Activation of the jasmonic acid pathway by depletion of the hydroperoxide lyase OsHPL3 reveals crosstalk between the HPL and AOS branches of the oxylipin pathway in rice

PLoS One. 2012;7(11):e50089. doi: 10.1371/journal.pone.0050089. Epub 2012 Nov 29.

Abstract

The allene oxide synthase (AOS) and hydroperoxide lyase (HPL) branches of the oxylipin pathway, which underlie the production of jasmonates and aldehydes, respectively, function in plant responses to a range of stresses. Regulatory crosstalk has been proposed to exist between these two signaling branches; however, there is no direct evidence of this. Here, we identified and characterized a jasmonic acid (JA) overproduction mutant, cea62, by screening a rice T-DNA insertion mutant library for lineages that constitutively express the AOS gene. Map-based cloning was used to identify the underlying gene as hydroperoxide lyase OsHPL3. HPL3 expression and the enzyme activity of its product, (E)-2-hexenal, were depleted in the cea62 mutant, which resulted in the dramatic overproduction of JA, the activation of JA signaling, and the emergence of the lesion mimic phenotype. A time-course analysis of lesion formation and of the induction of defense responsive genes in the cea62 mutant revealed that the activation of JA biosynthesis and signaling in cea62 was regulated in a developmental manner, as was OsHPL3 activity in the wild-type plant. Microarray analysis showed that the JA-governed defense response was greatly activated in cea62 and this plant exhibited enhanced resistance to the T1 strain of the bacterial blight pathogen Xanthomonasoryzaepvoryzae (Xoo). The wounding response was attenuated in cea62 plants during the early stages of development, but partially recovered when JA levels were elevated during the later stages. In contrast, the wounding response was not altered during the different developmental stages of wild-type plants. These findings suggest that these two branches of the oxylipin pathway exhibit crosstalk with regards to biosynthesis and signaling and cooperate with each other to function in diverse stress responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aldehyde-Lyases / chemistry*
  • Aldehydes
  • Cloning, Molecular
  • Cyclopentanes / metabolism*
  • Cytochrome P-450 Enzyme System / chemistry*
  • Gene Expression Regulation, Enzymologic*
  • Gene Expression Regulation, Fungal
  • Gene Expression Regulation, Plant
  • Gene Library
  • Genetic Complementation Test
  • Mutation
  • Oligonucleotide Array Sequence Analysis
  • Oryza / enzymology*
  • Oryza / genetics
  • Oxylipins / metabolism*
  • Phenotype
  • Plant Proteins / chemistry*
  • Plant Proteins / metabolism
  • Signal Transduction
  • Xanthomonas / metabolism

Substances

  • Aldehydes
  • Cyclopentanes
  • Oxylipins
  • Plant Proteins
  • jasmonic acid
  • Cytochrome P-450 Enzyme System
  • Aldehyde-Lyases
  • hydroperoxide lyase

Grants and funding

This work was supported by the National Natural Science Foundation of China (31270323, 30971544 and 30825029) and the 973 Project from the Ministry of Sciences and Technology of China (2010CB126202). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.