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

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.

A 2-kb Mycovirus Converts a Pathogenic Fungus into a Beneficial Endophyte for Brassica Protection and Yield Enhancement

“…In addition, SsSaxA was downregulated approximately 2-fold in DT-8 when infecting leaves. Its product, isothiocyanate hydrolase, degrades plant isothiocyanate and contributes to the virulence of S. sclerotiorum on glucosinolate-producing plants (Chen et al, 2020). These results suggested that the production of virulence factors was suppressed in DT-8 and that resistance of rapeseed was induced to inhibit the destructive growth of DT-8 in plants during infection.…”

“…Lignin and glucosinolates are very important substances for plant resistance (Clay et al, 2009;Denness et al, 2011;Chen et al, 2020). Genes encoding cinnamoyl-CoA reductase (BnaA02g36250D), peroxidase (BnaA04g23960D, BnaA07g03710D), and desulfoglucosinolate sulfotransferase (ST5A) (BnaC06g35000D) were significantly upregulated (Supplemental Table 1).…”

“…Sclerotinia sclerotiorum is a typical necrotrophic pathogen with numerous hosts, including many economically important crops such as rapeseed, soybean, and sunflower (Bolton et al, 2006;Amselem et al, 2011). S. sclerotiorum has developed intricate mechanisms to attack its hosts (Xu et al, 2018;Chen et al, 2020) whereby lesions develop and the host is killed within a few days. S. sclerotiorum can infect the aerial parts of plants by means of ascospores that initially infect petals and wounded or senescent tissue; it can also infect roots or stem bases by means of infectious hyphae that germinate from sclerotia in the soil (Bolton et al, 2006).…”

Genome‐wide alternative splicing profiling in the fungal plant pathogen Sclerotinia sclerotiorum during the colonization of diverse host families

“…Furthermore, S. sclerotiorum produces secondary metabolites such as sclerin and botcinic acid acting as toxins to facilitate infection (Graham‐Taylor et al, 2020; Pedras and Ahiahonu, 2004). Finally, S. sclerotiorum is able to detoxify plant defence compounds, enabling the colonization of certain hosts (Pedras and Ahiahonu, 2005), but the underlying molecular mechanisms are known in rare cases only (Chen et al, 2020). Whether the requirement for these diverse virulence mechanisms varies from one host to another remains largely elusive.…”

Transcriptional response to host chemical cues underpins expansion of host range in a fungal plant pathogen lineage

“…Plants in the order Brassicales like A. thaliana produce tryptophan-derived defensive metabolites such as indolic glucosinolates (iGLs) and the indole alkaloid camalexin (cam.). The ability of some insect and fungal pathogens to metabolize these plant defense compounds into non-toxic derivatives contributes to their capacity to infect plants from the Brassicales (Chen et al, 2020). To test whether the toxicity of tryptophan-derived plant defense metabolites could explain the inability of S. trifoliorum to colonize Brassicales, we compared the sensitivity of S. sclerotiorum and S. trifoliorum to the five major defense tryptophan-derivatives produced by A. thaliana using an in vitro growth assay ( Figure 5A, Supplementary Figure 2 ).…”