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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.

Appendix C

Biotech Tree Research and Development, 1987–2018

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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.

Species	Common Name	Hybrid of?	Insect/Fungus/Pest/Other Trait	Common Name/Taxonomy	Biotech Approach	Targeted Genes/Other	Final Outcome	Country of Report	Reference
Poplars
Populus tomentosa	Chinese white poplar		Clostera anachoreta	Moth	Transformation	Cry1Ac	Resistance in field trial	China	Ren et al., 2018
			Lymantria dispar	Gypsy moth	Transformation		Resistance in field trial	China	Ren et al., 2018
Populus sp. hybrid	741 clone poplar	Populus alba L. × (P. davidiana Dode + P. simonii Carr.) × P. tomentosa Carr.		Lepidopterans	Transformation	Cry1Ac, Cry3A, nptII	Resistance	China	Zuo et al., 2018
Populus sp.	Hybrid poplar	P. alba × P. grandidentata	Melampsora aecidiodes	Leaf rust fungus	Transformation	AtGolS3 (A. thaliana)	Repressed resistance to leaf rust and enhanced ROS tolerance	Canada	La Mantia et al., 2018
Populus sp.	Hybrid poplar	P. alba × P. grandidentata	Melampsora aecidiodes	Leaf rust fungus	Transformation	CsRFS (Cucumber sativus)	Repressed resistance to leaf rust and enhanced ROS tolerance	Canada	La Mantia et al., 2018
Populus sp.	84K poplar	P. alba × P. glandulosa	Drought tolerance		Transformation	PeCHYR1 (from P. euphratica)	Increased WUE and drought tolerance	China	He et al., 2018
Salix mongolica					Transformation—proof of concept	GUS	Proof-of-concept transformation	China	Guan et al., 2018
Populus sp.	Haploid poplar	P. simonii × P. nigra	Early flowering		Transformation with gene from Salix integra	AP1 (Apetala 1)	Early flowering transgenics	China	Yang et al., 2018
Populus tomentosa	Poplar		Melampsora sp.	Leaf rust fungus	Transformation	PtrWRKY18 and PtrWRKY35	resistance to Melampsora fungus	China	Jiang et al., 2017

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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.

Populus sp. hybrid	Hybrid poplar	P. alba × P. tremula 717 clone	Mechanism of lignin biosynthesis		CRISPR/Cas9	4CL1, 4CL2	Downregulation of genes through CRISPR mutagenesis	USA	Zhou et al., 2015
Populus tomentosa	Poplar		Gene knockout		CRISPR/Cas9	PtoPDS	Gene knocked out	China	Fan et al., 2015
Populus sp.	Hybrid poplar	P. alba × P. tremula var glandulosa	Enhanced wood production		Transformation with gene from Pinus densiflora	Gibberellin 20-oxidase 1	Enhanced wood production with gelatinous wood fibers	Republic of Korea, Canada	Park et al., 2015
Populus sp.	Poplars	P. tremula × P. alba var glandula	Heavy metal remediation		Transformation	ScYCF1	Heavy cadmium tolerance	Republic of Korea	Shim et al., 2013
Populus tomentosa	Chinese white poplar		Alternaria alternata	Poplar leaf blight	Transformation	Bbchit1 and LJAMP2	Resistance to both diseases	China	Huang et al., 2012
			Colletotrichum sp.	Anthracnose disease	Transformation	Bbchit1 and LJAMP2		China	Huang et al., 2012
Populus sp.	Hybrid poplar	P. nigra × P. maximowiczii	Melampsora medusae	Leaf rust	Transformation	ech42 (endocinitase gene from Trichoderma harzianum)	Resistance to leaf rust	Canada	Noël et al., 2005
Populus sp.			Anoplophora glabripennis	Asian longhorned beetle	Bt886 expression in E. coli	Cry3Aa	Expression of gene is toxic to the beetle in E. coli	China	Chen et al., 2005
Populus sp.	Poplars	[(Populus tomentosa × P. bolleana) × P. tomentosa]	Malacosoma disstria, Lymantria dispar, Stilpnotia candida	Moths	Transformation	CpTI (cowpea trypsin inhibitor)	High resistance to moths	China	Zhang et al., 2004

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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.

Species	Common Name	Hybrid of?	Insect/Fungus/Pest/Other Trait	Common Name/Taxonomy	Biotech Approach	Targeted Genes/Other	Final Outcome	Country of Report	Reference
Populus sp. hybrid	INRA 353-38	P. tremula × P. tremuloides	Chrysomela tremulae	Arthropod	Transformation	Cry3Aa	Resistance	France	Génissel et al., 2003
Populus sp.	Hybrid poplar	P. tremula × P. tremuloides	Chrysomela tremulae	Arthropod	Transformation	Cry3Aa	Resistance	France	Génissel et al., 2003
Populus sp.	Hybrid poplar Ogy	Populus × P. euamericana	Septoria musiva	Leaf spot disease	Transformation	OxO	Resistance to Septoria	USA	Liang et al., 2001
Populus sp.	Hybrid poplar N-106	P. deltoides × P. simonii	Lymantria dispar	Gypsy moth	Transformation	AaIT (scorpion neurotoxin)	Resistance to gypsy moth	China	Wu et al., 2000
Chestnut
Castanea dentata	American chestnut	with Chinese chestnut	Cryphonectria parasitica	Chestnut blight fungus	Transformation	Oxalate oxidase (wheat)	Resistance against chestnut blight fungus	USA	Newhouse et al., 2014
Castanea dentata	American chestnut		Cryphonectria parasitica	Chestnut blight fungus	Transformation—proof of concept	gfp, bar, OxO	Proof-of-concept transformation	USA	Polin et al., 2006
Castanea sativa	European chestnut				Transformation—proof of concept	nptII, uidA	Proof-of-concept transformation	Spain	Corredoira et al., 2004
Eucalypts
Eucalyptus sp.			Realized pollen flow assessment			GM eucalypt	No pollen flow beyond 240 m in a stand that was established in 2009	Brazil	da Silva et al., 2017
Eucalyptus sp.		E. urophylla × E. grandis	Ralstonia solanacearum	Bacterial wilt, fungal infection, gray mold	Transformation	aiiA	Bacterial wilt resistance	China	Ouyang and Li, 2016

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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.

Eucalyptus globulus			Salt tolerance		Transformation	codA	Salt tolerance and no adverse effect on soil microbial communities in a 4-year trial	Japan	Oguchi et al., 2014
						Mangrin	Increase salt tolerance	Japan, Pakistan	Yu et al., 2013
Eucalyptus camaldulensis	Red river gum		Salt tolerance			codA family	Increase salt tolerance	Japan	Kikuchi et al., 2009
Eucalyptus sp.		E. urophylla × E. grandis	Frost tolerance		Transformation	CBF2 (A. thaliana)	Increase freeze tolerance	USA	Hinchee et al., 2009
Ash
Fraxinus pennsylvanica	Green ash		Proof-of-concept transformation		Transformation	nptII, GUS		USA	Du and Pijut, 2009
Birch
Betula platyphylla	Birch		Salt/drought tolerance		Transformation	BpSPL9	Improved ROS scavenging leading to better salt/drought tolerance in transgenic lines	China	Ning et al., 2017
Betula platyphylla	Birch		Salt tolerance		Transformation	BplMYB46	Overexpression induces improved ROS scavenging	China	Guo et al., 2017
Betula platyphylla	Birch		Lymantria dispar	Gypsy moth	Transformation	bgt	Resistance to gypsy moth	China	Zeng et al., 2009
Betula pendula	Silver birch		Pyrenopeziza betulicola	Fuckel leaf spot disease	Transformation	Chitinase 4 (sugar beet)	Resistance to leaf spot disease	Finland	Pappinen et al., 2002
Spruce
Picea glauca	White spruce		Choristoneura fumiferana	Spruce budworm	Transformation	PBgGlu1	Resistance to budworm	Canada	Mageroy et al., 2017
Picea abies	Norway spruce		Heterobasidion annosum	Annosum root rot	Transformation	PaNACO3	Resistance to fungus	Sweden	Dalman et al., 2017

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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.

Species	Common Name	Insect/Fungus/Pest/Other Trait	Common Name/Taxonomy	Biotech Approach	Targeted Genes/Other	Final Outcome	Country of Report	Reference
Picea abies	Norway spruce	Cyratocystis polonica	Bark beetle co-invading fungus	Transformation	Flavan-3-ols, LAR	Resistance to fungus	Canada	Hammerbacher et al., 2014
Picea glauca	White spruce			Somatic embryogenesis	CHAP3A and WUS		Canada	Klimaszewska et al., 2010
Picea mariana	Black spruce	Cylindrocladium floridanum	Root pathogen	Transformation	ech42 (endocinitase gene from Trichoderma harzianum)	Resistance to root disease	Canada	Noël et al., 2005
Picea glauca	White spruce	Functional characterization: CAD		Post-transformation analysis	CAD	Validation of CAD transformation	Canada, France	Bedon et al., 2009
Picea glauca	White spruce	Choristoneura fumiferana	Spruce budworm	Transformation	Cry1AB	Resistant to spruce budworm	Canada	Lachance et al., 2007
Picea glauca	White spruce			Transformation to test effect on rhizosphere communities	nptII, CryIA, uidA	Rhizosphere communities significantly affected by transgenes	Canada	LeBlanc et al., 2007
Picea glauca	White spruce			Transformation–proof of concept	nptII, uidA		Canada	Le et al., 2001
Picea abies	Norway spruce			Particle bombardment	bar	Resistant to Basta herbicide	Sweden	Brukhin et al., 2000
Picea mariana	Black spruce			Particle bombardment	nptII, GUS	Proof-of-concept transformation	Canada	Charest et al., 1996
Douglas Fir
Pseudotsuga menziesii	Douglas fir	Proof of concept		Transformation	Kanamycin resistance	Proof-of-concept transformation	USA	Dandekar et al., 1987

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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.

Pseudotsuga menziesii	Douglas fir		Proof of concept	Particle bombardment	GUS	Proof of concept	USA	Goldfarb et al., 1991
Larch
Larix sp.	Larch	L. kaempferi × L. decidua	Proof of concept	Transformation	Kanamycin resistance	Proof-of-concept transformation	France, Canada	Levée et al., 1997
Larix decidua	European larch		Proof of concept	Transformation		Proof-of-concept transformation	USA	Huang et al., 1991
Pines
Pinus massoniana	Masson pine			Transformation—proof of concept	CslA2	Proof-of-concept transformation	China	Maleki et al., 2018
Pinus elliottii	Hybrid pine	P. elliottii var. elliottii × P. caribaea var. hondurensis		Somatic embryogenesis		Proof of concept	Portugal	Nunes et al., 2018
Pinus pinea	Stone pine			Transformation—proof of concept	GUS	Proof-of-concept transformation	Spain, Ecuador	Blasco et al., 2016
Pinus radiata	Radiata pine			Transformation of micropropagated shoots	nptII, GUS	Proof-of-concept transformation	New Zealand	Grant et al., 2015
Pinus thunbergii	Japanese black pine			Somatic embryogenesis		Proof of concept	Japan	Maruyama and Hosoi, 2016
Pinus radiata	Radiata pine		Syringil lignin production	Transformation	F5H, COMT	Syringil lignin production in conifers	USA, New Zealand	Wagner et al., 2015
Pinus elliottii	Slash pine			Transformation—proof of concept	hpt, uidA	Proof-of-concept transformation	China	Tang et al., 2014
Pinus radiata	Radiata pine		Lignin composition changes	RNAi suppression and transformation	CCoA reductase	Changes to cell wall composition	New Zealand, USA, Belgium	Wagner et al., 2013
Pinus radiata	Radiata pine		Lignin reduction	Transformation	PrCCoAOMT	Modification of lignin composition	New Zealand	Wagner et al., 2011

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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.

Species	Common Name	Insect/Fungus/Pest/Other Trait	Common Name/Taxonomy	Biotech Approach	Targeted Genes/Other	Final Outcome	Country of Report	Reference
Pinus radiata	Radiata pine			Transformation—proof of concept	nptII, uidA, bar	Proof-of-concept transformation	New Zealand	Charity et al., 2005
Pinus radiata	Radiata pine	Gene silencing		Transformation	CAD	Silencing of CAD gene	New Zealand, Australia	Wagner et al., 2005
Pinus taeda	Loblolly pine	Dendrolimus punctatus and Cryphothelea formisicola	Moth pests of pines	Transformation	Cry1Ac	Resistance to moth pests	USA	Tang and Tian, 2003
Pinus strobus	Eastern white pine	Proof of concept		Transformation	GUS	Proof-of-concept transformation	Canada	Levée et al., 1999
Elm
Ulmus americana	American elm	Ophiostoma novoulmi	Dutch elm disease	Transformation	ESF39A	Resistance to Dutch elm disease	USA	Newhouse et al., 2007
Ulmus procera	English elm	Ophiostoma novoulmi	Dutch elm disease	Transformation—proof of concept	nptII, uidA	Proof-of-concept transformation	USA	Gartland et al., 2000
Apple
Malus × domestica	Apple	Dwarf phenotype		Transformation	MdNAC1	Overexpression results in dwarf phenotype	China	Jia et al., 2018
Malus × domestica	Apple	Stress tolerance		Transformation	MdATG18a	Tolerance to drought stress	China, USA	Sun et al., 2018
Malus × domestica	Apple	Stress tolerance		Transformation	MdcyMDH	Tolerance to cold and salt stresses	China	Wang et al., 2016
Malus × domestica	Apple	Venturia inaequalis	Scab	Transformation	Puroindoline-B (pinB)	Reduction in scab susceptibility	France	Faize et al., 2004
Malus × domestica	Apple	Early flowering		Transformation	MdTFL	Early onset of flowering (15 months)	Japan	Kotoda et al., 2002

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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.

Cherry
Prunus avium	Cherry		Proof-of-concept regeneration		Transformation	gusA, vcFT	Shoot regeneration/proof of concept	USA, China, Egypt	Zong et al., 2018
Prunus sp.	Black cherry		Flowering control and insect resistance	Bark beetles	Transformation	PH3, MDL4, PsTFL1	Early flowering and pest resistance	USA	Wang and Pijut, 2014
Prunus sp.	Cherry	Gisela 6 and Glsela 7	Proof of concept	Necrotic ring spot virus	Transformation	RNAi	Resistance to Prunus necrotic ringspot virus	USA	Song et al., 2013
Prunus serotina	Black cherry		Proof of concept		Transformation	Agamous	Proof-of-concept transformation	USA	Liu and Pijut, 2010
Prunus cerasus and hybrid	Cherry	P. cerasus × P. canescens	Proof of concept		Transformation	nptII, gusA	Proof-of-concept transformation	USA	Song and Sink, 2006
Prunus sp.	Cherry	P. avium × P. pseudocerasus	Proof of concept		Somatic embryogenesis		Proof of concept	Italy	Gutièrrez-Pesce and Rugini, 2004
Prunus sp.	Cherry	P. avium × P. pseudocerasus	Proof of concept		Transformation		Proof of concept	Italy, USA	Gutièrrez-Pesce et al., 1998
Peach
Prunus persica	Peach		Proof of concept		Transformation	GUS, GFP	Proof-of-concept transformation	USA, Poland, Italy, Spain	Padilla et al., 2006
Prunus persica	Peach		Proof-of-concept regeneration		Transformation and regeneration	nptII, sGFP	Regeneration of transformed plants	Spain	Pérez-Clemente et al., 2005
Papaya
Carica papaya	Papaya			Ring spot virus	Transformation	Coat protein gene CP	Resistance to PRSV	China, Taiwan	Bau et al., 2003
Carica papaya	Papaya			Ring spot virus	RNAi particle bombardment	Coat protein gene CP	Resistance to PRSV	China, Taiwan	Jia et al., 2017

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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.

Species	Common Name	Hybrid of?	Insect/Fungus/Pest/Other Trait	Common Name/Taxonomy	Biotech Approach	Targeted Genes/Other	Final Outcome	Country of Report	Reference
Walnut
Juglans regia	Persian walnut				Transformation	fld	Increased tolerance to osmotic stress	Iran	Sheikh Beig Goharrizi et al., 2016
Juglans regia	Walnut				Transformation	nptII, uidA	Proof-of-concept transformation	USA	Walawage et al., 2014
Juglans sp.	Walnut	J. hindsii × J. regia			Transformation	rolABC	Induce rooting in hybrids	USA	Vahdati et al., 2002
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 regeneration	APHII	Transformation and regeneration of plants	USA	McGranahan et al., 1988
Plum
Prunus sp.	Plum	(P. pumila × P. salicina) × P. cerasifera	Plum pox virus (PPV)	Plum pox virus	RNAi	PPV-CV	Resistance to PPV	Russia	Sidorova et al., 2018
Prunus sp.	Plum		Plum pox virus (PPV)		Transformation	PPV-CV	Resistance to PPV	France, USA	Scorza et al., 1994
Avocado
Persea americana	Avocado		Proof of concept		Transformation	gfp, DsRed, gfp-gus	Proof-of-concept transformation and plant recovery	Spain	Palomo-Rios et al., 2017
Black Locust
Robinia pseudoacacia	Black locust		Proof of concept		Transformation	Kanamycin-resistant gene	Proof-of-concept transformation	USA	Han et al., 1993

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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.

Robinia pseudoacacia	Black locust		Herbicide tolerance		Transformation with sonication	bar, gusA	Herbicide tolerance	Spain	Zaragoza et al., 2004
Robinia pseudoacacia	Black locust		Proof of concept		Transformation	GUS	Proof-of-concept transformation	Japan	Igasaki et al., 2000
Robinia pseudoacacia	Black locust		Proof of concept		Transformation	nptII, GUS	Proof-of-concept transformation	India	Kanwar et al., 2003
Citrus
Citrus sp.	Citrus	(C. sinensis and C. paradisi) × Poncirus trifoliata	Proof of concept		Transformation	nptII, GUS	Proof of concept	Brazil, USA	de Oliveira et al., 2009
Citrus jambhiri	Rough lemon		Proof of concept		Transformation (protoplasts)	nptII and cat	Proof of concept	Israel	Vardi et al., 1990
Citrus sinensis	Citrus		Disease resistance	Xanthomonas axonopodis	Transformation	hrpN	Resistance to citrus canker	Brazil, USA	Barbosa-Mendes et al., 2009
Sweetgum
Liquidambar styraciflua			Proof of concept		Transformation	Kanamycin and GUS	Proof of concept	USA	Sullivan and Lagrimini, 1993
Liquidambar formosana	Chinese sweetgum		Stress tolerance		Transformation	AtNHXI	Tolerance to salt stress	China	Qiao et al., 2010
Liquidambar sp.	Hybrid Sweetgum	L. styraciflua × L. formosana	Phytoremediation		Transformation	ECS and merA	Mercury phytoremediation	USA	Dai et al., 2009
Liquidambar styraciflua			Insect resistance	Lymantria dispar	Transformation	Tobacco anionic peroxidase	Gypsy moth resistance	USA	Dowd et al., 1998
Liquidambar formosana	Chinese sweetgum		Stress tolerance		Transformation	SOD and POD	Tolerance to salt, drought, and cold	China	Renying et al., 2007
Cocoa
Theobroma cocoa	Cocoa		Proof of concept		Transformation	Kanamycin and nptII	Proof of concept	USA, Ghana	Sain et al., 1994
Theobroma cocoa	Cocoa		Proof of concept		Transformation	uidA	Proof of concept	Brazil	Silva et al., 2009

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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.

Species	Common Name	Insect/Fungus/Pest/Other Trait	Common Name/Taxonomy	Biotech Approach	Targeted Genes/Other	Final Outcome	Country of Report	Reference
Theobroma cocoa	Cocoa	Proof of concept		Transformation	Chi, nptII, and EGFP	Proof of concept	USA	Maximova et al., 2003
Theobroma cocoa	Cocoa	Fungal resistance	Colletotrichum gloeosporoides	Transformation	TcChi1	Resistance to Colletotrichum	USA	Maximova et al., 2006
Theobroma cocoa	Cocoa	Proof of concept		Somatic embryogenesis		Proof of concept	Colombia	Ramírez et al., 2018
Theobroma cocoa	Cocoa	Proof of concept		Transformation	GFP	Proof of concept	USA	Fister et al., 2016

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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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Guan, Q., M. He, H. Ma, X. Liao, Z. Wang, and S. Liu. 2018. Construction of genetic transformation system of Salix mongolica: In vitro leaf-based callus induction, adventitious buds differentiation, and plant regeneration. Plant Cell, Tissue and Organ Culture 132(1):213–217.

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Levée, V., E. Garin, K. Klimaszewska, and A. Seguin. 1999. Stable genetic transformation of white pine (Pinus strobus L.) after cocultivation of embryogenic tissues with Agrobacterium tumefaciens. Molecular Breeding 5(5):429–440.

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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.