Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor

Abstract Background The development of bioenergy crops with reduced recalcitrance to enzymatic degradation represents an important challenge to enable the sustainable production of advanced biofuels and bioproducts. Biomass recalcitrance is partly attributed to the complex structure of plant cell wa...

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Autores principales: Yang Tian, Chien-Yuan Lin, Joon-Hyun Park, Chuan-Yin Wu, Ramu Kakumanu, Venkataramana R. Pidatala, Khanh M. Vuu, Alberto Rodriguez, Patrick M. Shih, Edward E. K. Baidoo, Stephen Temple, Blake A. Simmons, John M. Gladden, Henrik V. Scheller, Aymerick Eudes
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spelling oai:doaj.org-article:d3ff27bdda604632aaf7f10e8a8282cd2021-11-21T12:25:38ZOverexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor10.1186/s13068-021-02068-91754-6834https://doaj.org/article/d3ff27bdda604632aaf7f10e8a8282cd2021-11-01T00:00:00Zhttps://doi.org/10.1186/s13068-021-02068-9https://doaj.org/toc/1754-6834Abstract Background The development of bioenergy crops with reduced recalcitrance to enzymatic degradation represents an important challenge to enable the sustainable production of advanced biofuels and bioproducts. Biomass recalcitrance is partly attributed to the complex structure of plant cell walls inside which cellulose microfibrils are protected by a network of hemicellulosic xylan chains that crosslink with each other or with lignin via ferulate (FA) bridges. Overexpression of the rice acyltransferase OsAT10 is an effective bioengineering strategy to lower the amount of FA involved in the formation of cell wall crosslinks and thereby reduce cell wall recalcitrance. The annual crop sorghum represents an attractive feedstock for bioenergy purposes considering its high biomass yields and low input requirements. Although we previously validated the OsAT10 engineering approach in the perennial bioenergy crop switchgrass, the effect of OsAT10 expression on biomass composition and digestibility in sorghum remains to be explored. Results We obtained eight independent sorghum (Sorghum bicolor (L.) Moench) transgenic lines with a single copy of a construct designed for OsAT10 expression. Consistent with the proposed role of OsAT10 in acylating arabinosyl residues on xylan with p-coumarate (pCA), a higher amount of p-coumaroyl-arabinose was released from the cell walls of these lines upon hydrolysis with trifluoroacetic acid. However, no major changes were observed regarding the total amount of pCA or FA esters released from cell walls upon mild alkaline hydrolysis. Certain diferulate (diFA) isomers identified in alkaline hydrolysates were increased in some transgenic lines. The amount of the main cell wall monosaccharides glucose, xylose, and arabinose was unaffected. The transgenic lines showed reduced lignin content and their biomass released higher yields of sugars after ionic liquid pretreatment followed by enzymatic saccharification. Conclusions Expression of OsAT10 in sorghum leads to an increase of xylan-bound pCA without reducing the overall content of cell wall FA esters. Nevertheless, the amount of total cell wall pCA remains unchanged indicating that most pCA is ester-linked to lignin. Unlike other engineered plants overexpressing OsAT10 or a phylogenetically related acyltransferase with similar putative function, the improvements of biomass saccharification efficiency in sorghum OsAT10 lines are likely the result of lignin reductions rather than reductions of cell wall-bound FA. These results also suggest a relationship between xylan-bound pCA and lignification in cell walls.Yang TianChien-Yuan LinJoon-Hyun ParkChuan-Yin WuRamu KakumanuVenkataramana R. PidatalaKhanh M. VuuAlberto RodriguezPatrick M. ShihEdward E. K. BaidooStephen TempleBlake A. SimmonsJohn M. GladdenHenrik V. SchellerAymerick EudesBMCarticleSorghumBioenergyLigninXylanFerulatep-CoumarateFuelTP315-360BiotechnologyTP248.13-248.65ENBiotechnology for Biofuels, Vol 14, Iss 1, Pp 1-9 (2021)
institution DOAJ
collection DOAJ
language EN
topic Sorghum
Bioenergy
Lignin
Xylan
Ferulate
p-Coumarate
Fuel
TP315-360
Biotechnology
TP248.13-248.65
spellingShingle Sorghum
Bioenergy
Lignin
Xylan
Ferulate
p-Coumarate
Fuel
TP315-360
Biotechnology
TP248.13-248.65
Yang Tian
Chien-Yuan Lin
Joon-Hyun Park
Chuan-Yin Wu
Ramu Kakumanu
Venkataramana R. Pidatala
Khanh M. Vuu
Alberto Rodriguez
Patrick M. Shih
Edward E. K. Baidoo
Stephen Temple
Blake A. Simmons
John M. Gladden
Henrik V. Scheller
Aymerick Eudes
Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor
description Abstract Background The development of bioenergy crops with reduced recalcitrance to enzymatic degradation represents an important challenge to enable the sustainable production of advanced biofuels and bioproducts. Biomass recalcitrance is partly attributed to the complex structure of plant cell walls inside which cellulose microfibrils are protected by a network of hemicellulosic xylan chains that crosslink with each other or with lignin via ferulate (FA) bridges. Overexpression of the rice acyltransferase OsAT10 is an effective bioengineering strategy to lower the amount of FA involved in the formation of cell wall crosslinks and thereby reduce cell wall recalcitrance. The annual crop sorghum represents an attractive feedstock for bioenergy purposes considering its high biomass yields and low input requirements. Although we previously validated the OsAT10 engineering approach in the perennial bioenergy crop switchgrass, the effect of OsAT10 expression on biomass composition and digestibility in sorghum remains to be explored. Results We obtained eight independent sorghum (Sorghum bicolor (L.) Moench) transgenic lines with a single copy of a construct designed for OsAT10 expression. Consistent with the proposed role of OsAT10 in acylating arabinosyl residues on xylan with p-coumarate (pCA), a higher amount of p-coumaroyl-arabinose was released from the cell walls of these lines upon hydrolysis with trifluoroacetic acid. However, no major changes were observed regarding the total amount of pCA or FA esters released from cell walls upon mild alkaline hydrolysis. Certain diferulate (diFA) isomers identified in alkaline hydrolysates were increased in some transgenic lines. The amount of the main cell wall monosaccharides glucose, xylose, and arabinose was unaffected. The transgenic lines showed reduced lignin content and their biomass released higher yields of sugars after ionic liquid pretreatment followed by enzymatic saccharification. Conclusions Expression of OsAT10 in sorghum leads to an increase of xylan-bound pCA without reducing the overall content of cell wall FA esters. Nevertheless, the amount of total cell wall pCA remains unchanged indicating that most pCA is ester-linked to lignin. Unlike other engineered plants overexpressing OsAT10 or a phylogenetically related acyltransferase with similar putative function, the improvements of biomass saccharification efficiency in sorghum OsAT10 lines are likely the result of lignin reductions rather than reductions of cell wall-bound FA. These results also suggest a relationship between xylan-bound pCA and lignification in cell walls.
format article
author Yang Tian
Chien-Yuan Lin
Joon-Hyun Park
Chuan-Yin Wu
Ramu Kakumanu
Venkataramana R. Pidatala
Khanh M. Vuu
Alberto Rodriguez
Patrick M. Shih
Edward E. K. Baidoo
Stephen Temple
Blake A. Simmons
John M. Gladden
Henrik V. Scheller
Aymerick Eudes
author_facet Yang Tian
Chien-Yuan Lin
Joon-Hyun Park
Chuan-Yin Wu
Ramu Kakumanu
Venkataramana R. Pidatala
Khanh M. Vuu
Alberto Rodriguez
Patrick M. Shih
Edward E. K. Baidoo
Stephen Temple
Blake A. Simmons
John M. Gladden
Henrik V. Scheller
Aymerick Eudes
author_sort Yang Tian
title Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor
title_short Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor
title_full Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor
title_fullStr Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor
title_full_unstemmed Overexpression of the rice BAHD acyltransferase AT10 increases xylan-bound p-coumarate and reduces lignin in Sorghum bicolor
title_sort overexpression of the rice bahd acyltransferase at10 increases xylan-bound p-coumarate and reduces lignin in sorghum bicolor
publisher BMC
publishDate 2021
url https://doaj.org/article/d3ff27bdda604632aaf7f10e8a8282cd
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