The phytopathogenic fungus Sclerotinia sclerotiorum detoxifies plant glucosinolate hydrolysis products via an isothiocyanate hydrolase

Jingyuan Chen,Zhi-Ling Yang,Almuth Hammerbacher,Franziska Beran,Michael Reichelt,Daniel G Vassão,Chhana Ullah,Jonathan Gershenzon

doi:10.1038/s41467-020-16921-2

Jingyuan Chen, Zhi-Ling Yang + Show 6 more

Open Access

https://doi.org/10.1038/s41467-020-16921-2

Copy DOI

Abstract

Brassicales plants produce glucosinolates and myrosinases that generate toxic isothiocyanates conferring broad resistance against pathogens and herbivorous insects. Nevertheless, some cosmopolitan fungal pathogens, such as the necrotrophic white mold Sclerotinia sclerotiorum, are able to infect many plant hosts including glucosinolate producers. Here, we show that S. sclerotiorum infection activates the glucosinolate-myrosinase system, and isothiocyanates contribute to resistance against this fungus. S. sclerotiorum metabolizes isothiocyanates via two independent pathways: conjugation to glutathione and, more effectively, hydrolysis to amines. The latter pathway features an isothiocyanate hydrolase that is homologous to a previously characterized bacterial enzyme, and converts isothiocyanate into products that are not toxic to the fungus. The isothiocyanate hydrolase promotes fungal growth in the presence of the toxins, and contributes to the virulence of S. sclerotiorum on glucosinolate-producing plants.

Highlights

Brassicales plants produce glucosinolates and myrosinases that generate toxic isothiocyanates conferring broad resistance against pathogens and herbivorous insects
Despite our knowledge on GL metabolism in insects and bacteria, we know very little about fungal metabolism of GLs and how pathogenic fungi colonizing Brassicaceae plants cope with GLs and their toxic hydrolysis products
In this study, we found that a major group of two-component defenses in plants, the GL-myrosinase system of the Brassicales, plays an important role in defense against fungal infection

Summary

Introduction

Brassicales plants produce glucosinolates and myrosinases that generate toxic isothiocyanates conferring broad resistance against pathogens and herbivorous insects. S. sclerotiorum metabolizes isothiocyanates via two independent pathways: conjugation to glutathione and, more effectively, hydrolysis to amines The latter pathway features an isothiocyanate hydrolase that is homologous to a previously characterized bacterial enzyme, and converts isothiocyanate into products that are not toxic to the fungus. Plants of the order Brassicales produce amino acid-derived glucosinolates (GLs) which are activated by β-thioglucoside glucohydrolase enzymes (myrosinases) upon tissue damage to produce toxic isothiocyanates (ITCs) and nitriles[5]. This so-called “mustard oil bomb” provides defense against attack by many insect herbivores and some pathogens[6,7,8]. Despite our knowledge on GL metabolism in insects and bacteria, we know very little about fungal metabolism of GLs and how pathogenic fungi colonizing Brassicaceae plants cope with GLs and their toxic hydrolysis products

Methods

Results

Conclusion