Fungal Jasmonate as a Novel Morphogenetic Signal for Pathogenesis.

Yingyao Liu,Naweed I Naqvi,Martin Pagac,Fan Yang,Rajesh N Patkar

doi:10.3390/jof7090693

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 phytohormone jasmonic acid (JA), as the principal regulator of such a developmental switch to isotropic growth and pathogenicity in the rice-blast fungus Magnaporthe oryzae. Using specific inhibitors and mutant analyses, we determined the molecular function of intrinsic jasmonates during M. oryzae pathogenesis. Loss of 12-Oxo-phytodienoic Acid (OPDA) Reductase and/or consequent reduction of jasmonate biosynthesis, prolonged germ tube growth and caused delayed initiation and improper development of infection structures in M. oryzae, reminiscent of phenotypic defects upon impaired cyclic AMP (cAMP) signaling. Chemical- or genetic-complementation completely restored proper vegetative growth and appressoria in opr1Δ. Mass spectrometry-based quantification revealed increased OPDA accumulation and significantly decreased jasmonate levels in opr1Δ. Most interestingly, exogenous jasmonate restored proper appressorium formation in pth11Δ that lacks G protein/cAMP signaling; but failed to do so in the Mitogen-activated protein (MAP) kinase mutants. Epistasis analysis placed jasmonate upstream of the cAMP pathway in rice blast. Mechanistically, intrinsic jasmonate orchestrates timely cessation of the vegetative phase and induces pathogenic development via a complex regulatory interaction with the cAMP-PKA cascade and redox signaling in rice blast.

Highlights

Phytohormone mimics are produced and utilized by some pathogenic fungi in crosskingdom communication with the hosts for immuno-modulation to aid their survival and infectivity
We found that jasmonic acid (JA) and its derivate 12-hydroxyjasmonic acid (12OH-JA) are synthesized by the rice blast fungus M. oryzae and subsequently secreted into the host cells to suppress the JA-dependent plant immunity [3]
We describe a fungal enzyme, Opr1, involved in JA biosynthesis in the rice-blast pathogen M. oryzae

Summary

Introduction

Phytohormone mimics are produced and utilized by some pathogenic fungi in crosskingdom communication with the hosts for immuno-modulation to aid their survival and infectivity. We found that jasmonic acid (JA) and its derivate 12-hydroxyjasmonic acid (12OH-JA) are synthesized by the rice blast fungus M. oryzae and subsequently secreted into the host cells to suppress the JA-dependent plant immunity [3]. This remarkable discovery identified that the phytopathogenic fungus M. oryzae follows Lasiodiplodia theobromae [4], Fusarium oxysporum, and Gibberella fujikuroi [5], in biosynthesis of such fungal JA-like oxygenated lipids or oxylipins in vivo. Prostaglandins, the mammalian oxylipins with different hormone-like functions (including immune response), are found to induce the yeast to hyphal transition in C. albicans [8]. While the underlying mechanism is still not clear, it is believed that the oxylipins may be involved in such morphological changes, especially given the inhibitory effect of these phytoalexins on fungal fatty acid oxidases and prostaglandin production in Cryptococcus neoformans [13]

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Conclusion