Conjugation ofcis-OPDA with amino acids is a conserved pathway affectingcis-OPDA homeostasis upon stress responses

Abstract

AbstractJasmonates (JAs) are a family of oxylipin phytohormones regulating plant development and growth and mediating ‘defenseversusgrowth’ responses. The upstream JA biosynthetic precursorcis-(+)-12-oxo-phytodienoic acid (cis-OPDA) has been reported to act independently of the COI1-mediated JA signaling in several stress-induced and developmental processes. However, its means of perception and metabolism are only partially understood. Furthermore,cis-OPDA, but not JA, occurs in non-vascular plant species, such as bryophytes, exhibiting specific functions in defense and development. A few years ago, a low abundant isoleucine analog of the biologically active JA-Ile, OPDA-Ile, was detected in wounded leaves of flowering plants, opening up to the possibility that conjugation ofcis-OPDA to amino acids might be a relevant mechanism forcis-OPDA regulation. Here, we extended the analysis of amino acid conjugates ofcis-OPDA and identified naturally occurring OPDA-Val, OPDA-Phe, OPDA-Ala, OPDA-Glu, and OPDA-Asp in response to biotic and abiotic stress in Arabidopsis. The newly identified OPDA-amino acid conjugates showcis-OPDA-related plant responses in a JAR1-dependent manner. We also discovered that the synthesis and hydrolysis ofcis-OPDA amino acid conjugates are regulated by members of the amidosynthetase GH3 and the amidohydrolase ILR1/ILL families. Finally, we found that thecis-OPDA conjugative pathway already functions in non-vascular plants and gymnosperms. Thus, one level of regulation by which plants modulatecis-OPDA homeostasis is the synthesis and hydrolysis of OPDA-amino acid conjugates, which temporarily storecis-OPDA in stress responses.