Suppression of a single BAHD gene in Setaria viridis causes large, stable decreases in cell wall feruloylation and increases biomass digestibility

Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identif...

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Published inThe New phytologist Vol. 218; no. 1; pp. 81 - 93
Main Authors Souza, Wagner R., Martins, Polyana K., Freeman, Jackie, Pellny, Till K., Michaelson, Louise V., Sampaio, Bruno L., Vinecky, Felipe, Ribeiro, Ana P., Cunha, Barbara A. D. B., Kobayashi, Adilson K., Oliveira, Patricia A., Campanha, Raquel B., Pacheco, Thályta F., Martarello, Danielly C. I., Marchiosi, Rogério, Ferrarese‐Filho, Osvaldo, Santos, Wanderley D., Tramontina, Robson, Squina, Fabio M., Centeno, Danilo C., Gaspar, Marília, Braga, Marcia R., Tiné, Marco A. S., Ralph, John, Mitchell, Rowan A. C., Molinari, Hugo B. C.
Format Journal Article
LanguageEnglish
Published England New Phytologist Trust 01.04.2018
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Abstract Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identified within the BAHD acyl-CoA transferase family. We used RNA interference (RNAi) silencing of orthologs in the model grasses Setaria viridis (SvBAHD01) and Brachypodium distachyon (BdBAHD01) and determined effects on AX feruloylation. Silencing of SvBAHD01 in Setaria resulted in a c. 60% decrease in AX feruloylation in stems consistently across four generations. Silencing of BdBAHD01 in Brachypodium stems decreased feruloylation much less, possibly due to higher expression of functionally redundant genes. Setaria SvBAHD01 RNAi plants showed: no decrease in total lignin, approximately doubled arabinose acylated by p-coumarate, changes in two-dimensional NMR spectra of unfractionated cell walls consistent with biochemical estimates, no effect on total biomass production and an increase in biomass saccharification efficiency of 40–60%. We provide the first strong evidence for a key role of the BAHD01 gene in AX feruloylation and demonstrate that it is a promising target for improvement of grass crops for biofuel, biorefining and animal nutrition applications.
AbstractList Feruloylation of arabinoxylan ( AX ) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identified within the BAHD acyl‐CoA transferase family. We used RNA interference (RNAi) silencing of orthologs in the model grasses Setaria viridis ( Sv BAHD 01 ) and Brachypodium distachyon ( Bd BAHD 01 ) and determined effects on AX feruloylation. Silencing of Sv BAHD 01 in Setaria resulted in a c . 60% decrease in AX feruloylation in stems consistently across four generations. Silencing of Bd BAHD 01 in Brachypodium stems decreased feruloylation much less, possibly due to higher expression of functionally redundant genes. Setaria Sv BAHD 01 RNA i plants showed: no decrease in total lignin, approximately doubled arabinose acylated by p ‐coumarate, changes in two‐dimensional NMR spectra of unfractionated cell walls consistent with biochemical estimates, no effect on total biomass production and an increase in biomass saccharification efficiency of 40–60%. We provide the first strong evidence for a key role of the BAHD 01 gene in AX feruloylation and demonstrate that it is a promising target for improvement of grass crops for biofuel, biorefining and animal nutrition applications. See also the Commentary on this article by Gómez & McQueen‐Mason, 218 : 5–7 .
Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identified within the BAHD acyl-CoA transferase family. We used RNA interference (RNAi) silencing of orthologs in the model grasses Setaria viridis (SvBAHD01) and Brachypodium distachyon (BdBAHD01) and determined effects on AX feruloylation. Silencing of SvBAHD01 in Setaria resulted in a c. 60% decrease in AX feruloylation in stems consistently across four generations. Silencing of BdBAHD01 in Brachypodium stems decreased feruloylation much less, possibly due to higher expression of functionally redundant genes. Setaria SvBAHD01 RNAi plants showed: no decrease in total lignin, approximately doubled arabinose acylated by p-coumarate, changes in two-dimensional NMR spectra of unfractionated cell walls consistent with biochemical estimates, no effect on total biomass production and an increase in biomass saccharification efficiency of 40-60%. We provide the first strong evidence for a key role of the BAHD01 gene in AX feruloylation and demonstrate that it is a promising target for improvement of grass crops for biofuel, biorefining and animal nutrition applications.
Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identified within the BAHD acyl-CoA transferase family. We used RNA interference (RNAi) silencing of orthologs in the model grasses Setaria viridis (SvBAHD01) and Brachypodium distachyon (BdBAHD01) and determined effects on AX feruloylation. Silencing of SvBAHD01 in Setaria resulted in a c. 60% decrease in AX feruloylation in stems consistently across four generations. Silencing of BdBAHD01 in Brachypodium stems decreased feruloylation much less, possibly due to higher expression of functionally redundant genes. Setaria SvBAHD01 RNAi plants showed: no decrease in total lignin, approximately doubled arabinose acylated by p-coumarate, changes in two-dimensional NMR spectra of unfractionated cell walls consistent with biochemical estimates, no effect on total biomass production and an increase in biomass saccharification efficiency of 40-60%. We provide the first strong evidence for a key role of the BAHD01 gene in AX feruloylation and demonstrate that it is a promising target for improvement of grass crops for biofuel, biorefining and animal nutrition applications.Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identified within the BAHD acyl-CoA transferase family. We used RNA interference (RNAi) silencing of orthologs in the model grasses Setaria viridis (SvBAHD01) and Brachypodium distachyon (BdBAHD01) and determined effects on AX feruloylation. Silencing of SvBAHD01 in Setaria resulted in a c. 60% decrease in AX feruloylation in stems consistently across four generations. Silencing of BdBAHD01 in Brachypodium stems decreased feruloylation much less, possibly due to higher expression of functionally redundant genes. Setaria SvBAHD01 RNAi plants showed: no decrease in total lignin, approximately doubled arabinose acylated by p-coumarate, changes in two-dimensional NMR spectra of unfractionated cell walls consistent with biochemical estimates, no effect on total biomass production and an increase in biomass saccharification efficiency of 40-60%. We provide the first strong evidence for a key role of the BAHD01 gene in AX feruloylation and demonstrate that it is a promising target for improvement of grass crops for biofuel, biorefining and animal nutrition applications.
Summary Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identified within the BAHD acyl‐CoA transferase family. We used RNA interference (RNAi) silencing of orthologs in the model grasses Setaria viridis (SvBAHD01) and Brachypodium distachyon (BdBAHD01) and determined effects on AX feruloylation. Silencing of SvBAHD01 in Setaria resulted in a c. 60% decrease in AX feruloylation in stems consistently across four generations. Silencing of BdBAHD01 in Brachypodium stems decreased feruloylation much less, possibly due to higher expression of functionally redundant genes. Setaria SvBAHD01 RNAi plants showed: no decrease in total lignin, approximately doubled arabinose acylated by p‐coumarate, changes in two‐dimensional NMR spectra of unfractionated cell walls consistent with biochemical estimates, no effect on total biomass production and an increase in biomass saccharification efficiency of 40–60%. We provide the first strong evidence for a key role of the BAHD01 gene in AX feruloylation and demonstrate that it is a promising target for improvement of grass crops for biofuel, biorefining and animal nutrition applications. See also the Commentary on this article by Gómez & McQueen‐Mason, 218: 5–7.
Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass crops, and of interest in grass evolution. Definitive evidence on the genes responsible is lacking so we studied a candidate gene that we identified within the BAHD acyl-CoA transferase family. We used RNA interference (RNAi) silencing of orthologs in the model grasses Setaria viridis (SvBAHD01) and Brachypodium distachyon (BdBAHD01) and determined effects on AX feruloylation. Silencing of SvBAHD01 in Setaria resulted in a c. 60% decrease in AX feruloylation in stems consistently across four generations. Silencing of BdBAHD01 in Brachypodium stems decreased feruloylation much less, possibly due to higher expression of functionally redundant genes. Setaria SvBAHD01 RNAi plants showed: no decrease in total lignin, approximately doubled arabinose acylated by p-coumarate, changes in two-dimensional NMR spectra of unfractionated cell walls consistent with biochemical estimates, no effect on total biomass production and an increase in biomass saccharification efficiency of 40–60%. We provide the first strong evidence for a key role of the BAHD01 gene in AX feruloylation and demonstrate that it is a promising target for improvement of grass crops for biofuel, biorefining and animal nutrition applications.
Author Jackie Freeman
Raquel B. Campanha
Bruno L. Sampaio
Osvaldo Ferrarese-Filho
Wagner R. de Souza
Rowan A. C. Mitchell
Marco A. S. Tiné
Barbara A. D. B. da Cunha
Marília Gaspar
Robson Tramontina
Danielly C. I. Martarello
Rogério Marchiosi
John Ralph
Adilson K. Kobayashi
Ana P. Ribeiro
Polyana K. Martins
Felipe Vinecky
Wanderley D. dos Santos
Hugo B. C. Molinari
Louise V. Michaelson
Patricia A. de Oliveira
Fabio M. Squina
Till K. Pellny
Thályta F. Pacheco
Danilo C. Centeno
Marcia R. Braga
AuthorAffiliation 9 Department of Energy's Great Lakes Bioenergy Research Center Wisconsin Energy Institute University of Wisconsin Madison WI 537 USA
5 Programa de Processos Tecnológicos e Ambientais Universidade de Sorocaba (UNISO) Sorocaba 18060‐000 Brazil
2 Plant Sciences Rothamsted Research Harpenden, Hertfordshire AL5 2JQ UK
4 Brazilian Bioethanol Science and Technology Laboratory Brazilian Center for Research in Energy and Materials Campinas, Sao Paulo 13083‐100 Brazil
8 Department of Biochemistry University of Wisconsin Madison WI 537 USA
1 Embrapa Agroenergy Brasília DF 70770901 Brazil
7 Department of Plant Physiology and Biochemistry Institute of Botany Sao Paulo 04301‐012, 04301‐902 Brazil
3 Department of Biochemistry State University of Maringá Maringá, Paraná 87020‐900 Brazil
6 Centre of Natural Sciences and Humanities Federal University of ABC São Bernardo do Campo SP 09606‐045 Brazil
AuthorAffiliation_xml – name: 1 Embrapa Agroenergy Brasília DF 70770901 Brazil
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– name: 6 Centre of Natural Sciences and Humanities Federal University of ABC São Bernardo do Campo SP 09606‐045 Brazil
– name: 9 Department of Energy's Great Lakes Bioenergy Research Center Wisconsin Energy Institute University of Wisconsin Madison WI 537 USA
– name: 7 Department of Plant Physiology and Biochemistry Institute of Botany Sao Paulo 04301‐012, 04301‐902 Brazil
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29315591$$D View this record in MEDLINE/PubMed
https://www.osti.gov/servlets/purl/1500216$$D View this record in Osti.gov
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2017 The Authors. New Phytologist © 2017 New Phytologist Trust
2017 The Authors. New Phytologist © 2017 New Phytologist Trust.
Copyright_xml – notice: Copyright © 2018 New Phytologist Trust
– notice: 2017 The Authors. New Phytologist © 2017 New Phytologist Trust
– notice: 2017 The Authors. New Phytologist © 2017 New Phytologist Trust.
CorporateAuthor Univ. of Wisconsin, Madison, WI (United States)
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Issue 1
Keywords grass evolution
lignocellulosic feedstock
cell wall acylation
ferulic acid
hydroxycinnamates
Language English
License Attribution
http://creativecommons.org/licenses/by/4.0
2017 The Authors. New Phytologist © 2017 New Phytologist Trust.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
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Notes 218
5–7
Gómez & McQueen‐Mason
See also the Commentary on this article by
.
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USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
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These authors contributed equally to this work.
See also the Commentary on this article by Gómez & McQueen‐Mason, 218: 5–7.
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Snippet Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass...
Summary Feruloylation of arabinoxylan (AX) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of...
Feruloylation of arabinoxylan ( AX ) in grass cell walls is a key determinant of recalcitrance to enzyme attack, making it a target for improvement of grass...
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StartPage 81
SubjectTerms AC generators
acyl coenzyme A
Animal nutrition
Arabinose
arabinoxylan
BASIC BIOLOGICAL SCIENCES
Biofuels
Biological evolution
Biomass
biomass production
biorefining
Brachypodium distachyon
cell wall acylation
Cell walls
CoA transferase
Crops
Digestibility
Dimensional changes
evolution
Evolutionary genetics
ferulic acid
Gene expression
Genes
grass evolution
Grasses
hydroxycinnamates
Lignin
lignocellulosic feedstock
NMR
Nuclear magnetic resonance
nuclear magnetic resonance spectroscopy
Nucleic acids
Nutrition
Ribonucleic acid
RNA
RNA interference
RNA-mediated interference
Saccharification
Setaria
Setaria viridis
Stems
transferases
Title Suppression of a single BAHD gene in Setaria viridis causes large, stable decreases in cell wall feruloylation and increases biomass digestibility
URI https://www.jstor.org/stable/90019617
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fnph.14970
https://www.ncbi.nlm.nih.gov/pubmed/29315591
https://www.proquest.com/docview/2008710565
https://www.proquest.com/docview/1989557173
https://www.proquest.com/docview/2067309964
https://www.osti.gov/servlets/purl/1500216
https://pubmed.ncbi.nlm.nih.gov/PMC5873385
Volume 218
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