A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.

Understanding the mechanisms triggering variation of cell wall degradability is a prerequisite to improving the energy value of lignocellulosic biomass for animal feed or biorefinery. Here, we implemented a multiscale systems approach to shed light on the genetic basis of cell wall degradability in...

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Main Authors: Clément Cuello, Aurélie Baldy, Véronique Brunaud, Johann Joets, Etienne Delannoy, Marie-Pierre Jacquemot, Lucy Botran, Yves Griveau, Cécile Guichard, Ludivine Soubigou-Taconnat, Marie-Laure Martin-Magniette, Philippe Leroy, Valérie Méchin, Matthieu Reymond, Sylvie Coursol
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2019-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0227011
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spelling doaj-63ecd0a8bd694da79b4692b2664375e02021-03-03T21:23:16ZengPublic Library of Science (PLoS)PLoS ONE1932-62032019-01-011412e022701110.1371/journal.pone.0227011A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.Clément CuelloAurélie BaldyVéronique BrunaudJohann JoetsEtienne DelannoyMarie-Pierre JacquemotLucy BotranYves GriveauCécile GuichardLudivine Soubigou-TaconnatMarie-Laure Martin-MagniettePhilippe LeroyValérie MéchinMatthieu ReymondSylvie CoursolUnderstanding the mechanisms triggering variation of cell wall degradability is a prerequisite to improving the energy value of lignocellulosic biomass for animal feed or biorefinery. Here, we implemented a multiscale systems approach to shed light on the genetic basis of cell wall degradability in maize. We demonstrated that allele replacement in two pairs of near-isogenic lines at a region encompassing a major quantitative trait locus (QTL) for cell wall degradability led to phenotypic variation of a similar magnitude and sign to that expected from a QTL analysis of cell wall degradability in the F271 × F288 recombinant inbred line progeny. Using DNA sequences within the QTL interval of both F271 and F288 inbred lines and Illumina RNA sequencing datasets from internodes of the selected near-isogenic lines, we annotated the genes present in the QTL interval and provided evidence that allelic variation at the introgressed QTL region gives rise to coordinated changes in gene expression. The identification of a gene co-expression network associated with cell wall-related trait variation revealed that the favorable F288 alleles exploit biological processes related to oxidation-reduction, regulation of hydrogen peroxide metabolism, protein folding and hormone responses. Nested in modules of co-expressed genes, potential new cell-wall regulators were identified, including two transcription factors of the group VII ethylene response factor family, that could be exploited to fine-tune cell wall degradability. Overall, these findings provide new insights into the regulatory mechanisms by which a major locus influences cell wall degradability, paving the way for its map-based cloning in maize.https://doi.org/10.1371/journal.pone.0227011
collection DOAJ
language English
format Article
sources DOAJ
author Clément Cuello
Aurélie Baldy
Véronique Brunaud
Johann Joets
Etienne Delannoy
Marie-Pierre Jacquemot
Lucy Botran
Yves Griveau
Cécile Guichard
Ludivine Soubigou-Taconnat
Marie-Laure Martin-Magniette
Philippe Leroy
Valérie Méchin
Matthieu Reymond
Sylvie Coursol
spellingShingle Clément Cuello
Aurélie Baldy
Véronique Brunaud
Johann Joets
Etienne Delannoy
Marie-Pierre Jacquemot
Lucy Botran
Yves Griveau
Cécile Guichard
Ludivine Soubigou-Taconnat
Marie-Laure Martin-Magniette
Philippe Leroy
Valérie Méchin
Matthieu Reymond
Sylvie Coursol
A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.
PLoS ONE
author_facet Clément Cuello
Aurélie Baldy
Véronique Brunaud
Johann Joets
Etienne Delannoy
Marie-Pierre Jacquemot
Lucy Botran
Yves Griveau
Cécile Guichard
Ludivine Soubigou-Taconnat
Marie-Laure Martin-Magniette
Philippe Leroy
Valérie Méchin
Matthieu Reymond
Sylvie Coursol
author_sort Clément Cuello
title A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.
title_short A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.
title_full A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.
title_fullStr A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.
title_full_unstemmed A systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.
title_sort systems biology approach uncovers a gene co-expression network associated with cell wall degradability in maize.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2019-01-01
description Understanding the mechanisms triggering variation of cell wall degradability is a prerequisite to improving the energy value of lignocellulosic biomass for animal feed or biorefinery. Here, we implemented a multiscale systems approach to shed light on the genetic basis of cell wall degradability in maize. We demonstrated that allele replacement in two pairs of near-isogenic lines at a region encompassing a major quantitative trait locus (QTL) for cell wall degradability led to phenotypic variation of a similar magnitude and sign to that expected from a QTL analysis of cell wall degradability in the F271 × F288 recombinant inbred line progeny. Using DNA sequences within the QTL interval of both F271 and F288 inbred lines and Illumina RNA sequencing datasets from internodes of the selected near-isogenic lines, we annotated the genes present in the QTL interval and provided evidence that allelic variation at the introgressed QTL region gives rise to coordinated changes in gene expression. The identification of a gene co-expression network associated with cell wall-related trait variation revealed that the favorable F288 alleles exploit biological processes related to oxidation-reduction, regulation of hydrogen peroxide metabolism, protein folding and hormone responses. Nested in modules of co-expressed genes, potential new cell-wall regulators were identified, including two transcription factors of the group VII ethylene response factor family, that could be exploited to fine-tune cell wall degradability. Overall, these findings provide new insights into the regulatory mechanisms by which a major locus influences cell wall degradability, paving the way for its map-based cloning in maize.
url https://doi.org/10.1371/journal.pone.0227011
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