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Forest Health and Biotechnology: Possibilities and Considerations (2019)

Chapter: Appendix C: Biotech Tree Research and Development, 19872018

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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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Suggested Citation:"Appendix C: Biotech Tree Research and Development, 19872018." National Academies of Sciences, Engineering, and Medicine. 2019. Forest Health and Biotechnology: Possibilities and Considerations. Washington, DC: The National Academies Press. doi: 10.17226/25221.
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  Appendix C Prepublication Copy Biotech Tree Research and Development, 1987–2018 Targeted Common Insect/Fungus/Pest/ Common Name/ Biotech Genes/ Country of Species Name Hybrid of? Other Trait Taxonomy Approach Other Final Outcome Report Reference Poplars Populus Chinese Clostera anachoreta Moth Transformation Cry1Ac Resistance in field trial China Ren et al., 2018 tomentosa white poplar Lymantria dispar Gypsy moth Transformation Resistance in field trial China Ren et al., 2018 Populus sp. 741 clone Populus alba L. × Lepidopterans Transformation Cry1Ac, Cry3A, Resistance China Zuo et al., 2018 hybrid Poplar (P. davidiana Dode nptII + P. simonii Carr.) × P. tomentosa Carr. Populus sp. Hybrid P. alba × P. Melampsora aecidiodes Leaf rust fungus Transformation AtGolS3 Repressed resistance to Canada La Mantia et al., 2018 poplar grandidentata (A. thaliana) leaf rust & enhanced ROS tolerance Populus sp. Hybrid P. alba × Melampsora aecidiodes Leaf rust fungus Transformation CsRFS Repressed resistance to Canada La Mantia et al., 2018 poplar P. grandidentata (Cucumber leaf rust & enhanced sativus) ROS tolerance Populus sp. 84K poplar P. alba × Drought tolerance Transformation PeCHYR1 Increased WUE and China He et al., 2018 P. glandulosa (from P. drought tolerance euphratica) Salix mongolica Transformation— GUS Proof of concept China Guan et al., 2018 proof of concept transformation Populus sp. Haploid P. simonii × Early flowering Transformation with AP1 (Apetala Early flowering China Yang et al., 2018 poplar P. nigra gene from Salix 1) transgenics integra Populus Poplar Melampsora sp. Leaf rust fungus Transformation PtrWRKY18 & resistance to China Jiang et al., 2017 tomentosa PtrWRKY35 Melampsora fungus Populus sp. Hybrid P. alba × Mechanism of lignin CRISPR/Cas9 4CL1, 4CL2 Downregulation of USA Zhou et al., 2015 hybrid poplar P. tremula biosynthesis genes through CRISPR 717 clone mutagenesis Populus Poplar gGene knockout CRISPR/Cas9 PtoPDS Gene knocked out China Fan et al., 2015 tomentosa (Continued) 185  

  Continued 186 Common Insect/Fungus/Pest/ Common Name/ Biotech Targeted Genes/ Country of Species Name Hybrid of? Other Trait Taxonomy Approach Other Final Outcome Report Reference Poplars Populus sp. Hybrid P. alba × Enhanced wood production Transformation with Gibberellin 20- Enhanced wood Republic of Park et al., 2015 poplar P. tremula var gene from Pinus oxidase 1 production with Korea, glandulosa densiflora gelatinous wood fibers Canada Populus sp. Poplars P. tremula × Heavy metal remediation Transformation ScYCF1 Heavy cadmium Republic of Shim et al., 2013 P. alba var glandula tolerance Korea Populus Chinese Alternaria alternata Poplar leaf blight Transformation Bbchit1 & Resistance to both China Huang et al., 2012 tomentosa white LJAMP2 diseases poplar Colletotrichum sp. Anthracnose Transformation Bbchit1 & China Huang et al., 2012 disease LJAMP2 Populus sp. Hybrid P. nigra × Melampsora medusae Leaf rust Transformation ech42 Resistance to leaf rust Canada Noël et al., 2009 poplar P. maximowiczii (endocinitase gene from Trichoderma harzianum) Populus sp. Anoplophora glabripennis Asian Bt886 expression in Cry3Aa Expression of gene China Chen et al., 2005 longhorned E. coli is toxic to the beetle beetle in E. coli Populus sp. Poplars [(Populus Malacosoma disstria, Moths Transformation CpTI (cowpea High resistance to China Zhang et al., 2004 tomentosa × Lymantria dispar, Stilpnotia trypsin inhibitor) moths P. bolleana) × candida P. tomentosa] Populus sp. INRA P. tremula × Chrysomela tremulae Arthropod Transformation Cry3Aa Resistance France Génissel et al., 2003 hybrid 353-38 P. tremuloides Populus sp. Hybrid P. tremula × Chrysomela tremulae Arthropod Transformation Cry3Aa Resistance France Génissel et al., 2003 poplar P. tremuloides Populus sp. Hybrid Populus × Septoria musiva Leaf spot disease Transformation OxO Resistance to Septoria USA Liang et al., 2001 poplar Ogy P. euamericana Populus sp. Hybrid P. deltoides × Lymantria dispar Gypsy moth Transformation AaIT (scorpion Resistance to China Wu et al., 2000 poplar P. simonii neurotoxin) gypsy moth N-106 Chestnut Castanea American with Chinese Cryphonectria parasitica Chestnut blight Transformation Oxalate oxidase Resistance against USA Newhouse et al., 2014 dentata chestnut chestnut fungus (wheat) chestnut blight fungus Castanea American Cryphonectria parasitica Chestnut blight Transformation— gfp, bar, OxO Transformation— USA Polin et al., 2006 Prepublication Copy dentata chestnut fungus proof of concept proof of concept Castanea sativa European Transformation— nptII, uidA Transformation— Spain Corredoira et al., 2004 chestnut proof of concept proof of concept  

  Eucalypts Prepublication Copy Eucalyptus sp. Realized pollen flow GM eucalypt No pollen flow Brazil da Silva et al., 2017 assessment beyond 240 m in a stand that was established in 2009 Eucalyptus sp. E. urophylla × Ralstonia solanacearum Bacterial wilt, Transformation aiiA Bacterial wilt resistance China Ouyang and Li, 2016 E. grandis fungal infection, gray mold Eucalyptus Salt tolerance Transformation codA Salt tolerance and no adverse Japan Oguchi et al., 2014 globulus effect on soil microbial communities in a 4-year trial Mangrin Increase salt tolerance Japan, Yu et al., 2013 Pakistan Eucalyptus Red river Salt tolerance codA family Increase salt tolerance Japan Kikuchi et al., 2009 camaldulensis gum Eucalyptus sp. E. urophylla × Frost tolerance Transformation CBF2 (A. Increase freeze tolerance USA Hinchee et al., 2009 E. grandis thaliana) Ash Fraxinus Green ash Proof-of-concept transformation Transformation nptII, GUS USA Du and Pijut, 2009 pennsylvanica Birch Betula Birch Salt/drought tolerance Transformation BpSPL9 Improved ROS scavenging China Ning et al., 2017 platyphylla leading to better salt/drought tolerance in transgenic lines Betula Birch Salt tolerance Transformation BplMYB46 Overexpression induces China Guo et al., 2016 platyphylla improved ROS scavenging Betula Birch Lymantria dispar Gypsy moth Transformation bgt Resistance to gypsy moth China Zeng et al., 2009 platyphylla Betula pendula Silver birch Pyrenopeziza betulicola Fuckel leaf spot Transformation Chitinase 4 Resistance to leaf Finland Pappinen et al. 2002 disease (sugar beet) spot disease Spruce Picea glauca White Choristoneura fumiferana Spruce budworm Transformation PBgGlu1 Resistance to budworm Canada Mageroy et al., 2017 spruce Picea abies Norway Heterobasidion annosum Annosum root Transformation PaNACO3 Resistance to fungus Sweden Dalman et al., 2017 spruce rot Picea abies Norway Cyratocystis polonica Bark beetle Transformation Flavan-3-ols, Resistance to fungus Canada Hammerbacher et al., spruce co-invading LAR 2014 fungus (Continued) 187  

  Continued 188 Common Insect/Fungus/Pest/ Common Name/ Biotech Targeted Genes/ Country of Species Name Hybrid of? Other Trait Taxonomy Approach Other Final Outcome Report Reference Spruce Picea glauca White Somatic CHAP3A & WUS Canada Klimaszewska et al., spruce embryogenesis 2010 Picea mariana Black Cylindrocladium floridanum Root pathogen Transformation ech42 Resistance to root Canada Noël et al., 2009 spruce (endocinitase gene disease from Trichoderma harzianum) Picea glauca White Functional characterization: Post-transformation CAD Validation of CAD Canada, Bedon et al., 2009 spruce CAD analysis transformation France Picea glauca White Choristoneura fumiferana Spruce budworm Transformation Cry1AB Resistant to spruce Canada Lachance et al., 2007 spruce budworm Picea glauca White Transformation to test nptII, CryIA, uidA Rhizosphere Canada LeBlanc et al., 2007 spruce effect on rhizosphere communities communities significantly affected by transgenes Picea glauca White Transformation proof nptII, uidA Canada Le et al., 2001 spruce of concept Picea abies Norway Particle bombardment bar Resistant to Basta Sweden Brukhin et al., 2000 spruce herbicide Picea mariana Black Particle bombardment nptII, GUS Proof-of-concept Canada Charest et al,, 1996 spruce transformation Douglas Fir Pseudotsuga Douglas fir Proof of concept Transformation Kanamycin Proof-of-concept USA Dandekar et al., 1987 menziesii resistance transformation Pseudotsuga Douglas fir Proof of concept Particle bombardment GUS Proof of concept USA Goldfarb et al., 1991 menziesii Larch Larix sp. Larch L. kaempferi × Proof of concept Transformation Kanamycin Proof-of-concept France, Levée et al., 1997 L. decidua resistance transformation Canada Larix decidua European Proof of concept Transformation Proof-of-concept USA Huang et al., 1991 larch transformation Pines Pinus Masson Transformation—proof CslA2 Proof-of-concept China Maleki et al., 2018 massoniana pine of concept transformation Prepublication Copy Pinus elliottii Hybrid pine P. elliottii var. Somatic Proof of concept Portugal Nunes et al., 2018 elliottii × embryogenesis P. caribaea var. hondurensis  

  Pinus pinea Stone pine Transformation—proof GUS Proof-of-concept Spain, Blasco et al., 2016 Prepublication Copy of concept transformation Ecuador Pinus radiata Radiata Transformation of nptII, GUS Proof-of-concept New Grant et al., 2015 pine micropropagated shoots transformation Zealand Pinus Japanese Somatic embryogenesis Proof of concept Japan Maruyama and Hosoi, thunbergii black pine 2016 PInus radiata Radiata Syringil lignin production Transformation F5H, COMT Syringil lignin USA, New Wagner et al., 2015 pine production in conifers Zealand Pinus elliottii Slash pine Transformation—proof hpt, uidA Proof-of-concept China Tang et al., 2014 of concept transformation Pinus radiata Radiata Lignin composition changes RNAi suppression and CCoA Changes to cell wall New Wagner et al., 2013 pine transformation reductase composition Zealand, USA, Belgium Pinus radiata Radiata Lignin reduction Transformation PrCCoAOMT Modification of lignin New Wagner et al., 2011 pine composition Zealand Pinus radiata Radiata Transformation—proof nptII, uidA, bar Proof-of-concept New Charity et al., 2005 pine of concept transformation Zealand Pinus radiata Radiata Gene silencing Transformation CAD Silencing of CAD New Wagner et al., 2005 pine gene Zealand, Australia Pinus taeda Loblolly Dendrolimus punctatus & Moth pests of Transformation Cry1Ac Resistance to moth USA Tang and Tian, 2003 pine Cryphothelea formisicola pines pests Pinus strobus Eastern Proof of concept Transformation GUS Proof-of-concept Canada Levée et al., 1999 white pine transformation Elm Ulmus American Ophiostoma novoulmi Dutch elm Transformation ESF39A Resistance to Dutch USA Newhouse et al., 2007 americana elm disease elm disease Ulmus procera English elm Ophiostoma novoulmi Dutch elm Transformation—proof nptII, uidA Proof-of-concept USA Gartland et al., 2000 disease of concept transformation Apple Malus × Apple Dwarf phenotype Transformation MdNAC1 Overexpression results China Jia et al., 2018 domestica in dwarf phenotype Malus × Apple Stress tolerance Transformation MdATG18a Tolerance to drought China, USA Sun et al., 2018 domestica stress Malus × Apple Stress tolerance Transformation MdcyMDH Tolerance to cold and China Wang et al., 2016 domestica salt stresses Malus × Apple Venturia inaequalis Scab Transformation Puroindoline-B Reduction in scab France Faize et al., 2004 domestica (pinB) susceptibility Malus × Apple Early flowering Transformation MdTFL Early onset of Japan Kotoda et al., 2002 domestica flowering (15 months) (Continued) 189  

  Continued 190 Targeted Common Insect/Fungus/Pest/ Common Name/ Biotech Genes/ Country of Species Name Hybrid of? Other Trait Taxonomy Approach Other Final Outcome Report Reference Cherry Prunus avium Cherry Proof-of-concept regeneration Transformation gusA, vcFT Shoot regeneration/proof of USA, China, Zong et al., 2018 concept Egypt Prunus sp. Black Flowering control & insect Bark beetles Transformation PH3, MDL4, Early flowering and pest USA Wang and Pijut, 2014 cherry resistance PsTFL1 resistance Prunus sp. Cherry Gisela 6 and Glsela Proof of concept Necrotic ring Transformation RNAi Resistance to Prunus USA Song et al., 2013 7 spot virus necrotic ringspot virus Prunus serotina Black Proof of concept Transformation Agamous Proof-of-concept USA Liu and Pijut, 2010 cherry transformation Prunus cerasus Cherry P. cerasus × Proof of concept Transformation nptII, gusA Proof-of-concept USA Song and Sink, 2006 & hybrid P. canescens transformation Prunus sp. Cherry P. avium × Proof of concept Somatic Proof of concept Italy Gutièrrez-Pesce and P. pseudocerasus embryogenesis Rugini, 2004 Prunus sp. Cherry P. avium × Proof of concept Transformation Proof of concept Italy, USA Gutièrrez-Pesce et al., P. pseudocerasus 1998 Peach Prunus persica Peach Proof of concept Transformation GUS, GFP Proof of concept USA, Padilla et al., 2006 transformation Poland, Italy, Spain Prunus persica Peach Proof-of-concept regeneration Transformation and nptII, sGFP Regeneration of Spain Pérez-Clemente et al., regeneration transformed plants 2005 Papaya Carica papaya Papaya Ring spot virus Transformation Coat protein Resistance to PRSV China, Bau et al., 2003 gene CP Taiwan Carica papaya Papaya Ring spot virus RNAi particle Coat protein Resistance to PRSV China, Jia et al., 2017 bombardment gene CP Taiwan Walnut Juglans regia Persian Transformation fld Increased tolerance to Iran Sheikh Beig Goharrizi walnut osmotic stress et al., 2016 Juglans regia Walnut Transformation nptII, uidA Proof-of-concept USA Walawage et al., 2014 transformation Juglans sp. Walnut J. hindsii × Transformation rolABC Induce rooting in hybrids USA Vahdati et al., 2002 J. regia Prepublication Copy Juglans regia Walnut Cydia pomonella Codling moth Bt transformation CryIIA(c) Resistance to insects USA Dandekar et al., 1998 Juglans regia Walnut Proof of concept Transformation and APHII Transformation and USA McGranahan et al., regeneration regeneration of plants 1988  

  Plum Prepublication Copy Prunus sp. Plum (P. pumila × Plum pox virus (PPV) Plum pox virus RNAi PPV-CV Resistance to PPV Russia Sidorova et al., 2018 P. salicina) × P. cerasifera Prunus sp. Plum Plum pox virus (PPV) Transformation PPV-CV Resistance to PPV France, Scorza et al., 1994 USA Avocado Persea Avocado Proof of concept Transformation gfp, DsRed, gfp- Proof-of-concept Spain Palomo-Rios et al., americana gus transformation and plant 2017 recovery Black Locust Robinia Black locust Proof of concept Transformation Kanamycin- Proof-of-concept USA Han et al., 1993 pseudoacacia resistant gene transformation Robinia Black locust Herbicide tolerance Transformation bar, gusA Herbicide tolerance Spain Zaragoza et al., 2004 pseudoacacia with sonication Robinia Black locust Proof of concept Transformation GUS Proof-of-concept Japan Igasaki et al., 2000 pseudoacacia transformation Robinia Black locust Proof of concept Transformation nptII, GUS Proof-of-concept India Kanwar et al., 2003 pseudoacacia transformation Citrus Citrus sp. Citrus (C. sinensis & Proof of concept Transformation nptII, GUS Proof of concept Brazil, USA de Oliveira et al., 2009 C. paradisi) × Poncirus trifoliata Citrus jambhiri Rough Proof of concept Transformation nptII & cat Proof of concept Israel Vardi et al., 1990 lemon (protoplasts) Citrus sinensis Citrus Disease resistance Xanthomonas Transformation hrpN Resistance to citrus canker Brazil, USA Barbosa-Mendes et al., axonopodis 2009 Sweetgum Liquidambar Proof of concept Transformation Kanamycin & Proof of concept USA Sullivan and styraciflua GUS Lagrimini, 1993 Liquidambar Chinese Stress tolerance Transformation AtNHXI Tolerance to salt stress China Qiao et al., 2010 formosana sweetgum Liquidambar Hybrid L. styraciflua × Phytoremediation Transformation ECS & merA Mercury phytoremediation USA Dai et al., 2009 sp. Sweetgum L. formosana Liquidambar Insect resistance Lymantria dispar Transformation Tobacco anionic Gypsy moth resistance USA Dowd et al., 1998 styraciflua peroxidase Liquidambar Chinese Stress tolerance Transformation SOD & POD Tolerance to salt, drought, China Renying et al., 2007 formosana sweetgum and cold (Continued) 191  

  Continued 192 Common Insect/Fungus/Pest/ Common Name/ Biotech Targeted Genes/ Country of Species Name Hybrid of? Other Trait Taxonomy Approach Other Final Outcome Report Reference Cocoa Theobroma Cocoa Proof of concept Transformation Kanamycin & Proof of concept USA, Ghana Sain et al., 1994 cocoa nptII Theobroma Cocoa Proof of concept Transformation uidA Proof of concept Brazil Silva et al., 2009 cocoa Theobroma Cocoa Proof of concept Transformation Chi, nptII, & Proof of concept USA Maximova et al., 2003 cocoa EGFP Theobroma Cocoa Fungal resistance Colletotrichum Transformation TcChi1 Resistance to USA Maximova et al., 2006 cocoa gloeosporoides Colletotrichum Theobroma Cocoa Proof of concept Somatic Proof of concept Colombia Ramírez et al., 2018 cocoa embryogenesis Theobroma Cocoa Proof of concept Transformation GFP Proof of concept USA Fister et al., 2016 cocoa Prepublication Copy  

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Appendix C Lachance, D., L.P. Hamel, F. Pelletier, J. Valéro, M. Bernier-Cardou, K. Chapman, K. Van Frankenhuyzen, and A. Séguin. 2007. Expression of a Bacillus thuringiensis cry1Ab gene in transgenic white spruce and its efficacy against the spruce budworm (Choristoneura fumiferana). Tree Genetics & Genomes 3(2):153–167. Le, V.Q., J. Belles Isles, M. Dusabenyagasani, and F.M. Tremblay. 2001. An improved procedure for production of white spruce (Picea glauca) transgenic plants using Agrobacterium tumefaciens. Journal of Experimental Botany 52(364):2089–2095. LeBlanc, P.M., R.C. Hamelin, and M. Filion. 2007. Alteration of soil rhizosphere communities following genetic transformation of white spruce. Applied and Environmental Microbiology 73(13):4128–4134. Levée, V., M.A. Lelu, L. Jouanin, D. Cornu, and G. Pilate. 1997. Agrobacterium tumefaciens-mediated transformation of hybrid larch (Larix kaempferi × L. decidua) and transgenic plant regeneration. Plant Cell Reports 16(10):680– 685. 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Forest Health and Biotechnology: Possibilities and Considerations Palomo-Ríos, E., S. Cerezo, J.A. Mercado, and F. Pliego-Alfaro. 2017. Agrobacterium-mediated transformation of avocado (Persea americana Mill.) somatic embryos with fluorescent marker genes and optimization of trans- genic plant recovery. Plant Cell, Tissue and Organ Culture 128(2):447–455. Pappinen, A., Y. Degefu, L. Syrjälä, K. Keinonen, and K. von Weissenberg. 2002. Transgenic silver birch (Betula pendula) expressing sugarbeet chitinase 4 shows enhanced resistance to Pyrenopeziza betulicola. Plant Cell Reports 20(11):1046–1051. Park, E.J., H.T. Kim, Y.I. Choi, C. Lee, V.P. Nguyen, H.W. Jeon, J.S. Cho, R. Funada, R.P. Pharis, L.V. Kurepin, and J.H. Ko. 2015. Overexpression of gibberellin 20-oxidase1 from Pinus densiflora results in enhanced wood for- mation with gelatinous fiber development in a transgenic hybrid poplar. Tree Physiology 35(11):1264–1277. Pérez-Clemente, R.M., A. Pérez-Sanjuán, L. García-Férriz, J.P. 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Appendix C Tang, W., B. Xiao, and Y. Fei. 2014. Slash pine genetic transformation through embryo cocultivation with A. tumefaciens and transgenic plant regeneration. In Vitro Cellular & Developmental Biology-Plant 50(2):199–209. Vahdati, K., J.R. MeKenna, A.M. Dandekar, C.A. Leslie, S.L. Uratsu, W.P. Hackett, P. Negri, and G.H. McGranahan. 2002. Rooting and other characteristics of a transgenic walnut hybrid (Juglans hindsii × J. regia) rootstock expressing rolABC. Journal of the American Horticultural Society 127(5):724–728. Vardi, A., S. Bleichman, and D. Aviv. 1990. Genetic transformation of Citrus protoplasts and regeneration of trans- genic plants. Plant Science 69(2):199–206. Wagner, A., L. Phillips, R.D. Narayan, J.M. Moody, and B. Geddes. 2005. Gene silencing studies in the gymnosperm species Pinus radiata. Plant Cell Reports 24(2):95–102. Wagner, A., Y. Tobimatsu, L. Phillips, H. Flint, K. Torr, L. Donaldson, L. Pears, and J. Ralph. 2011. CCoAOMT suppression modifies lignin composition in Pinus radiata. Plant Journal 67(1):119–129. Wagner, A., Y. Tobimatsu, G. Goeminne, L. Phillips, H. Flint, D. Steward, K. Torr, L. Donaldson, W. Boerjan, and J. Ralph. 2013. Suppression of CCR impacts metabolite profile and cell wall composition in Pinus radiata tracheary elements. Plant Molecular Biology 81(1–2):105–117. Wagner, A., Y. Tobimatsu, L. Phillips, H. Flint, B., Geddes, F. Lu, and J. Ralph. 2015. Syringyl lignin production in conifers: Proof of concept in a Pine tracheary element system. Proceedings of the National Academy of Sciences of the United States of America 12(19):6218–6223. Walawage, S.L., C.A. Leslie, M.A. Escobar, and A.M. Dandekar. 2014. Agrobacterium tumefaciens-mediated trans- formation of walnut (Juglans regia). Plant Physiology 4(19):e1258. Wang, Q.J., H. Sun, Q.L. Dong, T.Y. Sun, Z.X. Jin, Y.J. Hao, and Y.X. Yao. 2016. The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydro- genase gene in transgenic apple plants. Plant Biotechnology Journal 14(10):1986–1997. Wang, Y., and P.M. Pijut. 2014. Agrobacterium-mediated transformation of black cherry for flowering control and insect resistance. Plant Cell, Tissue and Organ Culture 119(1):107–116. Wu, N.F., Q. Sun, B. Yao, Y.L. Fan, H.Y. Rao, M.R. Huang, and M.X. Wang. 2000. Insect-resistant transgenic poplar expressing AaIT gene. Chinese Journal of Biotechnology 16(2):129–133. Yang, J., K. Li, C. Li, J. Li, B. Zhao, W. Zheng, Y. Gao, and C. Li. 2018. In vitro anther culture and Agrobacterium- mediated transformation of the AP1 gene from Salix integra Linn. in haploid poplar (Populus simonii × P. nigra). Journal of Forestry Research 29(2):321–330. Yu, X., A. Kikuchi, T. Shimazaki, A. Yamada, Y. Ozeki, E. Matsunaga, H. Ebinuma, and K.N. Watanabe. 2013. Assessment of the salt tolerance and environmental biosafety of Eucalyptus camaldulensis harboring a mangrin transgene. Journal of Plant Research 126(1):141–150. Zaragoza, C., J. Munoz-Bertomeu, and I. Arrillaga. 2004. Regeneration of herbicide-tolerant black locust transgenic plants by SAAT. Plant Cell Reports 22(11):832–838. Zeng, F., Y. Zhan, N. Nan, Y. Xin, F. Qi, and C. Yang. 2009. Expression of bgt gene in transgenic birch (Betula platyphylla Suk.). African Journal of Biotechnology 8(15):3392–3398. Zhang, Q., S. Lin, Y. Lin, Z. Zhang, H. Liu, Y. Zou, and Z. Wang. 2004. Identification of CpTI gene integration for 2-year-old transgenic poplars at DNA level. Forestry Studies in China 6(3):15–19. Zhou, X., T.B. Jacobs, L.J. Xue, S.A. Harding, and C.J. Tsai. 2015. Exploiting SNP s for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4 coumarate: CoA ligase specificity and redundancy. New Phytologist 208(2):298–301. Zong, X., Q. Chen, M.A. Nagaty, Y. Kang, G. Lang, and G.Q. Song. 2018. Adventitious shoot regeneration and Agrobacterium tumefaciens-mediated transformation of leaf explants of sweet cherry (Prunus avium L.). Journal of Horticultural Science and Biotechnology: 1–8. Zuo, L., R. Yang, Z. Zhen, J. Liu, L. Huang, and M. Yang. 2018. A 5-year field study showed no apparent effect of the Bt transgenic 741 poplar on the arthropod community and soil bacterial diversity. Scientific Reports 8(1):1956. Prepublication Copy 197 

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The American chestnut, whitebark pine, and several species of ash in the eastern United States are just a few of the North American tree species that have been functionally lost or are in jeopardy of being lost due to outbreaks of pathogens and insect pests. New pressures in this century are putting even more trees at risk. Expanded human mobility and global trade are providing pathways for the introduction of nonnative pests for which native tree species may lack resistance. At the same time, climate change is extending the geographic range of both native and nonnative pest species.

Biotechnology has the potential to help mitigate threats to North American forests from insects and pathogens through the introduction of pest-resistant traits to forest trees. However, challenges remain: the genetic mechanisms that underlie trees’ resistance to pests are poorly understood; the complexity of tree genomes makes incorporating genetic changes a slow and difficult task; and there is a lack of information on the effects of releasing new genotypes into the environment.

Forest Health and Biotechnology examines the potential use of biotechnology for mitigating threats to forest tree health and identifies the ecological, economic, and social implications of deploying biotechnology in forests. This report also develops a research agenda to address knowledge gaps about the application of the technology.

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