. 2019 Jul 25;10:912. doi: 10.3389/fpls.2019.00912

TABLE 1.

Overview of forest trees with modified expression of lignin biosynthesis genes.

Species	Gene	Method	Growth conditions	Lignin amount	Lignin composition	Saccharification efficiency	Pulping efficiency	Biomass yield	References
Pinus radiata	HCT	RNAi	TE cultures	↓42%	↑ H/G	n.d.	n.d.	n/a	Wagner et al., 2007
Pinus radiata	CCoAOMT	RNAi	TE cultures	↓20%	↑ H/G	n.d.	n.d.	n/a	Wagner et al., 2011
Pinus radiata	CCR	RNAi	TE cultures	↓46%	Trace amount of ferulic acid	n.d.	n.d.	n/a	Wagner et al., 2013
Pinus radiata	F5H + COMT	Heterologous (over) expression	TE cultures	n.d.	Incorporation of S units	n.d.	n.d.	n/a	Wagner et al., 2015
Betula pendula	COMT	Co-suppression	Greenhouse	WT	↓ S/G	n.d.	n.d.	WT/↓	Tiimonen et al., 2005
Leucaena leucocephala	COMT	Antisense	Greenhouse	↓30%	↓ S units (histochemical)	n.d.	↑	WT	Rastogi and Dwivedi, 2006
Pinus radiata	4CL	RNAi	Greenhouse	↓36%	↑ H/G	n.d.	n.d.	↓	Wagner et al., 2009
Pinus taeda	4CL	Xylem-specific RNAi	Greenhouse	↓33%	n.d.	↑	n.d.	n.d.	Edmunds et al., 2017
Pinus taeda	CAD	Mutant allele	Greenhouse	n.d.	↑ cinnamaldehydes, ↑ benzaldehyde, ↑ dihydroconiferyl alcohol, ↓ G units	n.d.	n.d.	n.d.	Ralph et al., 1997
				↓9%	↑ coniferaldehyde	n.d.	n.d.	WT	MacKay et al., 1997
				n.d.	↑ dihydroconiferyl alcohol, ↑ vanillin, ↑ coniferaldehyde, ↑ H/G	n.d.	n.d.	n.d.	Lapierre et al., 2000
Pinus taeda	F5H + COMT + SAD/CAD	Heterologous (over) expression	Greenhouse	WT	Incorporation of S units	WT	n.d.	WT	Edmunds et al., 2017
Picea abies	CCR	Antisense	Greenhouse	↓8%	↓ H/G	n.d.	↑	↓ diameter	Wadenbäck et al., 2008
Eucalyptus urophylla × E. grandis	C3’H	Antisense	Greenhouse	↓27%	↓ S/G, ↑ H units	↑	n.d.	↓ height	Sykes et al., 2015
Eucalyptus urophylla × E. grandis	C4H	Antisense	Greenhouse	↓36%	↓ S/G	↑	n.d.	↓ height	Sykes et al., 2015
P. tremula × P.tremuloides	C4H	Antisense	Greenhouse	↓33%	WT	n.d.	n.d.	↓ height	Bjurhager et al., 2010
P. tremuloides Michx.	4CL	Antisense	Greenhouse	↓45%	WT S/G	n.d.	n.d.	↑	Hu et al., 1999^*
P. tremuloides	4CL	Downregulation	Greenhouse	Up to ↓40%	WT S/G	n.d.	n.d.	WT	Li L. et al., 2003^*
	4CL + F5H	Downregulation + overexpression	Greenhouse	↓52%	↑ S/G	n.d.	n.d.	WT
P. tremuloides	4CL	Antisense	Greenhouse	↓40%	WT S/G	n.d.	n.d.	WT	Li L. et al., 2003
P. tomentosa	4CL	Antisense	Greenhouse	↓42%	n.d.	n.d.	n.d.	WT	Jia et al., 2004
P. trichocarpa	4CL	Downregulation	Greenhouse	↓30%	WT S/V	↑	n.d.	n.d.	Min et al., 2012
P. nigra L. × P. maximowiczii	4CL	Antisense	Greenhouse	Up to ↓55%	↓ S/V/↑ S/V	n.d.	n.d.	n.d.	Min et al., 2014
P. nigra L. × P. maximowiczii	4CL + F5H	Antisense + antisense	Greenhouse	WT/↓	WT	n.d.	n.d.	n.d.
P. nigra L. × P. maximowiczii	4CL + F5H	Antisense + overexpression	Greenhouse	↓	↑S/V	n.d.	n.d.	n.d.
P. tremula × P. alba	4CL1	CRISPR/Cas9 mutants	Greenhouse	↓23%	↓S/G	n.d.	n.d.	WT	Zhou et al., 2015
P. tremula × P. alba	4CL2	CRISPR/Cas9 mutants	Greenhouse	WT	WT S/G	n.d.	n.d.	WT	Zhou et al., 2015
P. nigra L. × P. maximowiczii	4CL	Antisense	Greenhouse	↓47%	↑S/V	n.d.	n.d.	n.d.	Xiang et al., 2017
P. alba × P. grandidentata	C3’H	RNAi	Greenhouse	↓56%	↑H units, ↑S/G	n.d.	n.d.	n.d.	Coleman et al., 2008a
				n.d.	n.d.	n.d.	n.d.	↓	Coleman et al., 2008b
				WT/↓	n.d.	↑	↑	↓	Mansfield et al., 2012
P. alba × P. grandidentata	C3’H	Hairpin	Greenhouse	↓50%	↑H units, ↑ S/G	n.d.	n.d.	n.d.	Ralph et al., 2012
P. alba × P. glandulosa	C3’H	Downregulation	Greenhouse	↓30%	n.d.	n.d.	n.d.	↓ diameter	Zhou et al., 2018
P. nigra	HCT	Mutant allele	Greenhouse	WT	↑H units, ↑S/G	n.d.	n.d.	n.d.	Vanholme et al., 2013a
P. alba × P. glandulosa	HCT	Downregulation	Greenhouse	↓20%	n.d.	n.d.	n.d.	↓ diameter	Zhou et al., 2018
P. tremula × P. alba	CSE	Hairpin	Greenhouse	up to ↓25%	↑H units, ↓S/G	↑	n.d.	WT	Saleme et al., 2017
P. tremula × P. alba	CCoAOMT	Sense	Greenhouse	↓12%	↑ S/G, incorporation of p-hydroxybenzoic acid	n.d.	n.d.	WT	Meyermans et al., 2000
P. tremula × P. alba	CCoAOMT	Antisense	Greenhouse	Up to ↓40%	WT, incorporation of p-hydroxybenzoic acid	n.d.	n.d.	WT	Zhong et al., 2000
P. tormentosa	CCoAOMT	Antisense	Greenhouse	Up to ↓26%	n.d.	n.d.	n.d.	WT	Lu et al., 2004
P. tremula × P. alba	CCR	Antisense and co-suppression	Greenhouse	up to ↓30%	↓S/G, ferulic acid incorporation	n.d.	n.d.	WT	Leplé et al., 2007^*
				↓19%	WT/↓	↑	n.d.	n.d.	Van Acker et al., 2014
P. nigra L. × P. maximowiczii	F5H	Antisense	Greenhouse	WT/↑	↓S/G	n.d.	n.d.	n.d.	Min et al., 2014
P. tremuloides	F5H	Heterologous OE	Greenhouse	WT	↑S/G	n.d.	n.d.	WT	Li L. et al., 2003
P. tremula × P. alba	F5H	Heterologous OE	Greenhouse	n.d.	↑ S/G	n.d.	n.d.	n.d.	Franke et al., 2000
				WT	↑ S/G	n.d.	↑	WT	Huntley et al., 2003
				↓	↑ S/G, ↓ p-hydroxybenzoic acid	n.d.	n.d.	WT	Stewart et al., 2009
				WT	↑ S/G	WT	↑	WT	Mansfield et al., 2012
P. tremula × P. alba	COMT	Antisense	Greenhouse	WT	↓ S/G, incorporation of 5-OH-G	n.d.	n.d.	WT	Van Doorsselaere et al., 1995^*
				WT	↓ S/G	n.d.	↓	WT	Lapierre et al., 1999
P. tremula × P. alba	COMT	Co-suppression	Greenhouse	↓17%	↓ S/G, incorporation of 5-OH-G	n.d.	↑	WT	Jouanin et al., 2000
P. tremula × P. alba	CAD	Antisense and co-suppression	Greenhouse	WT	WT S/G, ↑ conjugated aldehyde moieties	n.d.	↑	WT	Baucher et al., 1996^*
				↓	WT S/G	n.d.	↑	WT	Lapierre et al., 1999
P. tremula × P. alba	CAD	Hairpin	Greenhouse	↓10%	↓ canonical S/G, ↑ sinapaldehyde	↑	n.d.	WT	Van Acker et al., 2017
P. tremula × P. alba	MOMT4	Heterologous OE	Greenhouse	↓15%	↓ S/G, ↓ p-hydroxybenzoic acid	↑	n.d.	WT	Cai et al., 2016
P. alba × P. grandidentata	PMT	Heterologous OE	Greenhouse	WT	WT S/G, incorporation of p-coumarate conjugates	n.d.	n.d.	WT	Smith et al., 2015
P. alba × P. grandidentata	FMT	Heterologous OE	Greenhouse	WT	↑ S/G, incorporation of acylated monolignols	↑	n.d.	WT	Wilkerson et al., 2014
				n.d.	n.d.	↑	n.d.	n.d.	Kim et al., 2017
				WT	WT S/G	↑	n.d.	n.d.	Bhalla et al., 2018
P. tremula × P. alba	4CL	Antisense	Field trial	WT	Low S/G in brown wood	WT	n.d.	↓	Voelker et al., 2010
P. tomentosa Carr.	4CL	Sense	Field trial	Up to ↓30%	↑ S/G	n.d.	n.d.	↑	Tian X.M. et al., 2013
P. nigra L. × P. maximowiczii A	4CL	Antisense	Field trial	WT/ ↓	WT	↑	n.d.	n.d.	Xiang et al., 2017
P. trichocarpa	4CL	Antisense	Field trial	↓	↓ S/G	n.d.	n.d.	↓	Stout et al., 2014
P. tomentosa	4CL	Antisense	Field trial	Up to ↓10%	n.d.	WT	n.d.	WT	Wang et al., 2012
P. tomentosa	CCoAOMT	Antisense	Field trial	↓6-10%	n.d.	↑	n.d.	WT	Wang et al., 2012
P. tremula × P. alba	CCoAOMT	Antisense	Field trial	↓13%	Slight increment in S/G	n.d.	↑	WT	Wei et al., 2008
P. tremula × P. alba	CCR	Antisense and co-suppression	Field trial	Up to ↓47%	↓ S/G, Incorporation of ferulic acid	n.d.	↑	↓	Leplé et al., 2007
				Up to ↓24%	Incorporation of ferulic acid	↑	n.d.	↓	Van Acker et al., 2014
P. tremula × P. alba	COMT	Antisense	Field trial	WT	↓ S/G, incorporation of 5-OH-G	n.d.	↓	WT	Lapierre et al., 1999^*
P. tremula × P. alba	COMT	Antisense	Field trial	WT	↓ S/G, incorporation of 5-OH-G	n.d.	↓	WT	Pilate et al., 2002^*
P. tremula × P. alba	CAD	Sense and antisense	Field trial	Slightly ↓	WT S/G, ↑ free phenolic units	n.d.	↑	WT	Lapierre et al., 1999^*
P. tremula × P. alba	CAD	Antisense	Field trial	Slightly ↓	WT S/G, ↑ free phenolic units	n.d.	↑	WT	Pilate et al., 2002^*

n.d., not determined; n/a, not applicable; S/G, syringyl/guaiacyl ratio; S/V, syringaldehyde/vanillin ratio; H/G, p-hydroxyphenyl/guaiacyl ratio. Papers reporting plants that have been used for independent studies reporting on biotic or abiotic stress tolerance are shown with a ^*. For abbreviations of gene names (see legend Figure 1). Lignin amount was determined by various methods, see the corresponding reference for specific information. Readers are referred to Wang et al. (2018) for additional raw data on downregulated lines for monolignol biosynthesis genes in P. trichocarpa.