Hijacking of the jasmonate pathway by the mycotoxin fumonisin B1 (FB1) to initiate programmed cell death in Arabidopsis is modulated by RGLG3 and RGLG4

J Exp Bot. 2015 May;66(9):2709-21. doi: 10.1093/jxb/erv068. Epub 2015 Mar 18.

Abstract

The mycotoxin fumonisin B1 (FB1) is a strong inducer of programmed cell death (PCD) in plants, but its underlying mechanism remains unclear. Here, we describe two ubiquitin ligases, RING DOMAIN LIGASE3 (RGLG3) and RGLG4, which control FB1-triggered PCD by modulating the jasmonate (JA) signalling pathway in Arabidopsis thaliana. RGLG3 and RGLG4 transcription was sensitive to FB1. Arabidopsis FB1 sensitivity was suppressed by loss of function of RGLG3 and RGLG4 and was increased by their overexpression. Thus RGLG3 and RGLG4 have coordinated and positive roles in FB1-elicited PCD. Mutated JA perception by coi1 disrupted the RGLG3- and RGLG4-related response to FB1 and interfered with their roles in cell death. Although FB1 induced JA-responsive defence genes, it repressed growth-related, as well as JA biosynthesis-related, genes. Consistently, FB1 application reduced JA content in wild-type plants. Furthermore, exogenously applied salicylic acid additively suppressed JA signalling with FB1 treatment, suggesting that FB1-induced salicylic acid inhibits the JA pathway during this process. All of these effects were attenuated in rglg3 rglg4 plants. Altogether, these data suggest that the JA pathway is hijacked by the toxin FB1 to elicit PCD, which is coordinated by Arabidopsis RGLG3 and RGLG4.

Keywords: Arabidopsis; RGLG3; RGLG4; fumonisin B1; jasmonate; programmed cell death; salicylic acid..

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Apoptosis / drug effects
  • Apoptosis / physiology*
  • Arabidopsis / cytology
  • Arabidopsis / drug effects
  • Arabidopsis / physiology*
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Arabidopsis Proteins / physiology*
  • Cell Nucleus / metabolism
  • Cyclopentanes / metabolism*
  • Cytoplasm / metabolism
  • Fumonisins / pharmacology*
  • Gene Expression Regulation, Plant
  • Ligases / genetics
  • Ligases / metabolism
  • Ligases / physiology*
  • Oxylipins / metabolism*
  • RING Finger Domains*
  • Salicylic Acid / metabolism
  • Signal Transduction*

Substances

  • Arabidopsis Proteins
  • Cyclopentanes
  • Fumonisins
  • Oxylipins
  • fumonisin B1
  • jasmonic acid
  • Ligases
  • RGLG3 protein, Arabidopsis
  • RGLG4 protein, Arabidopsis
  • Salicylic Acid