MYC2 Orchestrates a Hierarchical Transcriptional Cascade That Regulates Jasmonate-Mediated Plant Immunity in Tomato

Plant Cell. 2017 Aug;29(8):1883-1906. doi: 10.1105/tpc.16.00953. Epub 2017 Jul 21.

Abstract

The hormone jasmonate (JA), which functions in plant immunity, regulates resistance to pathogen infection and insect attack through triggering genome-wide transcriptional reprogramming in plants. We show that the basic helix-loop-helix transcription factor (TF) MYC2 in tomato (Solanum lycopersicum) acts downstream of the JA receptor to orchestrate JA-mediated activation of both the wounding and pathogen responses. Using chromatin immunoprecipitation sequencing (ChIP-seq) coupled with RNA sequencing (RNA-seq) assays, we identified 655 MYC2-targeted JA-responsive genes. These genes are highly enriched in Gene Ontology categories related to TFs and the early response to JA, indicating that MYC2 functions at a high hierarchical level to regulate JA-mediated gene transcription. We also identified a group of MYC2-targeted TFs (MTFs) that may directly regulate the JA-induced transcription of late defense genes. Our findings suggest that MYC2 and its downstream MTFs form a hierarchical transcriptional cascade during JA-mediated plant immunity that initiates and amplifies transcriptional output. As proof of concept, we showed that during plant resistance to the necrotrophic pathogen Botrytis cinerea, MYC2 and the MTF JA2-Like form a transcription module that preferentially regulates wounding-responsive genes, whereas MYC2 and the MTF ETHYLENE RESPONSE FACTOR.C3 form a transcription module that preferentially regulates pathogen-responsive genes.

MeSH terms

  • Amino Acid Motifs
  • Binding Sites
  • Botrytis / physiology
  • Cyclopentanes / pharmacology*
  • Disease Resistance / drug effects
  • Disease Resistance / genetics
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant / drug effects
  • Gene Ontology
  • Genes, Plant
  • Lycopersicon esculentum / drug effects
  • Lycopersicon esculentum / genetics*
  • Lycopersicon esculentum / immunology*
  • Models, Biological
  • Oxylipins / pharmacology*
  • Plant Diseases / microbiology
  • Plant Immunity / drug effects*
  • Plant Immunity / genetics
  • Plant Proteins / metabolism*
  • Promoter Regions, Genetic / genetics
  • Protein Binding / drug effects
  • Sequence Analysis, RNA
  • Transcription, Genetic / drug effects*
  • Transcriptome / genetics

Substances

  • Cyclopentanes
  • Oxylipins
  • Plant Proteins
  • jasmonic acid