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 · Thu Mar 12 00:00:00 EDT 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

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Multitrait genome‐wide association analysis of Populus trichocarpa identifies key polymorphisms controlling morphological and physiological traits Chhetri, Hari B.; Macaya‐Sanz, David; Kainer, David New Phytologist, Vol. 223, Issue 1 https://doi.org/10.1111/nph.15777	journal	April 2019
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Genetic Engineering of Energy Crops to Reduce Recalcitrance and Enhance Biomass Digestibility Yadav, Monika; Paritosh, Kunwar; Chawade, Aakash Agriculture, Vol. 8, Issue 6 https://doi.org/10.3390/agriculture8060076	journal	June 2018
Immunological Approaches to Biomass Characterization and Utilization Pattathil, Sivakumar; Avci, Utku; Zhang, Tiantian Frontiers in Bioengineering and Biotechnology, Vol. 3 https://doi.org/10.3389/fbioe.2015.00173	journal	October 2015
Downregulation of pectin biosynthesis gene GAUT4 leads to reduced ferulate and lignin-carbohydrate cross-linking in switchgrass Li, Mi; Yoo, Chang Geun; Pu, Yunqiao Communications Biology, Vol. 2, Issue 1 https://doi.org/10.1038/s42003-018-0265-6	journal	January 2019
Xylan epitope profiling: an enhanced approach to study organ development-dependent changes in xylan structure, biosynthesis, and deposition in plant cell walls Peralta, Angelo G.; Venkatachalam, Sivasankari; Stone, Sydney C. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0935-5	journal	November 2017
Defining functional diversity for lignocellulose degradation in a microbial community using multi-omics studies Alessi, Anna M.; Bird, Susannah M.; Oates, Nicola C. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1164-2	journal	June 2018
Downregulating aspen xylan biosynthetic GT43 genes in developing wood stimulates growth via reprograming of the transcriptome Ratke, Christine; Terebieniec, Barbara K.; Winestrand, Sandra New Phytologist, Vol. 219, Issue 1 https://doi.org/10.1111/nph.15160	journal	April 2018
A collection of genetically engineered Populus trees reveals wood biomass traits that predict glucose yield from enzymatic hydrolysis Escamez, Sacha; Latha Gandla, Madhavi; Derba-Maceluch, Marta Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-16013-0	journal	November 2017
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High Throughput Screening Technologies in Biomass Characterization Decker, Stephen R.; Harman-Ware, Anne E.; Happs, Renee M. Frontiers in Energy Research, Vol. 6 https://doi.org/10.3389/fenrg.2018.00120	journal	November 2018
Overexpression of a Prefoldin β subunit gene reduces biomass recalcitrance in the bioenergy crop Populus Zhang, Jin; Xie, Meng; Li, Mi Plant Biotechnology Journal, Vol. 18, Issue 3 https://doi.org/10.1111/pbi.13254	journal	September 2019
Knockdown of a laccase in Populus deltoides confers altered cell wall chemistry and increased sugar release Bryan, Anthony C.; Jawdy, Sara; Gunter, Lee Plant Biotechnology Journal, Vol. 14, Issue 10 https://doi.org/10.1111/pbi.12560	journal	April 2016
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Biotechnological Strategies to Improve Plant Biomass Quality for Bioethanol Production Peña-Castro, Julián Mario; del Moral, Sandra; Núñez-López, Lizeth BioMed Research International, Vol. 2017 https://doi.org/10.1155/2017/7824076	journal	January 2017
Transgenic switchgrass ( Panicum virgatum L.) targeted for reduced recalcitrance to bioconversion: a 2-year comparative analysis of field-grown lines modified for target gene or genetic element expression Dumitrache, Alexandru; Natzke, Jace; Rodriguez, Miguel Plant Biotechnology Journal, Vol. 15, Issue 6 https://doi.org/10.1111/pbi.12666	journal	February 2017
Designer biomass for next-generation biorefineries: leveraging recent insights into xylan structure and biosynthesis Smith, Peter J.; Wang, Hsin-Tzu; York, William S. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0973-z	journal	November 2017
Suppression of PtrDUF579-3 Expression Causes Structural Changes of the Glucuronoxylan in Populus Song, Dongliang; Gui, Jinshan; Liu, Chenchen Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00493	journal	April 2016
Evaluation of Relationships between Growth Rate, Tree Size, Lignocellulose Composition, and Enzymatic Saccharification in Interspecific Corymbia Hybrids and Parental Taxa Healey, Adam L.; Lee, David J.; Lupoi, Jason S. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.01705	journal	November 2016
Saccharification Performances of Miscanthus at the Pilot and Miniaturized Assay Scales: Genotype and Year Variabilities According to the Biomass Composition Belmokhtar, Nassim; Arnoult, Stéphanie; Chabbert, Brigitte Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00740	journal	May 2017
A New Calmodulin-Binding Protein Expresses in the Context of Secondary Cell Wall Biosynthesis and Impacts Biomass Properties in Populus Badmi, Raghuram; Payyavula, Raja S.; Bali, Garima Frontiers in Plant Science, Vol. 9 https://doi.org/10.3389/fpls.2018.01669	journal	December 2018
Biomass Accumulation and Cell Wall Structure of Rice Plants Overexpressing a Dirigent-Jacalin of Sugarcane (ShDJ) Under Varying Conditions of Water Availability Andrade, Larissa Mara; Peixoto-Junior, Rafael Fávero; Ribeiro, Rafael Vasconcelos Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00065	journal	February 2019
Xylan in the Middle: Understanding Xylan Biosynthesis and Its Metabolic Dependencies Toward Improving Wood Fiber for Industrial Processing Wierzbicki, Martin P.; Maloney, Victoria; Mizrachi, Eshchar Frontiers in Plant Science, Vol. 10 https://doi.org/10.3389/fpls.2019.00176	journal	February 2019
Dynamic Changes of Pectin Epitopes in Cell Walls during the Development of the Procambium–Cambium Continuum in Poplar Liu, Jundi; Hou, Jie; Chen, Huimin International Journal of Molecular Sciences, Vol. 18, Issue 8 https://doi.org/10.3390/ijms18081716	journal	August 2017