Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-L-isoleucine

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 108; no. 22; pp. 9298 - 9303
• Main Authors: Koo, Abraham J.K, Cooke, Thomas F, Howe, Gregg A
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 31.05.2011; National Acad Sciences
• Subjects: Animals; Arabidopsis; Arabidopsis - metabolism; biochemical pathways; Biological Sciences; Catabolism; Cyclopentanes - metabolism; Cyclopentanes - pharmacology; cytochrome P-450; Cytochrome P-450 Enzyme System - metabolism; Cytochromes; Enzymes; Fatty acids; Fatty Acids - metabolism; Flowers & plants; Gene expression; Gene Expression Regulation, Enzymologic; gene overexpression; genes; Genotype & phenotype; growth retardation; Hormones; hyperaccumulators; in vitro studies; insects; Isoleucine - analogs & derivatives; Isoleucine - pharmacology; jasmonic acid; Leaves; male fertility; Metabolism; metabolites; Mixed Function Oxygenases - metabolism; Models, Genetic; mutants; Oxylipins - metabolism; Phenotype; Phenotypes; plant growth; Plant Growth Regulators - metabolism; plant hormones; Plant Proteins - metabolism; Plants; Receptors; Signal Transduction; Spodoptera; Yeasts
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1103542108

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.