Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyon
Abstract Background Hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase (HCT) is a central enzyme of the so-called “esters” pathway to monolignols. As originally envisioned, HCT functions twice in this pathway, to form coumaroyl shikimate and then, in the “reverse” direction, to convert caf...
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doaj-8d288122d7754353a1e447272c92ce442021-03-11T12:49:52ZengBMCBiotechnology for Biofuels1754-68342021-02-0114111710.1186/s13068-021-01905-1Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyonJuan Carlos Serrani-Yarce0Luis Escamilla-Trevino1Jaime Barros2Lina Gallego-Giraldo3Yunqiao Pu4Art Ragauskas5Richard A. Dixon6BioDiscovery Institute and Department of Biological Sciences, University of North TexasBioDiscovery Institute and Department of Biological Sciences, University of North TexasBioDiscovery Institute and Department of Biological Sciences, University of North TexasBioDiscovery Institute and Department of Biological Sciences, University of North TexasBioEnergy Science Center (BESC), Oak Ridge National LaboratoryBioEnergy Science Center (BESC), Oak Ridge National LaboratoryBioDiscovery Institute and Department of Biological Sciences, University of North TexasAbstract Background Hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase (HCT) is a central enzyme of the so-called “esters” pathway to monolignols. As originally envisioned, HCT functions twice in this pathway, to form coumaroyl shikimate and then, in the “reverse” direction, to convert caffeoyl shikimate to caffeoyl CoA. The discovery of a caffeoyl shikimate esterase (CSE) that forms caffeic acid directly from caffeoyl shikimate calls into question the need for the reverse HCT reaction in lignin biosynthesis. Loss of function of HCT gives severe growth phenotypes in several dicot plants, but less so in some monocots, questioning whether this enzyme, and therefore the shikimate shunt, plays the same role in both monocots and dicots. The model grass Brachypodium distachyon has two HCT genes, but lacks a classical CSE gene. This study was therefore conducted to evaluate the utility of HCT as a target for lignin modification in a species with an “incomplete” shikimate shunt. Results The kinetic properties of recombinant B. distachyon HCTs were compared with those from Arabidopsis thaliana, Medicago truncatula, and Panicum virgatum (switchgrass) for both the forward and reverse reactions. Along with two M. truncatula HCTs, B. distachyon HCT2 had the least kinetically unfavorable reverse HCT reaction, and this enzyme is induced when HCT1 is down-regulated. Down regulation of B. distachyon HCT1, or co-down-regulation of HCT1 and HCT2, by RNA interference led to reduced lignin levels, with only modest changes in lignin composition and molecular weight. Conclusions Down-regulation of HCT1, or co-down-regulation of both HCT genes, in B. distachyon results in less extensive changes in lignin content/composition and cell wall structure than observed following HCT down-regulation in dicots, with little negative impact on biomass yield. Nevertheless, HCT down-regulation leads to significant improvements in biomass saccharification efficiency, making this gene a preferred target for biotechnological improvement of grasses for bioprocessing.https://doi.org/10.1186/s13068-021-01905-1Lignin modificationPhenylpropanoid biosynthesisSaccharification efficiencyRNA interferenceMonocotNMR analysis |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Juan Carlos Serrani-Yarce Luis Escamilla-Trevino Jaime Barros Lina Gallego-Giraldo Yunqiao Pu Art Ragauskas Richard A. Dixon |
spellingShingle |
Juan Carlos Serrani-Yarce Luis Escamilla-Trevino Jaime Barros Lina Gallego-Giraldo Yunqiao Pu Art Ragauskas Richard A. Dixon Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyon Biotechnology for Biofuels Lignin modification Phenylpropanoid biosynthesis Saccharification efficiency RNA interference Monocot NMR analysis |
author_facet |
Juan Carlos Serrani-Yarce Luis Escamilla-Trevino Jaime Barros Lina Gallego-Giraldo Yunqiao Pu Art Ragauskas Richard A. Dixon |
author_sort |
Juan Carlos Serrani-Yarce |
title |
Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyon |
title_short |
Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyon |
title_full |
Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyon |
title_fullStr |
Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyon |
title_full_unstemmed |
Targeting hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase for lignin modification in Brachypodium distachyon |
title_sort |
targeting hydroxycinnamoyl coa: shikimate hydroxycinnamoyl transferase for lignin modification in brachypodium distachyon |
publisher |
BMC |
series |
Biotechnology for Biofuels |
issn |
1754-6834 |
publishDate |
2021-02-01 |
description |
Abstract Background Hydroxycinnamoyl CoA: shikimate hydroxycinnamoyl transferase (HCT) is a central enzyme of the so-called “esters” pathway to monolignols. As originally envisioned, HCT functions twice in this pathway, to form coumaroyl shikimate and then, in the “reverse” direction, to convert caffeoyl shikimate to caffeoyl CoA. The discovery of a caffeoyl shikimate esterase (CSE) that forms caffeic acid directly from caffeoyl shikimate calls into question the need for the reverse HCT reaction in lignin biosynthesis. Loss of function of HCT gives severe growth phenotypes in several dicot plants, but less so in some monocots, questioning whether this enzyme, and therefore the shikimate shunt, plays the same role in both monocots and dicots. The model grass Brachypodium distachyon has two HCT genes, but lacks a classical CSE gene. This study was therefore conducted to evaluate the utility of HCT as a target for lignin modification in a species with an “incomplete” shikimate shunt. Results The kinetic properties of recombinant B. distachyon HCTs were compared with those from Arabidopsis thaliana, Medicago truncatula, and Panicum virgatum (switchgrass) for both the forward and reverse reactions. Along with two M. truncatula HCTs, B. distachyon HCT2 had the least kinetically unfavorable reverse HCT reaction, and this enzyme is induced when HCT1 is down-regulated. Down regulation of B. distachyon HCT1, or co-down-regulation of HCT1 and HCT2, by RNA interference led to reduced lignin levels, with only modest changes in lignin composition and molecular weight. Conclusions Down-regulation of HCT1, or co-down-regulation of both HCT genes, in B. distachyon results in less extensive changes in lignin content/composition and cell wall structure than observed following HCT down-regulation in dicots, with little negative impact on biomass yield. Nevertheless, HCT down-regulation leads to significant improvements in biomass saccharification efficiency, making this gene a preferred target for biotechnological improvement of grasses for bioprocessing. |
topic |
Lignin modification Phenylpropanoid biosynthesis Saccharification efficiency RNA interference Monocot NMR analysis |
url |
https://doi.org/10.1186/s13068-021-01905-1 |
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