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. Biotechnology For Biofuels

Biswal, Ajaya K.; Hao, Zhangying; Pattathil, Sivakumar; Yang, Xiaohan; Winkeler, Kim; Collins, Cassandra; Mohanty, Sushree S.; Richardson, Elizabeth A.; Gelineo-Albersheim, Ivana; Hunt, Kimberly; Ryno, David; Sykes, Robert W.; Turner, Geoffrey B.; Ziebell, Angela; Gjersing, Erica; Lukowitz, Wolfgang; Davis, Mark F.; Decker, Stephen R.; Hahn, Michael G.; Mohnen, Debra A.

doi:10.1186/s13068-015-0218-y

Title: 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. Biotechnology For Biofuels

Journal Article · 12 March 2015 · Biotechnology for Biofuels

DOI: https://doi.org/10.1186/s13068-015-0218-y · OSTI ID:1265706

Biswal, Ajaya K. ^[1]; Hao, Zhangying ^[1]; Pattathil, Sivakumar ^[1]; Yang, Xiaohan ^[2]; Winkeler, Kim ^[3]; Collins, Cassandra ^[3]; Mohanty, Sushree S. ^[1]; Richardson, Elizabeth A. ^[4]; Gelineo-Albersheim, Ivana ^[1]; Hunt, Kimberly ^[1]; Ryno, David ^[1]; Sykes, Robert W. ^[5]; Turner, Geoffrey B. ^[5]; Ziebell, Angela ^[5]; Gjersing, Erica ^[5]; Lukowitz, Wolfgang ^[4]; Davis, Mark F. ^[5]; Decker, Stephen R. ^[5]; Hahn, Michael G. ^[1]; Mohnen, Debra A. ^[1]

Univ. of Georgia, Athens, GA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); ArborGen Inc., Ridgeville, SC (United States)
Univ. of Georgia, Athens, GA (United States)
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); National Renewable Energy Lab. (NREL), Golden, CO (United States)

Background The inherent recalcitrance of woody bioenergy feedstocks is a major challenge for their use as a source of second-generation biofuel. Secondary cell walls that constitute the majority of hardwood biomass are rich in cellulose, xylan, and lignin. The interactions among these polymers prevent facile accessibility and deconstruction by enzymes and chemicals. Plant biomass that can with minimal pretreatment be degraded into sugars is required to produce renewable biofuels in a cost-effective manner. Results GAUT12/IRX8 is a putative glycosyltransferase proposed to be involved in secondary cell wall glucuronoxylan and/or pectin biosynthesis based on concomitant reductions of both xylan and the pectin homogalacturonan (HG) in Arabidopsis irx8 mutants. Two GAUT12 homologs exist in Populus trichocarpa, PtGAUT12.1 and PtGAUT12.2. Knockdown expression of both genes simultaneously has been shown to reduce xylan content in Populus wood. We tested the proposition that RNA interference (RNAi) downregulation of GAUT12.1 alone would lead to increased sugar release in Populus wood, that is, reduced recalcitrance, based on the hypothesis that GAUT12 synthesizes a wall structure required for deposition of xylan and that cell walls with less xylan and/or modified cell wall architecture would have reduced recalcitrance. Using an RNAi approach, we generated 11 Populus deltoides transgenic lines with 50 to 67% reduced PdGAUT12.1 transcript expression compared to wild type (WT) and vector controls. Ten of the eleven RNAi lines yielded 4 to 8% greater glucose release upon enzymatic saccharification than the controls. The PdGAUT12.1 knockdown (PdGAUT12.1-KD) lines also displayed 12 to 52% and 12 to 44% increased plant height and radial stem diameter, respectively, compared to the controls. Knockdown of PdGAUT12.1 resulted in a 25 to 47% reduction in galacturonic acid and 17 to 30% reduction in xylose without affecting total lignin content, revealing that in Populus wood as in Arabidopsis, GAUT12 affects both pectin and xylan formation. Analyses of the sugars present in sequential cell wall extracts revealed a reduction of glucuronoxylan and pectic HG and rhamnogalacturonan in extracts from PdGAUT12.1-KD lines. Conclusions The results show that downregulation of GAUT12.1 leads to a reduction in a population of xylan and pectin during wood formation and to reduced recalcitrance, more easily extractable cell walls, and increased growth in Populus.

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

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725; PS02-06ER64304; FG02-93ER20097

OSTI ID:: 1265706

Alternate ID(s):: OSTI ID: 1220619

Report Number(s):: NREL/JA-2700-62639; KP1601050; ERKP695

Journal Information:: Biotechnology for Biofuels, Vol. 8, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 100 works

Citation information provided by
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4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein Urbanowicz, B. R.; Pena, M. J.; Ratnaparkhe, S. Proceedings of the National Academy of Sciences, Vol. 109, Issue 35 https://doi.org/10.1073/pnas.1208097109	journal	August 2012
Arabidopsis thaliana T-DNA Mutants Implicate GAUT Genes in the Biosynthesis of Pectin and Xylan in Cell Walls and Seed Testa Caffall, Kerry H.; Pattathil, Sivakumar; Phillips, Sarah E. Molecular Plant, Vol. 2, Issue 5 https://doi.org/10.1093/mp/ssp062	journal	September 2009
IRX14 and IRX14-LIKE, Two Glycosyl Transferases Involved in Glucuronoxylan Biosynthesis and Drought Tolerance in Arabidopsis Keppler, Brian D.; Showalter, Allan M. Molecular Plant, Vol. 3, Issue 5 https://doi.org/10.1093/mp/ssq028	journal	September 2010
Molecular Dissection of Xylan Biosynthesis during Wood Formation in Poplar Lee, Chanhui; Teng, Quincy; Zhong, Ruiqin Molecular Plant, Vol. 4, Issue 4 https://doi.org/10.1093/mp/ssr035	journal	July 2011
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The irregular xylem9 Mutant is Deficient in Xylan Xylosyltransferase Activity Lee, C.; O'Neill, M. A.; Tsumuraya, Y. Plant and Cell Physiology, Vol. 48, Issue 11 https://doi.org/10.1093/pcp/pcm135	journal	September 2007
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Three Members of the Arabidopsis Glycosyltransferase Family 8 Are Xylan Glucuronosyltransferases Rennie, Emilie A.; Hansen, Sara Fasmer; Baidoo, Edward E. K. Plant Physiology, Vol. 159, Issue 4 https://doi.org/10.1104/pp.112.200964	journal	June 2012
Identification of Novel Genes in Arabidopsis Involved in Secondary Cell Wall Formation Using Expression Profiling and Reverse Genetics Brown, David M.; Zeef, Leo A. H.; Ellis, Joanne The Plant Cell, Vol. 17, Issue 8 https://doi.org/10.1105/tpc.105.031542	journal	June 2005
The Arabidopsis irregular xylem8 Mutant Is Deficient in Glucuronoxylan and Homogalacturonan, Which Are Essential for Secondary Cell Wall Integrity Persson, Staffan; Caffall, Kerry Hosmer; Freshour, Glenn The Plant Cell, Vol. 19, Issue 1 https://doi.org/10.1105/tpc.106.047720	journal	January 2007
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Arabidopsis thaliana IRX10 and two related proteins from psyllium and Physcomitrella patens are xylan xylosyltransferases Jensen, Jacob Krüger; Johnson, Nathan Robert; Wilkerson, Curtis Gene The Plant Journal, Vol. 80, Issue 2 https://doi.org/10.1111/tpj.12641	journal	September 2014
Two Arabidopsis proteins synthesize acetylated xylan in vitro Urbanowicz, Breeanna R.; Peña, Maria J.; Moniz, Heather A. The Plant Journal, Vol. 80, Issue 2 https://doi.org/10.1111/tpj.12643	journal	September 2014
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A review of xylan and lignin biosynthesis: Foundation for studying Arabidopsis irregular xylem mutants with pleiotropic phenotypes Hao, Zhangying; Mohnen, Debra Critical Reviews in Biochemistry and Molecular Biology, Vol. 49, Issue 3 https://doi.org/10.3109/10409238.2014.889651	journal	February 2014
Loss of Arabidopsis GAUT12/IRX8 causes anther indehiscence and leads to reduced G lignin associated with altered matrix polysaccharide deposition Hao, Zhangying; Avci, Utku; Tan, Li Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00357	journal	July 2014

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