maynard CA, Powell WA (2007) The effects of oxalic acid on transgenic Castanea dentata callus tissue expressing oxalate oxidase. Plant Sci 172:488–496

    Article  CAS  Google Scholar 

  • Weng J-K, Li X, Bonawitz ND, Chapple C (2008) Emerging strategies of lignin engineering anddegradation for cellulosic biofuel production. Curr Opin Biotechnol 19:166–172

    Article  PubMed  CAS  Google Scholar 

  • Whitehill JGA, Henderson H, Schwartz M, Skyba O, Yuen MMS, King J, Samuels AL, Mansfield SD, Bohlmann J (2016) Histology and cell wall biochemistry of stone cells in the physical defence of conifers against insects. Plant Cell Environ 39:1646–1661

    Article  PubMed  CAS  Google Scholar 

  • Wilcox PL, Amerson HV, Kuhlman EG, Liu B-H, O’Malley DM, Sederoff RR (1996) Detection of a major gene for resistance to fusiform rust disease in loblolly pine by genomic mapping. Proc Natl Acad Sci U S A 93:3859–3864

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wilkerson CG, Mansfield SD, Lu F, Withers S, Park J-Y, Karlen SD, Gonzales-Vigil E, Padmakshan D, Unda F, Rencoret J, Ralph J (2014) Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone. Science 344:90–93

    Article  PubMed  CAS  Google Scholar 

  • Willats WGT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9–27

    Article  PubMed  CAS  Google Scholar 

  • Withers S, Lu F, Kim H, Zhu Y, Ralph J, Wilkerson CG (2012) Identification of grass-specific enzyme that acylates monolignols with p-coumarate. J Biol Chem 287:8347–8355

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xia E-H, Zhang H-B, Sheng J, Li K, Zhang Q-J, Kim C, Zhang Y, Liu Y, Zhu T, Li W, Huang H, Tong Y, Nan H, Shi C, Shi C, Jiang J-J, Mao S-Y, Jiao J-J, Zhang D, Zhao Y, Zhao Y-J, Zhang L-P, Liu Y-L, Liu B-Y, Yu Y, Shao S-F, Ni D-J, Eichler EE, Gao L-Z (2017) The tea tree genome provides insights into tea flavor and independent evolution of caffeine biosynthesis. Mol Plant 10:866–877

    Article  PubMed  CAS  Google Scholar 

  • Xiang D-j, Hu X-y, Zhang Y, Yin K-d (2008) Over-expression of ICE1 gene in transgenic rice improves cold tolerance. Rice Sci 15:173–178

    Article  Google Scholar 

  • Xiang Z, Sen SK, Roy A, Min D, Savithri D, Jameel H, Chiang V, Chang H-m (2015) Wood characteristics and enzymatic saccharification efficiency of field-grown transgenic black cottonwood with altered lignin content and structure. Cellulose 22:683–693

    Article  CAS  Google Scholar 

  • Xiu Y, Iqbal A, Zhu C, Wu G, Chang Y, Li N, Cao Y, Zhang W, Zeng H, Chen S, Wang H (2016) Improvement and transcriptome analysis of root architecture by overexpression of Fraxinus pennsylvanica DREB2A transcription factor in Robinia pseudoacacia L. ‘Idaho’. Plant Biotechnol J 14:1456–1469

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu Q, Chen L-L, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao W-B, Hao B-H, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang J-W, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas KM, Zeng W, Guo F, Cao H, Yang X, Xu X-W, Cheng Y-J, Xu J, Liu J-H, Luo OJ, Tang Z, Guo W-W, Kuang H, Zhang H-Y, Roose ML, Nagarajan N, Deng X-X, Ruan Y (2013) The draft genome of seet orange (Citrus sinensis). Nat Genet 45:59–66

    Article  PubMed  CAS  Google Scholar 

  • Yamagishi N, Kishigami R, Yoshikawa N (2014) Reduced generation time of apple seedlings to within a year by means of a plant virus vector: a new plant-breeding technique with no transmission of genetic modification to the next generation. Plant Biotechnol J 12:60–68

    Article  PubMed  CAS  Google Scholar 

  • Yamagishi N, Li C, Yoshikawa N (2016) Promotion of flowering by apple latent spherical virus vector and virus elimination at high temperature allow accelerated breeding of apple and pear. Front Plant Sci 7:171

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (1993) Characterization of the expression of a desiccation-responsive rd29 gene of Arabidopsis thaliana and analysis of its promoter in transgenic plants. Mol Gen Genet 236:331–340

    Article  PubMed  CAS  Google Scholar 

  • Yang A, Dai X, Zhang W-H (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang F, Mitra P, Zhang L, Prak L, Verhertbruggen Y, Kim J-S, Sun L, Zheng K, Tang K, Auer M, Scheller HV, Loqué D (2013) Engineering secondary cell wall deposition in plants. Plant Biotechnol J 11:325–335

    Article  PubMed  CAS  Google Scholar 

  • Yang J, Yao P, Li Y, Mo J, Wang J, Kang X (2016) Induction of 2n pollen with colchicine during microsporogenesis in Eucalyptus. Euphytica 210:69–78

    Article  CAS  Google Scholar 

  • Yang ZN, Ingelbrecht IL, Louzada E, Skaria M, Mirkov TE (2000) Agrobacterium-mediated transformation of the commercially important grapefruit cultivar Rio red (Citrus paradisi Macf.). Plant Cell Rep 19:1203–1211

    Article  CAS  Google Scholar 

  • Yu L, Chen H, Sun J, Li L (2014) PtrKOR1 is required for secondary cell wall cellulose biosynthesis in Populus. Tree Physiol 34:1289–1300

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Sun J, Li L (2013) PtrCel9A6, an endo-1, 4-β-glucanase, is required for cell wall formation during xylem differentiation in Populus. Mol Plant 6:1904–1917

    Article  PubMed  CAS  Google Scholar 

  • Zelasco S, Reggi S, Calligari P, Balestrazzi A, Bongiorni C, Quattrini E, Delia G, Bisoffi S, Fogher C, Confalonieri M (2006) Expression of the Vitreoscilla hemoglobin (VHb)-encoding gene in transgenic white poplar: plant growth and biomass production, biochemical characterization and cell survival under submergence, oxidative and nitrosative stress conditions. Mol Breed 17:201–216

    Article  CAS  Google Scholar 

  • Zelasco S, Ressegotti V, Confaloniere M, Carbonera D, Calligari P, Bonadei M, Bisoffi S, Yamada K, Balestrazzi A (2007) Evaluation of MAT-vector system in white poplar (Populus alba L.) and production of ipt marker-free transgenic plants by ‘single-step transformation. Plant Cell Tissue Organ Cult 91:61–72

    Article  CAS  Google Scholar 

  • Zeng F, Qian J, Luo W, Zhan Y, Xin Y, Yang C (2010) Stability of transgenes in long-term micropropagation of plants of transgenic birch (Betula platyphylla). Biotechnol Lett 32:151–156

    Article  PubMed  CAS  Google Scholar 

  • Zeng F, Xin Y, Li B, Zhan Y, Yang C (2011) The stability of transgene expression and effect of DNA methylation on post transcriptional gene silencing (PTGS) in birch. Afr J Biotechnol 10:8188–8193

    Article  CAS  Google Scholar 

  • Zeng F, Zhan Y, Nan N, Xin Y, Qi F, Yang C (2009) Expression of bgt gene in transgenic birch (Betula platyphylla Suk.). Afr J Biotechnol 8:3392–3398

    CAS  Google Scholar 

  • Zetsche B, Gootenberg JS, Abudayyeh OO, Slaymaker IM, Makarova KS, Essletzbichler P, Volz SE, Joung J, van der Oost J, Regev A, Koonin EV, Zhang F (2015) Cpf1 is a single RNA-guided endonuclease of a class 2 CRISPR-Cas system. Cell 163:759–771

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhai M, Sun Y, Jia C, Peng S, Liu Z, Yang G (2016) Over-expression of JrsHSP17.3 gene from Juglans regia confer the tolerance to abnormal temperature and NaCl stresses. J Plant Biol 59:549–558

    Article  CAS  Google Scholar 

  • Zhang B, Oakes AD, Newhouse AE, Baier KM, Maynard CA, Powell WA (2013) A threshold level of oxalate oxidase transgene expression reduces Cryphonectria parasitica-induced necrosis in a transgenic American chestnut (Castanea dentata) leaf bioassay. Transgenic Res 22:973–982

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang C, Norris-Caneda KH, Rottmann WH, Gulledge JE, Chang S, Kwan BY-H, Thomas AM, Mandel LC, Kothera RT, Victor AD, Pearson L, Hinchee MAW (2012a) Control of pollen-mediated gene flow in transgenic trees. Plant Physiol 159:1319–1334

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang H, Harry DE, Ma C, Yuceer C, Hsu C-Y, Vikram V, Shevchenko O, Etherington E, Strauss SH (2010) Precocious flowering in trees: the FLOWERING LOCUS T gene as a research and breeding tool in Populus. J Exp Bot 61:2549–2560

    Article  PubMed  CAS  Google Scholar 

  • Zhang R-X, Qin L-J, Zhao D-G (2017) Overexpression of the OsIMP gene increases the accumulation of inositol and confers enhanced cold tolerance in tobacco through modulation of the antioxidant enzymes' activities. Genes 8:179

    Article  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Clemens A, Maximova SN, Guiltinan MJ (2014) The Theobroma cacao B3 domain transcription factor TcLEC2 plays a duel role in control of embryo development and maturation. BMC Plant Biol 14:106

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Wang Y, Wang C (2012b) Gene overexpression and gene silencing in birch using an Agrobacterium-mediated transient expression system. Mol Biol Rep 39:5537–5541

    Article  PubMed  CAS  Google Scholar 

  • Zheng L, Liu G, Meng X, Li Y, Wang Y (2012) A versatile Agrobacterium-mediated transient gene expression system for herbaceous plants and trees. Biochem Genet 50:761–769

    Article  PubMed  CAS  Google Scholar 

  • Zhou X, Jacobs TB, Xue L-J, Harding SA, Tsai C-J (2015) Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate: CoA ligase specificity and redundancy. New Phytol 208:298–301

    Article  PubMed  CAS  Google Scholar 

  • Zhu S-P, Wang J, Ye J-l, Zhu A-D, Guo W-w, Deng X-x (2014) Isolation and characterization of LEAFY COTYLEDON 1-LIKE gene related to embryogenic competence in Citrus sinensis. Plant Cell Tissue Organ Cult 119:1–13

    Article  CAS  Google Scholar 

  • Zhuo R, Qiao G, Sun Z (2007) Transgene expression in Chinese sweetgum driven by the salt induced expressed promoter. Plant Cell Tissue Organ Cult 88:101–107

    Article  CAS  Google Scholar 

  • Zuo J, Niu Q-W, Frugis G, Chua N-H (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

The authors are grateful for the contributions from Professor Ronald Sederoff and Professor Vincent Chiang of Department of Forestry and Environmental Resources, North Carolina State University.

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Correspondence to Todd J. Jones.

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Chang, S., Mahon, E.L., MacKay, H.A. et al. Genetic engineering of trees: progress and new horizons. In Vitro Cell.Dev.Biol.-Plant 54, 341–376 (2018). https://doi.org/10.1007/s11627-018-9914-1

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  • DOI: https://doi.org/10.1007/s11627-018-9914-1

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