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 in | The New phytologist Vol. 218; no. 1; pp. 81 - 93 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
England
New Phytologist Trust
01.04.2018
Wiley Subscription Services, Inc Wiley John Wiley and Sons Inc |
Subjects | |
Online Access | Get full text |
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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. |
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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 – name: 3 Department of Biochemistry State University of Maringá Maringá, Paraná 87020‐900 Brazil – name: 5 Programa de Processos Tecnológicos e Ambientais Universidade de Sorocaba (UNISO) Sorocaba 18060‐000 Brazil – name: 8 Department of Biochemistry University of Wisconsin Madison WI 537 USA – name: 4 Brazilian Bioethanol Science and Technology Laboratory Brazilian Center for Research in Energy and Materials Campinas, Sao Paulo 13083‐100 Brazil – 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 – name: 2 Plant Sciences Rothamsted Research Harpenden, Hertfordshire AL5 2JQ UK |
Author_xml | – sequence: 1 givenname: Wagner R. surname: Souza fullname: Souza, Wagner R. organization: Embrapa Agroenergy – sequence: 2 givenname: Polyana K. surname: Martins fullname: Martins, Polyana K. organization: Embrapa Agroenergy – sequence: 3 givenname: Jackie surname: Freeman fullname: Freeman, Jackie organization: Rothamsted Research – sequence: 4 givenname: Till K. surname: Pellny fullname: Pellny, Till K. organization: Rothamsted Research – sequence: 5 givenname: Louise V. surname: Michaelson fullname: Michaelson, Louise V. organization: Rothamsted Research – sequence: 6 givenname: Bruno L. surname: Sampaio fullname: Sampaio, Bruno L. organization: Embrapa Agroenergy – sequence: 7 givenname: Felipe surname: Vinecky fullname: Vinecky, Felipe organization: Embrapa Agroenergy – sequence: 8 givenname: Ana P. surname: Ribeiro fullname: Ribeiro, Ana P. organization: Embrapa Agroenergy – sequence: 9 givenname: Barbara A. D. B. surname: Cunha fullname: Cunha, Barbara A. D. B. organization: Embrapa Agroenergy – sequence: 10 givenname: Adilson K. surname: Kobayashi fullname: Kobayashi, Adilson K. organization: Embrapa Agroenergy – sequence: 11 givenname: Patricia A. surname: Oliveira fullname: Oliveira, Patricia A. organization: Embrapa Agroenergy – sequence: 12 givenname: Raquel B. surname: Campanha fullname: Campanha, Raquel B. organization: Embrapa Agroenergy – sequence: 13 givenname: Thályta F. surname: Pacheco fullname: Pacheco, Thályta F. organization: Embrapa Agroenergy – sequence: 14 givenname: Danielly C. I. surname: Martarello fullname: Martarello, Danielly C. I. organization: State University of Maringá – sequence: 15 givenname: Rogério surname: Marchiosi fullname: Marchiosi, Rogério organization: State University of Maringá – sequence: 16 givenname: Osvaldo surname: Ferrarese‐Filho fullname: Ferrarese‐Filho, Osvaldo organization: State University of Maringá – sequence: 17 givenname: Wanderley D. surname: Santos fullname: Santos, Wanderley D. organization: State University of Maringá – sequence: 18 givenname: Robson surname: Tramontina fullname: Tramontina, Robson organization: Brazilian Center for Research in Energy and Materials – sequence: 19 givenname: Fabio M. surname: Squina fullname: Squina, Fabio M. organization: Universidade de Sorocaba (UNISO) – sequence: 20 givenname: Danilo C. surname: Centeno fullname: Centeno, Danilo C. organization: Federal University of ABC – sequence: 21 givenname: Marília surname: Gaspar fullname: Gaspar, Marília organization: Institute of Botany – sequence: 22 givenname: Marcia R. surname: Braga fullname: Braga, Marcia R. organization: Institute of Botany – sequence: 23 givenname: Marco A. S. surname: Tiné fullname: Tiné, Marco A. S. organization: Institute of Botany – sequence: 24 givenname: John surname: Ralph fullname: Ralph, John organization: University of Wisconsin – sequence: 25 givenname: Rowan A. C. orcidid: 0000-0002-1412-8828 surname: Mitchell fullname: Mitchell, Rowan A. C. email: rowan.mitchell@rothamsted.ac.uk organization: Rothamsted Research – sequence: 26 givenname: Hugo B. C. surname: Molinari fullname: Molinari, Hugo B. C. email: hugo.molinari@embrapa.br organization: Embrapa Agroenergy |
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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ContentType | Journal Article |
Copyright | Copyright © 2018 New Phytologist Trust 2017 The Authors. New Phytologist © 2017 New Phytologist Trust 2017 The Authors. New Phytologist © 2017 New Phytologist Trust. |
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CorporateAuthor | Univ. of Wisconsin, Madison, WI (United States) |
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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 . ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23) FC02-07ER64494 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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References | 2010; 59 2013; 4 2012; 287 1997; 44 2007; 144 2004; 161 2004; 3 2010; 463 2008; 6 2013; 161 2017; 114 2010; 61 2010; 26 2014; 3 2013; 11 2013; 10 2004; 39 2008; 27 2010; 231 2014; 9 2017; 246 1992; 1 2006; 125 2010; 9 2010; 8 2015; 13 1990; 30 2015; 6 2012 1994; 193 1998 2016; 243 1995; 275 2014; 111 1995; 272 2012; 109 2012; 30 1998a; 77 2016; 6 1997; 127 2016; 2 2017; 15 2013; 73 1993; 11 1998b; 78 2017; 18 2012; 158 2009; 2 2016; 170 2003; 64 2014; 78 2014; 77 2012; 40 e_1_2_7_5_1 e_1_2_7_3_1 e_1_2_7_9_1 e_1_2_7_7_1 e_1_2_7_19_1 e_1_2_7_17_1 e_1_2_7_15_1 e_1_2_7_41_1 e_1_2_7_13_1 e_1_2_7_43_1 e_1_2_7_11_1 e_1_2_7_45_1 e_1_2_7_47_1 e_1_2_7_26_1 e_1_2_7_49_1 e_1_2_7_50_1 e_1_2_7_25_1 e_1_2_7_31_1 e_1_2_7_52_1 e_1_2_7_23_1 e_1_2_7_33_1 e_1_2_7_54_1 e_1_2_7_21_1 e_1_2_7_35_1 e_1_2_7_56_1 e_1_2_7_37_1 e_1_2_7_58_1 e_1_2_7_39_1 e_1_2_7_6_1 e_1_2_7_4_1 e_1_2_7_8_1 e_1_2_7_18_1 e_1_2_7_16_1 e_1_2_7_40_1 e_1_2_7_2_1 e_1_2_7_14_1 e_1_2_7_42_1 e_1_2_7_12_1 e_1_2_7_44_1 e_1_2_7_10_1 e_1_2_7_46_1 e_1_2_7_48_1 e_1_2_7_27_1 e_1_2_7_29_1 Martins PK (e_1_2_7_28_1) 2016; 6 e_1_2_7_51_1 e_1_2_7_30_1 e_1_2_7_53_1 e_1_2_7_24_1 e_1_2_7_32_1 e_1_2_7_55_1 e_1_2_7_22_1 e_1_2_7_34_1 e_1_2_7_57_1 e_1_2_7_20_1 e_1_2_7_36_1 e_1_2_7_38_1 29488282 - New Phytol. 2018 Apr;218(1):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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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 |
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