Growth under field conditions affects lignin content and … · 2016-03-10 · and productivity in transgenic Populus trichocarpa with altered lignin biosynthesis ... INRA UMR 1391
This document is posted to help you gain knowledge. Please leave a comment to let me know what you think about it! Share it to your friends and learn new things together.
Transcript
ww.sciencedirect.com
b i om a s s a n d b i o e n e r g y 6 8 ( 2 0 1 4 ) 2 2 8e2 3 9
Available online at w
ScienceDirect
ht tp: / /www.elsevier .com/locate/biombioe
Growth under field conditions affects lignin contentand productivity in transgenic Populus trichocarpawith altered lignin biosynthesis
Anna T. Stout a,*, Aletta A. Davis a, Jean-Christophe Domec a,b,Chenmin Yang a, Rui Shi a, John S. King a
a North Carolina State University, Department of Forestry & Environmental Resources, 3120 Jordan Hall,
Campus Box 8008, Raleigh, NC 27695, USAb Bordeaux Sciences Agro, INRA UMR 1391 ISPA, F-33170 Gradignan, France
Table 2 e Means, SE, and Dunnett p-values for lignin and S/G ratio after two years of growth in the field, biomass coppice one, height coppice one, sylleptic branches,biomass coppice two, height coppice two, number of stems, and percent survival at the Mountain site. Bold typeface denotes significant difference from wildtype.
Table 3 e Means, SE, and Dunnett p-values for lignin and S/G ratio after two years of growth in the field, biomass coppice one, height coppice one, sylleptic branches,biomass coppice two, height coppice two, number of stems, and percent survival at the Piedmont site. Bold typeface denotes significant difference from wildtype.
Table 4 e Means, SE, and Dunnett p-values for lignin and S/G ratio after two years of growth in the field, biomass coppice one, height coppice one, sylleptic branches,biomass coppice two, height coppice two, number of stems, and percent survival at the Coastal Plain site. Bold typeface denotes significant difference from wildtype.
Table 5 e Initial greenhouse lignin concentration and S/G ratio, field values and percent change of Populus trichocarpa transgenically modified for decreased wood ligninafter 3 years growth in the field.
b i om a s s a n d b i o e n e r g y 6 8 ( 2 0 1 4 ) 2 2 8e2 3 9238
stunted growth and a shrubby appearance, and the presence
of wood of a reddish-brown color occupying 24%e60% of
cross-sectional area. The brown wood coloration was associ-
ated with altered wood chemistry and morphology, most
significantly collapsed vessels and the deposition of phenolic
“extractives” that occluded vessels [41]. In our study, we
attempted to quantify production of reddish-brown wood
through digital analysis, but found essentially no detectable
change in wood color. Unlike our study, changes in total lignin
content or S/G ratio from greenhouse to field were not spe-
cifically addressed by Voelker et al., [29].
Wang et al. (2011) [32] found that a 6e10% reduction in total
lignin did not cause altered growth rates over a five year field
trial of two lines of antisense 4CL Populus tomentosa in Beijing,
China. However, Wang et al. (2011) [32] did find that insoluble
lignin content increased throughout development, from 10 to
15% in one year old clonal siblings to 19% after five years.
Lastly, although not specifically addressed in this study,
Voelkler et al. (2010) [29] andWang et al. (2011) [32] found that
total glucose and xylose release by enzymatic hydrolysis of
pretreated wood did not increase despite the reduction of
lignin content by antisense 4CL. In addition, Wang et al. (2011)
[32] found a strong negative correlation between soluble lignin
content (higher S content) and the amount of glucose released
by enzymatic hydrolysis.
5. Conclusion
The ability to decrease lignin and increase S/G ratio in trees for
improvement of ethanol feedstocks, while retaining or
enhancing productivity, could have a profound impact on the
economics of cellulosic biofuels. The U.S. Department of
Agriculture estimates that in order to be economically viable,
perennial biofuels feedstocks will require sustained agro-
nomic yields in excess of 24.71 ton ha�1 year�1 [3]. The results
from this study indicate that wildtype or low-lignin transgenic
P. trichocarpa may not be well suited for SRWC in the Coastal
Plain or Piedmont of North Carolina and that some lines of
antisense 4CL Populus develop unfavorable phenotypes when
exposed to field conditions. However, this study demonstrates
that wildtype P. trichocarpa can be grown in the Mountain re-
gion of North Carolina (and surrounding states) at yields that
can be competitive as a biofuel feedstock, although large-scale
field trials are necessary to estimate biomass production rates
comparable that would better simulate operational bioenergy
SRWC plantations. In addition, several transgenic low-lignin
lines (As4CL-6, CH-2, PT-1, PT-3, and PT-4) remain promising
possibilities for further studies. More research focused on
promising construct lines in appropriate environmental con-
ditions and with larger samples sizes is needed to clarify if a
significant reduction in total lignin content can be achieved on
a plantation scale, and whether that reduction will translate
into the increased efficiency of enzymatic hydrolysis.
Acknowledgments
The work of JSK, ATS, and AAD were principally supported by
grants USDA CSREES Rural Development Program 2009-10001-
05113 and USDA NIFA 2010-34458-21103. J-CD was supported
by USDA Forest Service Eastern Forest Environmental Threat
Assessment Center (EFETAC) grant 08-JV11330147-038 and by
the DOE e BER Terrestrial Ecosystem Sciences program (11-
DE-SC-0006700 - ER65189). The Department of Biology and
the Plant and Vegetation Ecology Research Group (PLECO) of
the University of Antwerp, the Belgian Francqui Foundation,
and the U.S. Council for International Exchange of Scholars-
Fulbright Program, all provided sabbatical support to JSK
during the writing of this manuscript.
r e f e r e n c e s
[1] Sims R, Hastings A, Schlamadinger B, Taylor G, Smith P.Energy crops: current status and future prospects. GlobChange Biol 2006;12:2054e76.
[2] EPA. EPA lifecycle analysis of greenhouse gas emissions fromrenewable fuels. Washington, DC: US EnvironmentalProtection Agency Office of Transportation and Air Quality;2010. EPA-420-F-09-024.
[3] USDA DOE. Biomass as a feedstock for a bioenergy andbioproducts industry: the technical feasibility of a billion-tonannual supply; 2005. United States Department of Energy,Oak Ridge, TN and United States Department of Commerce,Springfield, VA. Available from: http://www1.eere.energy.gov/bipmass/pdfs/final_billionton_vision_report2.pdf.
[4] Dale V, Kline K, Wiens J, Fargione J. Biofuels: implicationsfor land use and biodiversity. Biofuels Sustain ReportsEcol Soc Am 2010. Available from:www.esa.org/biofuelsreports.
[5] USDA. A USDA regional roadmap for meeting the biofuelsgoals of the renewable fuels standard by 2022; 2010.Available from: http://www.usda.gov/documents/USDA_Biofuels_Report_6232010.pdf.
[6] Kenney W, Sennerby-Forsse L, Layton P. A review of biomassquality research relevant to the use of poplar and willow forenergy conversion. Biomass 1990;21:163e88.
[7] Dickmann D. Silviculture and biology of short-rotationwoody crops in temperate regions: then and now. BiomassBioenergy 2006;30:696e705.
[8] Rae A, Pinel P, Bastien C, Sabatti M, Street N, Tucker J, et al.QTL for yield in bioenergy Populus: identifying GxEinteractions from growth at three contrasting sites. TreeGenet Genomes 2008;4:97e112.
[9] Al Afas N, Marron N, Van Dongen S, Laureysens I,Ceulemans R. Dynamics of biomass production in a poplarcoppice culture over three rotations (11 years). For EcolManag 2008;255:1883e91.
[10] Sjostrom E. Wood chemistry. San Diego: Academic Press;1993.
[11] Novaes E, Kirst M, Chiang V, Winter-Sederoff H, Sederoff R.Lignin and biomass: a negative correlation for woodformation and lignin content in trees. Plant Physiol2010;2010(154):555e61.
[12] Harris D, Debolt S. Synthesis, regulation, and utilizationof lignocellulosic biomass. Plant Biotechnol J2010;8:244e62.
[13] Chapple C, Ladisch M, Meilan R. Loosening lignin's grip onbiofuel production. Nat Biotechnol 2007;25:746e8.
[14] Keating J, Panganiban C, Mansfield S. Tolerance and adaptionof ethanologenic yeasts to lignocellulosic inhibitorycompounds. Biotechnol Bioeng 2006;93:1196e206.
[15] Whetten R, Mackay J, Sederoff R. Recent advances inunderstanding lignin biosynthesis. Annu Rev Plant PhysiolPlant Mol Biol 1998;49:585e609.
b i om a s s a n d b i o e n e r g y 6 8 ( 2 0 1 4 ) 2 2 8e2 3 9 239
[16] Bonawitz N, Chapple C. The genetics of lignin biosynthesis:connecting genotype to phenotype. Annu Rev Genet2010;44:337e63.
[17] Hancock J, Loya W, Giardina C, Li L, Chiang V, Pregitzer K.Plant growth, biomass partitioning and soil carbon formationin response to altered lignin biosynthesis in Populustremuloides. New Phytol 2007;173:732e42.
[18] Chaing V, Funaoka M. The dissolution and condensationreactions of guaiacyl and syringyl units in residual ligninduring kraft delignifaction of sweetgum. Holzforschung1990;44(2):147e56.
[19] Franke R, McMichael CM, Meyer K, Shirley AM, Cusumano JC,Chapple C. Modified lignin in tobacco and poplar plants over-expressing the arabadopsis gene encoding ferulate 5-hydroxylase. Plant J 2000;22:223e34.
[20] Chang H, Sarkanen K. Species variation in lignin- effect ofspecies on rate of kraft delignification. Tech Assoc Pulp PapIndustry 1973;56:132e4.
[21] Li L, Zhou Y, Cheng X, Sun J, Marita J, Ralph J, et al.Combinatorial modification of multiple lignin traits in treesthrough multigene cotransformation. Proc Natl Acad Sci U SA 2003;8:4939e44.
[22] Osakabe K, Tsao C, Li L, Popko J, Umezawa T, Carroway D,et al. Coniferyl aldehyde 5-hydroxylation and methylationdirect syringyl lignin biosynthesis in angiosperms. Proc NatlAcad Sci U S A 1999;96:8955e60.
[23] Huntley S, Ellis D, Gilbert M, Chapple C, Mansfield S.Significant increases in pulping efficiency in C4H-F5H-transformed poplars: improved chemical savings andreduced environmental toxins. J Agric Food Chem2003;51:6178e83.
[24] Mansfield SD, Kang K-Y, Chapple C. Designed fordeconstruction e Poplar trees altered in cell wall lignificationimprove the efficacy of bioethanol production. New Phytol2012;194(1):91e101.
[25] Kajita S, Katayama Y, Omori S. Alterations in biosynthesis oflignin in transgenic plants with chimeric genes for 4-coumarate:coenzme A ligase. Plant Cell Physiol1996;37:957e65.
[26] Lee D, Meyer K, Chapple C, Douglas C. Antisense suppressionof 4-coumarate: coenzyme A ligase activity in Arabidopsisleads to altered lignin subunit composition. Plant Cell1997;9:1985e98.
[27] Hu W, Harding S, Lung J, Popko J, Ralph J, Stokke D, et al.Repression of lignin biosynthesis promotes celluloseaccumulation and growth in transgenic trees. Nat Biotechnol1999;17:808e12.
[28] Horvath B, Peszlen I, Peralta P, Kasal B, Li L. Effect of ligningenetic modification on wood anatomy of aspen trees. IntAssoc Wood Anatomists 2010;31:29e38.
[29] Voelker S, Lachenbruch B, Meinzer F, Jourdes M, Ki C,Patten A, et al. Antisense down-regulation of 4CL expressionalters lignification, tree growth, and saccharificationpotential of field-grown poplar. Plant Physiol2010;154:874e86.
[30] Roque-Rivera R, Talhelm A, Johnson D, Chaing V, Pregitzer K.Effects of lignin-modified Populus tremuloides on soil organiccarbon. J Plant Nutr Soil Sci 2011;174:818e26.
[31] Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C,Lepl�e JC, et al. Filed and pulping performances oftransgenic trees with altered lignification. Nat Biotechnol2002;20:607e12.
[32] Wang H, Xue Y, Chen Y, Li R, Wei J. Lignin modificationimproves biofuel production potential in transgenic Populustomentosa. Industrial Crops Prod 2011;37:170e7.
[33] Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I,Hellsten U, et al. The genome of black cottonwood, Populustrichocarpa (Torr. & Gray). Science 2006;313:1596e604.
[34] Burns R, Honkala B. Silvics of North America: 1. conifers: 2.hardwoods. Agriculture handbook 654vol. 2. Washington,DC: U.S. Department of Agriculture, Forest Service; 1990.p. 877.
[35] Sykes R, Yung M, Novaes E, Kirst M, Peter G, Davis M. High-throughput screens of plant cell-wall composition usingpyrolysis molecular beam mass spectroscopy. Methods MolBiol 2009;581:169e83.
[36] Marron N, Bastien C, Maurizio S, Taylor G, Cuelmans R.Plasticity of growth and sylleptic branchiness in two poplarfamilies grown at three sites across Europe. Tree Physiol2006;26:935e46.
[37] Remphrey W, Powell G. Crown architecture of larix laricinasaplings: sylleptic branching on the main stem. Can J Bot1985;63:1296e302.
[38] Vance C, Kirk T, Sherwood R. Lignification as a mechanism ofdisease resistance. Annu Rev Phytopathol 1980;18:259e88.
[39] Boerjan W, Ralph J, Baucher M. Lignin biosynthesis. AnnuRev Plant Biol 2003;54:519e46.
[40] Amthor J. Efficiency of lignin biosynthesis: a quantitativeanalysis. Ann Bot 2003;91:673e95.
[41] Kitin P, Voelker S, Meinzer F, Beeckman H, Strauss S,Lachenbruch B. Tyloses and phenolic deposits in xylemvessels impede water transport in low-lignin transgenicpoplars: a study by cryo-flourescence microscopy. PlantPhysiol 2010;154:887e98.