Negative feedback control of jasmonate signaling by an alternative splice variant of JAZ10

Plant Physiol. 2013 Jun;162(2):1006-17. doi: 10.1104/pp.113.218164. Epub 2013 Apr 30.

Abstract

The plant hormone jasmonate (JA) activates gene expression by promoting ubiquitin-dependent degradation of jasmonate ZIM domain (JAZ) transcriptional repressor proteins. A key feature of all JAZ proteins is the highly conserved Jas motif, which mediates both JAZ degradation and JAZ binding to the transcription factor MYC2. Rapid expression of JAZ genes in response to JA is thought to attenuate JA responses, but little is known about the mechanisms by which newly synthesized JAZ proteins exert repression in the presence of the hormone. Here, we show in Arabidopsis (Arabidopsis thaliana) that desensitization to JA is mediated by an alternative splice variant (JAZ10.4) of JAZ10 that lacks the Jas motif. Unbiased protein-protein interaction screens identified three related basic helix-loop-helix transcription factors (MYC2, MYC3, and MYC4) and the corepressor NINJA as JAZ10.4-binding partners. We show that the amino-terminal region of JAZ10.4 contains a cryptic MYC2-binding site that resembles the Jas motif and that the ZIM motif of JAZ10.4 functions as a transferable repressor domain whose activity is associated with the recruitment of NINJA. Functional studies showed that the expression of JAZ10.4 from the native JAZ10 promoter complemented the JA-hypersensitive phenotype of a jaz10 mutant. Moreover, treatment of these complemented lines with JA resulted in the rapid accumulation of JAZ10.4 protein. Our results provide an explanation for how the unique domain architecture of JAZ10.4 links transcription factors to a corepressor complex and suggest how JA-induced transcription and alternative splicing of JAZ10 premessenger RNA creates a regulatory circuit to attenuate JA responses.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Alternative Splicing*
  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • Cyclopentanes / metabolism*
  • Cyclopentanes / pharmacology
  • Feedback, Physiological*
  • Gene Expression Regulation, Plant
  • Nuclear Proteins / genetics*
  • Nuclear Proteins / metabolism
  • Oxylipins / metabolism*
  • Oxylipins / pharmacology
  • Plants, Genetically Modified
  • Promoter Regions, Genetic
  • Protein Structure, Tertiary
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Signal Transduction
  • Trans-Activators / genetics
  • Trans-Activators / metabolism

Substances

  • Arabidopsis Proteins
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • Cyclopentanes
  • JAS1 protein, Arabidopsis
  • MYC2 protein, Arabidopsis
  • MYC3 protein, Arabidopsis
  • MYC4 protein, Arabidopsis
  • NINJA protein, Arabidopsis
  • Nuclear Proteins
  • Oxylipins
  • Repressor Proteins
  • Trans-Activators
  • jasmonic acid