Cytochrome P450 CYP94B3 Mediates Catabolism and Inactivation of the Plant Hormone jasmonoyl-L-isoleucine

Proc Natl Acad Sci U S A. 2011 May 31;108(22):9298-303. doi: 10.1073/pnas.1103542108. Epub 2011 May 16.

Abstract

The phytohormone jasmonoyl-L-isoleucine (JA-Ile) signals through the COI1-JAZ coreceptor complex to control key aspects of plant growth, development, and immune function. Despite detailed knowledge of the JA-Ile biosynthetic pathway, little is known about the genetic basis of JA-Ile catabolism and inactivation. Here, we report the identification of a wound- and jasmonate-responsive gene from Arabidopsis that encodes a cytochrome P450 (CYP94B3) involved in JA-Ile turnover. Metabolite analysis of wounded leaves showed that loss of CYP94B3 function in cyp94b3 mutants causes hyperaccumulation of JA-Ile and concomitant reduction in 12-hydroxy-JA-Ile (12OH-JA-Ile) content, whereas overexpression of this enzyme results in severe depletion of JA-Ile and corresponding changes in 12OH-JA-Ile levels. In vitro studies showed that heterologously expressed CYP94B3 converts JA-Ile to 12OH-JA-Ile, and that 12OH-JA-Ile is less effective than JA-Ile in promoting the formation of COI1-JAZ receptor complexes. CYP94B3-overexpressing plants displayed phenotypes indicative of JA-Ile deficiency, including defects in male fertility, resistance to jasmonate-induced growth inhibition, and susceptibility to insect attack. Increased accumulation of JA-Ile in wounded cyp94b3 leaves was associated with enhanced expression of jasmonate-responsive genes. These results demonstrate that CYP94B3 exerts negative feedback control on JA-Ile levels and performs a key role in attenuation of jasmonate responses.

Publication types

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

MeSH terms

  • Animals
  • Arabidopsis / metabolism*
  • Cyclopentanes / metabolism
  • Cyclopentanes / pharmacology*
  • Cytochrome P-450 Enzyme System / metabolism*
  • Fatty Acids / metabolism
  • Gene Expression Regulation, Enzymologic
  • Isoleucine / analogs & derivatives*
  • Isoleucine / pharmacology
  • Metabolism
  • Mixed Function Oxygenases / metabolism
  • Models, Genetic
  • Oxylipins / metabolism
  • Phenotype
  • Plant Growth Regulators / metabolism*
  • Plant Proteins / metabolism
  • Signal Transduction
  • Spodoptera

Substances

  • Cyclopentanes
  • Fatty Acids
  • Oxylipins
  • Plant Growth Regulators
  • Plant Proteins
  • jasmonoyl-isoleucine
  • Isoleucine
  • jasmonic acid
  • Cytochrome P-450 Enzyme System
  • Mixed Function Oxygenases
  • cytochrome P-450 94B3, Arabidopsis