Knockdown of a laccase in Populus deltoides confers altered cell wall chemistry and increased sugar release

Bryan, Anthony C.; Jawdy, Sara; Gunter, Lee; Gjersing, Erica; Sykes, Robert; Hinchee, Maud A. W.; Winkeler, Kimberly A.; Collins, Cassandra M.; Engle, Nancy; Tschaplinski, Timothy J.; Yang, Xiaohan; Tuskan, Gerald A.; Muchero, Wellington; Chen, Jin‐Gui

doi:10.1111/pbi.12560

Title: Knockdown of a laccase in Populus deltoides confers altered cell wall chemistry and increased sugar release

Journal Article · Fri Apr 15 00:00:00 EDT 2016 · Plant Biotechnology Journal

DOI:https://doi.org/10.1111/pbi.12560· OSTI ID:1247616

^[1]; Jawdy, Sara ^[1]; Gunter, Lee ^[1]; Gjersing, Erica ^[2]; Sykes, Robert ^[2]; Hinchee, Maud A. W. ^[3]; Winkeler, Kimberly A. ^[3]; Collins, Cassandra M. ^[3]; Engle, Nancy ^[1]; Tschaplinski, Timothy J. ^[1]; Yang, Xiaohan ^[1]; Tuskan, Gerald A. ^[1]; Muchero, Wellington ^[1]; Chen, Jin‐Gui ^[1]

BioEnergy Science Center and Biosciences Division Oak Ridge National Laboratory Oak Ridge TN USA
The Biosciences Center National Renewable Energy Laboratory Golden CO USA
ArborGen Inc Ridgeville SC USA

Plant laccases are thought to function in the oxidation of monolignols which leads to higher order lignin formation. Only a hand-full of laccases in plants have been functionally evaluated and as such little is known about the breadth of their impact on cell wall chemistry or structure. Here we describe a previously uncharacterized laccase from Populus, encoded by locus Potri.008G06400, whose reduced expression resulted in transgenic Populus trees with changes in syringyl/guaiacyl (S/G) ratios as well as altered sugar release phenotypes. These phenotypes are consistent with plant biomass exhibiting reduced recalcitrance. Interestingly, the transgene effect on recalcitrance is dependent on a mild pretreatment prior to chemical extraction of sugars. Metabolite profiling suggests the transgene modulates phenolics that are associated with the cell wall structure. Finally, we propose a model in which this particular laccase has a range of functions related to oxidation of phenolics that interact with lignin in the cell wall.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: DE‐AC05‐00OR22725; DE‐FG02‐93ER20097; AC05-00OR22725; FG02-93ER20097; AC36-08GO28308

OSTI ID:: 1247616

Alternate ID(s):: OSTI ID: 1247617; OSTI ID: 1311231; OSTI ID: 1325508

Report Number(s):: NREL/JA-5100-66207

Journal Information:: Plant Biotechnology Journal, Journal Name: Plant Biotechnology Journal Vol. 14 Journal Issue: 10; ISSN 1467-7644

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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Cited by: 51 works

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References (47)

The laccase multigene family in Arabidopsis thaliana: towards addressing the mystery of their gene function(s) Turlapati, Phanikanth V.; Kim, Kye-Won; Davin, Laurence B. Planta, Vol. 233, Issue 3 https://doi.org/10.1007/s00425-010-1298-3	journal	November 2010
Normal-12 and Brown Midrib-12 Sorghum. II. Chemical Variations and Digestibility1 Akin, D. E.; Hanna, W. W.; Snook, M. E. Agronomy Journal, Vol. 78, Issue 5 https://doi.org/10.2134/agronj1986.00021962007800050018x	journal	January 1986
Fungal laccases – occurrence and properties Baldrian, Petr FEMS Microbiology Reviews, Vol. 30, Issue 2 https://doi.org/10.1111/j.1574-4976.2005.00010.x	journal	March 2006
Tricin, a Flavonoid Monomer in Monocot Lignification Lan, Wu; Lu, Fachuang; Regner, Matthew Plant Physiology, Vol. 167, Issue 4 https://doi.org/10.1104/pp.114.253757	journal	February 2015
High-level hemicellulosic arabinose predominately affects lignocellulose crystallinity for genetically enhancing both plant lodging resistance and biomass enzymatic digestibility in rice mutants Li, Fengcheng; Zhang, Mingliang; Guo, Kai Plant Biotechnology Journal, Vol. 13, Issue 4 https://doi.org/10.1111/pbi.12276	journal	November 2014
Biomass digestibility is predominantly affected by three factors of wall polymer features distinctive in wheat accessions and rice mutants Wu, Zhiliang; Zhang, Mingliang; Wang, Lingqiang Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-183	journal	January 2013
The dual effects of lignin content on enzymatic hydrolysis using film composed of cellulose and lignin as a structure model Zhang, Lu; Zhang, Liming; Zhou, Tian Bioresource Technology, Vol. 200 https://doi.org/10.1016/j.biortech.2015.10.048	journal	January 2016
Lignin content in natural Populus variants affects sugar release Studer, M. H.; DeMartini, J. D.; Davis, M. F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305 https://doi.org/10.1073/pnas.1009252108	journal	March 2011
A Laccase Associated with Lignification in Loblolly Pine Xylem Bao, W.; O'Malley, D. M.; Whetten, R. Science, Vol. 260, Issue 5108 https://doi.org/10.1126/science.260.5108.672	journal	April 1993
Lignin modification improves fermentable sugar yields for biofuel production Chen, Fang; Dixon, Richard A. Nature Biotechnology, Vol. 25, Issue 7, p. 759-761 https://doi.org/10.1038/nbt1316	journal	June 2007
Characterization and localization of laccase forms in stem and cell cultures of sycamore Driouich, Azeddine; Laine, Anne-Catherine; Vian, Brigitte The Plant Journal, Vol. 2, Issue 1 https://doi.org/10.1111/j.1365-313X.1992.00013.x	journal	January 1992
The origin and evolution of lignin biosynthesis: Tansley review Weng, Jing-Ke; Chapple, Clint New Phytologist, Vol. 187, Issue 2 https://doi.org/10.1111/j.1469-8137.2010.03327.x	journal	June 2010
Disruption of LACCASE4 and 17 Results in Tissue-Specific Alterations to Lignification of Arabidopsis thaliana Stems Berthet, Serge; Demont-Caulet, Nathalie; Pollet, Brigitte The Plant Cell, Vol. 23, Issue 3 https://doi.org/10.1105/tpc.110.082792	journal	March 2011
Priming in Systemic Plant Immunity Jung, Ho Won; Tschaplinski, Timothy J.; Wang, Lin Science, Vol. 324, Issue 5923 https://doi.org/10.1126/science.1170025	journal	April 2009
High-Throughput Screening of Plant Cell-Wall Composition Using Pyrolysis Molecular Beam Mass Spectroscopy Sykes, Robert; Yung, Matthew; Novaes, Evandro Biofuels https://doi.org/10.1007/978-1-60761-214-8_12	book	January 2009
Insect multicopper oxidases: Diversity, properties, and physiological roles Dittmer, Neal T.; Kanost, Michael R. Insect Biochemistry and Molecular Biology, Vol. 40, Issue 3 https://doi.org/10.1016/j.ibmb.2010.02.006	journal	March 2010
Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa Lu, S.; Li, Q.; Wei, H. Proceedings of the National Academy of Sciences, Vol. 110, Issue 26 https://doi.org/10.1073/pnas.1308936110	journal	June 2013
MEGA5: Molecular Evolutionary Genetics Analysis Using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods Tamura, K.; Peterson, D.; Peterson, N. Molecular Biology and Evolution, Vol. 28, Issue 10 https://doi.org/10.1093/molbev/msr121	journal	May 2011
Biochemical characterization, molecular cloning and expression of laccases - a divergent gene family - in poplar Ranocha, Philippe; McDougall, Gordon; Hawkins, Simon European Journal of Biochemistry, Vol. 259, Issue 1-2 https://doi.org/10.1046/j.1432-1327.1999.00061.x	journal	January 1999
Biomass equations for sixty-five North American tree species Ter-Mikaelian, Michael T.; Korzukhin, Michael D. Forest Ecology and Management, Vol. 97, Issue 1 https://doi.org/10.1016/S0378-1127(97)00019-4	journal	September 1997
SignalP 4.0: discriminating signal peptides from transmembrane regions Petersen, Thomas Nordahl; Brunak, Søren; von Heijne, Gunnar Nature Methods, Vol. 8, Issue 10 https://doi.org/10.1038/nmeth.1701	journal	September 2011
Structural characterization of alkaline hydrogen peroxide pretreated grasses exhibiting diverse lignin phenotypes Li, Muyang; Foster, Cliff; Kelkar, Shantanu Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-38	journal	January 2012
Engineering of plant cell walls for enhanced biofuel production Loqué, Dominique; Scheller, Henrik V.; Pauly, Markus Current Opinion in Plant Biology, Vol. 25 https://doi.org/10.1016/j.pbi.2015.05.018	journal	June 2015
Progress in the biological synthesis of the plant cell wall: new ideas for improving biomass for bioenergy Carpita, Nicholas C. Current Opinion in Biotechnology, Vol. 23, Issue 3 https://doi.org/10.1016/j.copbio.2011.12.003	journal	June 2012
Galacturonosyltransferase 4 silencing alters pectin composition and carbon partitioning in tomato de Godoy, Fabiana; Bermúdez, Luisa; Lira, Bruno Silvestre Journal of Experimental Botany, Vol. 64, Issue 8 https://doi.org/10.1093/jxb/ert106	journal	April 2013
Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana McCaig, Bonnie C.; Meagher, Richard B.; Dean, Jeffrey F. D. Planta, Vol. 221, Issue 5 https://doi.org/10.1007/s00425-004-1472-6	journal	June 2005
Mutant identification and characterization of the laccase gene family in Arabidopsis Cai, Xiaoning; Davis, Elizabeth J.; Ballif, Jenny Journal of Experimental Botany, Vol. 57, Issue 11 https://doi.org/10.1093/jxb/erl022	journal	June 2006
Lignin extraction distinctively enhances biomass enzymatic saccharification in hemicelluloses-rich Miscanthus species under various alkali and acid pretreatments Si, Shengli; Chen, Yan; Fan, Chunfen Bioresource Technology, Vol. 183 https://doi.org/10.1016/j.biortech.2015.02.031	journal	May 2015
The Arabidopsis Information Resource (TAIR): a comprehensive database and web-based information retrieval, analysis, and visualization system for a model plant Huala, E. Nucleic Acids Research, Vol. 29, Issue 1 https://doi.org/10.1093/nar/29.1.102	journal	January 2001
Mechanisms of intrinsic resistance to antimicrobial peptides of Edwardsiella ictaluri and its influence on fish gut inflammation and virulence Gatlin, Delbert M.; Santander, Javier; Loh, Amanda Microbiology, Vol. 159, Issue 7 https://doi.org/10.1099/mic.0.066639-0	journal	July 2013
Hemicelluloses negatively affect lignocellulose crystallinity for high biomass digestibility under NaOH and H2SO4 pretreatments in Miscanthus Xu, Ning; Zhang, Wei; Ren, Shuangfeng Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-58	journal	January 2012
LACCASE Is Necessary and Nonredundant with PEROXIDASE for Lignin Polymerization during Vascular Development in Arabidopsis Zhao, Qiao; Nakashima, Jin; Chen, Fang The Plant Cell, Vol. 25, Issue 10 https://doi.org/10.1105/tpc.113.117770	journal	October 2013
Phytozome: a comparative platform for green plant genomics Goodstein, David M.; Shu, Shengqiang; Howson, Russell Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr944	journal	November 2011
Laccase from Sycamore Maple ( Acer pseudoplatanus ) Polymerizes Monolignols Sterjiades, Raja; Dean, Jeffrey F. D.; Eriksson, Karl-Erik L. Plant Physiology, Vol. 99, Issue 3 https://doi.org/10.1104/pp.99.3.1162	journal	July 1992
Characterization of cDNAs encoding putative laccase-like multicopper oxidases and developmental expression in the tobacco hornworm, Manduca sexta, and the malaria mosquito, Anopheles gambiae Dittmer, Neal T.; Suderman, Richard J.; Jiang, Haobo Insect Biochemistry and Molecular Biology, Vol. 34, Issue 1 https://doi.org/10.1016/j.ibmb.2003.08.003	journal	January 2004
Clonal differences in biomass characteristics, coppice ability, and biomass prediction equations among four Populus clones grown in eastern North Dakota Tuskan, Gerald A.; Rensema, Timothy R. Canadian Journal of Forest Research, Vol. 22, Issue 3 https://doi.org/10.1139/x92-045	journal	March 1992
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 Biswal, Ajaya K.; Hao, Zhangying; Pattathil, Sivakumar Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0218-y	journal	January 2015
Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone Wilkerson, C. G.; Mansfield, S. D.; Lu, F. Science, Vol. 344, Issue 6179, p. 90-93 https://doi.org/10.1126/science.1250161	journal	April 2014
Molecular docking and dynamics simulation analyses unraveling the differential enzymatic catalysis by plant and fungal laccases with respect to lignin biosynthesis and degradation Awasthi, Manika; Jaiswal, Nivedita; Singh, Swati Journal of Biomolecular Structure and Dynamics, Vol. 33, Issue 9 https://doi.org/10.1080/07391102.2014.975282	journal	November 2014
Deconstruction of Lignocellulosic Biomass to Fuels and Chemicals Chundawat, Shishir P. S.; Beckham, Gregg T.; Himmel, Michael E. Annual Review of Chemical and Biomolecular Engineering, Vol. 2, Issue 1, p. 121-145 https://doi.org/10.1146/annurev-chembioeng-061010-114205	journal	July 2011
The Minor Wall-Networks between Monolignols and Interlinked-Phenolics Predominantly Affect Biomass Enzymatic Digestibility in Miscanthus Li, Zhengru; Zhao, Chunqiao; Zha, Yi PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0105115	journal	August 2014
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method Livak, Kenneth J.; Schmittgen, Thomas D. Methods, Vol. 25, Issue 4 https://doi.org/10.1006/meth.2001.1262	journal	December 2001
Generation and characterization of transgenic poplar plants overexpressing a cotton laccase gene Wang, Ji; Wang, Chenglong; Zhu, Mulan Plant Cell, Tissue and Organ Culture, Vol. 93, Issue 3 https://doi.org/10.1007/s11240-008-9377-x	journal	April 2008
Bioprocessing for biofuels Blanch, Harvey W. Current Opinion in Biotechnology, Vol. 23, Issue 3, p. 390-395 https://doi.org/10.1016/j.copbio.2011.10.002	journal	June 2012
Laccases and their occurrence in prokaryotes Claus, Harald Archives of Microbiology, Vol. 179, Issue 3 https://doi.org/10.1007/s00203-002-0510-7	journal	February 2003
Laccase Down-Regulation Causes Alterations in Phenolic Metabolism and Cell Wall Structure in Poplar Ranocha, Philippe; Chabannes, Matthieu; Chamayou, Simon Plant Physiology, Vol. 129, Issue 1 https://doi.org/10.1104/pp.010988	journal	April 2002
Laccase: enzyme revisited and function redefined Sharma, Krishna Kant; Kuhad, Ramesh Chander Indian Journal of Microbiology, Vol. 48, Issue 3 https://doi.org/10.1007/s12088-008-0028-z	journal	June 2008

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Title: Knockdown of a laccase in Populus deltoides confers altered cell wall chemistry and increased sugar release

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