Responses to and detoxification of esculin in white-rot fungi

Plant metabolites have a great potential for limiting the spread of harmful fungi. However, a better understanding of the mode-of-action of these molecules and the defense systems developed by fungi to resist them, is needed to assess the benefits/risks of using them as antifungal treatment. White-rot fungi are excellent models in this respect, as they have adapted to the hostile habitat that is wood. In fact, wood is a source of putative antifungal compounds that can be derived using extraction techniques. In this study, we demonstrated that esculin and esculetin, which are coumarins found in plants and wood, reduce the growth of the wood-rotting fungi Fomitiporia mediterranea, Phanerochaete chrysosporium, Pycnoporus cinnabarinus and Trametes versicolor. We have shown that extracellular strategies are developed by the fungi to deal with esculin, through the involvement of laccases, peroxidases and glycoside hydrolases, and intracellular strategies, mainly via upregulated protein translation. Comparative proteomic and metabolomic approaches revealed that, despite the fact that the species analysed are closely related (they all belong to the Agaricomycetes, and have the same trophic mode), their defense responses to esculin differ.