The Arabidopsis non‐host defence‐associated coumarin scopoletin protects soybean from Asian soybean rust

Abstract

Summary The fungus Phakopsora pachyrhizi (Pp) causes Asian soybean rust (SBR) disease which provokes tremendous losses in global soybean production. Pp is mainly controlled with synthetic fungicides to which the fungus swiftly develops fungicide resistance. To substitute or complement synthetic fungicides in Asian soybean rust control, we aimed to identify antifungal metabolites in Arabidopsis which is not a host for Pp. Comparative transcriptional and metabolic profiling of the Pp‐inoculated Arabidopsis non‐host and the soybean host revealed induction of phenylpropanoid metabolism‐associated genes in both species but activation of scopoletin biosynthesis only in the resistant non‐host. Scopoletin is a coumarin and an antioxidant. In vitro experiments disclosed fungistatic activity of scopoletin against Pp, associated with reduced accumulation of reactive oxygen species (ROS) in fungal pre‐infection structures. Non‐antioxidant and antioxidant molecules including coumarins with a similar structure to scopoletin were inactive or much less effective at inhibiting fungal accumulation of ROS and germination of Pp spores. When sprayed onto Arabidopsis leaves, scopoletin also suppressed the formation of Pp pre‐infection structures and penetration of the plant. However, scopoletin neither directly activated defence nor did it prime Arabidopsis for enhanced defence, therefore emphasizing fungistatic activity as the exclusive mode of action of scopoletin against Pp. Because scopletin also protected soybean from Pp infection, the coumarin may serve as a natural fungicide or as a lead for the development of near‐to‐nature fungicides against Asian soybean rust.

Untargeted Metabolomics Analysis by UHPLC-MS/MS of Soybean Plant in a Compatible Response to Phakopsora pachyrhizi Infection

“…We (Table 1). Beyer et al, 2019, demonstrated fungistatic activity of coumarin scopoletin against P. pachyrhizi [49]. Coumarin was able to suppress the formation of pre-infection streaks and penetration of P. pachyrhizi when sprayed on leaves of Arabidopsis, a non-host plant from ASR [49].…”

“…We identified four coumarins, 7-methoxycoumarin [M + H] + m/z 177.0541; [M + H] + m/z 193.0488 scopoletin; xanthyletin [M + H] + m/z 229.0857, and osthole [M + H] + m/z 245.1168 ( Table 1 ). Beyer et al, 2019, demonstrated fungistatic activity of coumarin scopoletin against P. pachyrhizi [ 49 ]. Coumarin was able to suppress the formation of pre-infection streaks and penetration of P. pachyrhizi when sprayed on leaves of Arabidopsis , a non-host plant from ASR [ 49 ].…”

Pinpointing secondary metabolites that shape the composition and function of the plant microbiome

“…For example, feeding rats ochratoxin A, one of the major mycotoxins derived from a coumarin backbone, resulted in increased abundance of a Lactobacillus strain that is able to absorb this metabolite ( Guo et al , 2014 ). In plant roots, secreted coumarins have been recognized as important for increasing bioavailability of iron, through reduction and chelation ( Tsai and Schmidt, 2017 ), and also for their antimicrobial functions ( Beyer et al , 2019 ; Stringlis et al , 2019 ). Interestingly, a transcription factor, MYB72, which controls expression of several genes in coumarin synthesis, is also important for induced systemic resistance against pathogens triggered by the root bacterium Pseudomonas simiae WCS417 ( Zamioudis et al , 2014 ).…”

Roles of Plant-Derived Secondary Metabolites during Interactions with Pathogenic and Beneficial Microbes under Conditions of Environmental Stress

“…In addition to the roles of coumarins in iron uptake, in vitro chemical assays showed that several coumarins, such as scopoletin, which is the most abundantly expressed coumarin in low-iron conditions, exhibit direct antimicrobial activities against several pathogens [12,44,45,46]. In any case, scopoletin from seed kernels of Melia azedarach shows synergistic anti-fungal effects when combined with other coumarins [47].…”