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

PLoS One. 2019 Dec 31;14(12):e0227011. doi: 10.1371/journal.pone.0227011. eCollection 2019.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alleles
  • Animal Feed*
  • Cell Wall / genetics
  • Cell Wall / metabolism*
  • Cellulose / metabolism
  • Chromosome Mapping
  • Datasets as Topic
  • Gene Regulatory Networks*
  • Genome, Plant
  • Hydrogen Peroxide / metabolism
  • Lignin / metabolism
  • Oxidation-Reduction
  • Plant Breeding
  • Plants, Genetically Modified
  • Protein Folding
  • Quantitative Trait Loci*
  • RNA-Seq
  • Systems Biology
  • Zea mays / cytology
  • Zea mays / genetics*

Substances

  • Cellulose
  • Lignin
  • Hydrogen Peroxide

Grants and funding

This research was supported by grants from ProMaïs (ZeaWall II project to MR) and the French Government (LabEx Saclay Plant Sciences-SPS, ref. ANR-10-LABX-0040-SPS to SC, and ANR-11-BTBR-0006 BIOMASS FOR THE FUTURE to SC), managed by the French National Research Agency under an Investment for the Future program (ref. ANR-11-IDEX-0003-02 to SC).