Architecture and dynamics of the jasmonic acid gene regulatory network

Richard Hickman, Marcel C Van Verk, Anja J H Van Dijken, Marciel Pereira Mendes, Irene A Vroegop-Vos, Lotte Caarls, Merel Steenbergen, Ivo Van der Nagel, Gert Jan Wesselink, Aleksey Jironkin, Adam Talbot, Johanna Rhodes, Michel De Vries, Robert C Schuurink, Katherine Denby, Corne M. J. Pieterse, Saskia CM Van Wees

Research output: Contribution to journalArticlepeer-review

Abstract

Jasmonic acid (JA) is a critical hormonal regulator of plant growth and defense. To advance our understanding of the architecture and dynamic regulation of the JA gene regulatory network, we performed a high-resolution RNA-seq time series of methyl JA-treated Arabidopsis thaliana at 15 time points over a 16-h period. Computational analysis showed that methyl JA (MeJA) induces a burst of transcriptional activity, generating diverse expression patterns over time that partition into distinct sectors of the JA response targeting specific biological processes. The presence of transcription factor (TF) DNA binding motifs correlated with specific TF activity during temporal MeJA-induced transcriptional reprogramming. Insight into the underlying dynamic transcriptional regulation mechanisms was captured in a chronological model of the JA gene regulatory network. Several TFs, including MYB59 and bHLH27, were uncovered as early network components with a role in pathogen and insect resistance. Analysis of subnetworks surrounding the TFs ORA47, RAP2.6L, MYB59, and ANAC055, using transcriptome profiling of overexpressors and mutants, provided insights into their regulatory role in defined modules of the JA network. Collectively, our work illuminates the complexity of the JA gene regulatory network, pinpoints and validates previously unknown regulators, and provides a valuable resource for functional studies on JA signaling components in plant defense and development.

Original languageEnglish
Pages (from-to)2086-2105
Number of pages20
JournalThe Plant Cell
Volume29
Issue number9
Early online date21 Aug 2017
DOIs
Publication statusPublished - 1 Sept 2017

Bibliographical note

©2017 American Society of Plant Biologists. This is an author-produced version of the published paper. Uploaded in accordance with the publisher’s self-archiving policy. Further copying may not be permitted; contact the publisher for details

Keywords

  • Acetates/pharmacology
  • Animals
  • Arabidopsis/genetics
  • Base Sequence
  • Cyclopentanes/metabolism
  • DNA, Plant/metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant/drug effects
  • Gene Regulatory Networks/drug effects
  • Genes, Plant
  • Insecta/physiology
  • Multigene Family
  • Nucleotide Motifs/genetics
  • Oxylipins/metabolism
  • Time Factors
  • Transcription Factors/metabolism
  • Transcription, Genetic/drug effects

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