Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin Composition

Arabidopsis thaliana transcription factors belonging to the ERFIIId and ERFIIIe subclade (ERFIIId/e) of the APETALA 2/ethylene response factor (AP2/ERF) family enhance primary cell wall (PCW) formation. These transcription factors activate expression of genes encoding PCW-type cellulose synthase (CE...

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Main Authors: Miyuki T. Nakata, Shingo Sakamoto, Nuoendagula, Shinya Kajita, Nobutaka Mitsuda
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.654655/full
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author Miyuki T. Nakata
Shingo Sakamoto
Shingo Sakamoto
Nuoendagula
Shinya Kajita
Nobutaka Mitsuda
Nobutaka Mitsuda
author_facet Miyuki T. Nakata
Shingo Sakamoto
Shingo Sakamoto
Nuoendagula
Shinya Kajita
Nobutaka Mitsuda
Nobutaka Mitsuda
author_sort Miyuki T. Nakata
collection DOAJ
description Arabidopsis thaliana transcription factors belonging to the ERFIIId and ERFIIIe subclade (ERFIIId/e) of the APETALA 2/ethylene response factor (AP2/ERF) family enhance primary cell wall (PCW) formation. These transcription factors activate expression of genes encoding PCW-type cellulose synthase (CESA) subunits and other genes for PCW biosynthesis. In this study, we show that fiber-specific expression of ERF035-VP16 and ERF041-VP16, which are VP16-fused proteins of ERFIIId/e members, promote cell wall thickening in a wild-type background with a concomitant increase of alcohol insoluble residues (cell wall content) per fresh weight (FW) and monosaccharides related to the PCW without affecting plant growth. Furthermore, in the ERF041-VP16 lines, the total amount of lignin and the syringyl (S)/guaiacyl (G) ratio decreased, and the enzymatic saccharification yield of glucose from cellulose per fresh weight improved. In these lines, PCW-type CESA genes were upregulated and ferulate 5-hydropxylase1 (F5H1), which is necessary for production of the S unit lignin, was downregulated. In addition, various changes in the expression levels of transcription factors regulating secondary cell wall (SCW) formation were observed. In conclusion, fiber cell-specific ERF041-VP16 improves biomass yield, increases PCW components, and alters lignin composition and deposition and may be suitable for use in future molecular breeding programs of biomass crops.
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spelling doaj.art-8c6722724f3f4c9fb9dd6d0613af58e12022-12-21T23:06:09ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-04-011210.3389/fpls.2021.654655654655Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin CompositionMiyuki T. Nakata0Shingo Sakamoto1Shingo Sakamoto2 Nuoendagula3Shinya Kajita4Nobutaka Mitsuda5Nobutaka Mitsuda6Plant Gene Regulation Research Group, Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, JapanPlant Gene Regulation Research Group, Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, JapanSmart CO2 Utilization Research Team, Global Zero Emission Research Center, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, JapanGraduate School of Bio-Applications and Systems Engineering (BASE), Tokyo University of Agriculture and Technology (TUAT), Koganei, JapanGraduate School of Bio-Applications and Systems Engineering (BASE), Tokyo University of Agriculture and Technology (TUAT), Koganei, JapanPlant Gene Regulation Research Group, Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, JapanSmart CO2 Utilization Research Team, Global Zero Emission Research Center, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, JapanArabidopsis thaliana transcription factors belonging to the ERFIIId and ERFIIIe subclade (ERFIIId/e) of the APETALA 2/ethylene response factor (AP2/ERF) family enhance primary cell wall (PCW) formation. These transcription factors activate expression of genes encoding PCW-type cellulose synthase (CESA) subunits and other genes for PCW biosynthesis. In this study, we show that fiber-specific expression of ERF035-VP16 and ERF041-VP16, which are VP16-fused proteins of ERFIIId/e members, promote cell wall thickening in a wild-type background with a concomitant increase of alcohol insoluble residues (cell wall content) per fresh weight (FW) and monosaccharides related to the PCW without affecting plant growth. Furthermore, in the ERF041-VP16 lines, the total amount of lignin and the syringyl (S)/guaiacyl (G) ratio decreased, and the enzymatic saccharification yield of glucose from cellulose per fresh weight improved. In these lines, PCW-type CESA genes were upregulated and ferulate 5-hydropxylase1 (F5H1), which is necessary for production of the S unit lignin, was downregulated. In addition, various changes in the expression levels of transcription factors regulating secondary cell wall (SCW) formation were observed. In conclusion, fiber cell-specific ERF041-VP16 improves biomass yield, increases PCW components, and alters lignin composition and deposition and may be suitable for use in future molecular breeding programs of biomass crops.https://www.frontiersin.org/articles/10.3389/fpls.2021.654655/fullArabidopsis thalianaERFIIId/e transcription factorsprimary cell wallfiber cellligninsyringyl (S)/guaiacyl (G) ratio
spellingShingle Miyuki T. Nakata
Shingo Sakamoto
Shingo Sakamoto
Nuoendagula
Shinya Kajita
Nobutaka Mitsuda
Nobutaka Mitsuda
Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin Composition
Frontiers in Plant Science
Arabidopsis thaliana
ERFIIId/e transcription factors
primary cell wall
fiber cell
lignin
syringyl (S)/guaiacyl (G) ratio
title Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin Composition
title_full Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin Composition
title_fullStr Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin Composition
title_full_unstemmed Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin Composition
title_short Fiber Cell-Specific Expression of the VP16-Fused Ethylene Response Factor 41 Protein Increases Biomass Yield and Alters Lignin Composition
title_sort fiber cell specific expression of the vp16 fused ethylene response factor 41 protein increases biomass yield and alters lignin composition
topic Arabidopsis thaliana
ERFIIId/e transcription factors
primary cell wall
fiber cell
lignin
syringyl (S)/guaiacyl (G) ratio
url https://www.frontiersin.org/articles/10.3389/fpls.2021.654655/full
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