Fungal jasmonate as a novel morphogenetic signal for pathogenesis

Abstract

A key question that has remained unanswered is how pathogenic fungi switch from vegetative growth to infection-related morphogenesis during a disease cycle. Here, we identify a fungal oxylipin analogous to the well-known phytohormone jasmonic acid, as the principal morphogenesis signal responsible for such a developmental switch to pathogenicity in the rice-blast fungus Magnaporthe oryzae. We explored the molecular function(s) of such intrinsic jasmonic acid during pathogenic differentiation in M. oryzae via OPR1, which encodes a 12-Oxo-phytodienoic Acid Reductase essential for its biosynthesis. Loss of OPR1 led to prolonged vegetative growth, and a delayed initiation and improper development of infection structures in M. oryzae, reminiscent of phenotypes observed in mutants (e.g. pth11{Delta} and cpka{Delta}) that are compromised for cyclic AMP signaling. Genetic- or chemical-complementation completely restored proper germ tube growth and appressorium formation in opr1{Delta}. Liquid chromatography mass spectrometry-based quantification revealed increased OPDA accumulation and a significant decrease in JA levels in the opr1{Delta}. Most interestingly, exogenous jasmonic acid also restored appressorium formation in the pth11{Delta} mutant that lacks G protein/cyclic AMP signaling. Epistasis analysis placed fungal jasmonate upstream of the cyclic AMP signaling in rice blast. Lastly, we show that intrinsic jasmonate orchestrates the cessation of vegetative phase and initiates pathogenic development via a regulatory interaction with the cyclic AMP cascade and redox signaling in rice blast.