Abstract
The emerging resistance of crop pathogens to fungicides poses a challenge to food security and compels discovery of new antifungal compounds. Here, we show that mono-alkyl lipophilic cations (MALCs) inhibit oxidative phosphorylation by affecting NADH oxidation in the plant pathogens Zymoseptoria tritici, Ustilago maydis and Magnaporthe oryzae. One of these MALCs, consisting of a dimethylsulfonium moiety and a long alkyl chain (C18-SMe2+), also induces production of reactive oxygen species at the level of respiratory complex I, thus triggering fungal apoptosis. In addition, C18-SMe2+ activates innate plant defense. This multiple activity effectively protects cereals against Septoria tritici blotch and rice blast disease. C18-SMe2+ has low toxicity in Daphnia magna, and is not mutagenic or phytotoxic. Thus, MALCs hold potential as effective and non-toxic crop fungicides.
Highlights
The emerging resistance of crop pathogens to fungicides poses a challenge to food security and compels discovery of new antifungal compounds
We show that C12-G+ targets fungal mitochondria and strongly inhibits ATP synthesis by reducing NADH oxidation and depolarizing the inner membrane
We investigated the importance of alkyl chain length in the ability of C18-SMe2+ to trigger Mitochondria also produce reactive oxygen species (mROS) formation by DHR-123 staining of cells treated with a newly-synthesized C16-alkyl chain dimethylsulfonium cation (C16-SMe2+) and C12-SMe2+ (Supplementary Fig. 6)
Summary
The emerging resistance of crop pathogens to fungicides poses a challenge to food security and compels discovery of new antifungal compounds. We show that mono-alkyl lipophilic cations (MALCs) inhibit oxidative phosphorylation by affecting NADH oxidation in the plant pathogens Zymoseptoria tritici, Ustilago maydis and Magnaporthe oryzae One of these MALCs, consisting of a dimethylsulfonium moiety and a long alkyl chain (C18-SMe2+), induces production of reactive oxygen species at the level of respiratory complex I, triggering fungal apoptosis. An alternative approach is use of multi-site fungicides, which usually interfere with unknown essential cellular processes in multiple ways This broader activity often comes with increased toxicity. One potential target for fungicide development are fungal mitochondria These organelles are involved in a range of cellular processes, including ATP production by oxidative phosphorylation[9]. Increasing evidence suggests that this programmed cell death pathway exits in fungi[17]; targeting this is a promising strategy for anti-fungal development[18]
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