A fungal monooxygenase-derived jasmonate attenuates host innate immunity

Abstract

Distinct modifications fine-tune the activity of jasmonic acid (JA) in regulating plant growth and immunity. Hydroxylated JA (12OH-JA) promotes flower and tuber development but prevents induction of JA signaling, plant defense or both. However, biosynthesis of 12OH-JA has remained elusive. We report here an antibiotic biosynthesis monooxygenase (Abm) that converts endogenous free JA into 12OH-JA in the model rice blast fungus Magnaporthe oryzae. Such fungal 12OH-JA is secreted during host penetration and helps evade the defense response. Loss of Abm in M. oryzae led to accumulation of methyl JA (MeJA), which induces host defense and blocks invasive growth. Exogenously added 12OH-JA markedly attenuated abmΔ-induced immunity in rice. Notably, Abm itself is secreted after invasion and most likely converts plant JA into 12OH-JA to facilitate host colonization. This study sheds light on the chemical arms race during plant-pathogen interaction, reveals Abm as an antifungal target and outlines a synthetic strategy for transformation of a versatile small-molecule phytohormone.

Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid

“…The 12-OH-JA has been characterized as an inactive form of JA, because it is not capable of degrading JAZ9 and does not induce expression of JA-responsive genes or inhibition of root growth (15,18,19). The compound has been suggested to have tuber-inducing capabilities (22), but what the role of this compound is in non-tuber-forming plants such as Arabidopsis is not clear.…”

“…12-OH-JA has been identified in several plant species, including Arabidopsis, maize, potato, tomato, and rice, and accumulates in Arabidopsis after wounding and Botrytis cinerea infection (13,18,(20)(21)(22). Strikingly, hydroxylation of JA to 12-OH-JA by a monooxygenase produced by the blast fungus Magnaporthe oryzae attenuates plant immune responses to this pathogen (19). So far, no plant enzyme that hydroxylates JA has been identified (23).…”

“…The hydroxylated form of JA is thought to be inactive because it does not trigger degradation of JAZ repressors, and treatment with 12-OH-JA accordingly does not induce JA-responsive gene expression, nor does it inhibit root growth or seed germination (18,19). 12-OH-JA has been identified in several plant species, including Arabidopsis, maize, potato, tomato, and rice, and accumulates in Arabidopsis after wounding and Botrytis cinerea infection (13,18,(20)(21)(22).…”

Production of cross-kingdom oxylipins by pathogenic fungi: An update on their role in development and pathogenicity

“…Only recently has a monooxygenase been definitively linked to oxylipin production in fungi, specifically with the production of 12-OH-jasmonic acid (12-OH-JA) in the rice blast fungus, M. oryzae (Fig. 1B) (Patkar et al ., 2015). A possible connection has been inferred with the dimorphic fungus C. albicans .…”

“…Alternately, exogenous 12-OH-JA increases the number of Δabm invading appressoria in a dose-dependent fashion. The authors went on to identify that Abm is secreted from both the biotrophic interfacial complex (BIC) and the appressorium of M. oryzae during pathogenic growth, providing evidence that Abm hydroxylates not only M. oryzae JA, but plant-derived JA as well (Patkar et al ., 2015). …”