Comparative genomics between enophytic and pathogenic Colletotrichum species isolated from field-grown healthy Brassicaceae plants

In nature, plants are constantly associated with a rich diversity of microbes, ranging from potentially harmful pathogens to beneficial endophytes, typically without discernible disease symptoms. However, it remains poorly understood how the potential pathogenesis of pathogens that colonize inside the plant is suppressed. Here, we show that the root endophyte Colletotrichum fructicola (CfE), isolated from field-grown healthy Brassicaceae plants, inhibits the pathogenic growth of Colletotrichum fungi in Arabidopsis thaliana. Remarkably, CfE displays the antifungal function specifically in the host plants but not in axenic culture conditions. Isolation of C. gloeosporioides, a pathogenic relative to CfE, called CgP, from healthy Brassicaceae individuals accommodating CfE enables comparative genome and in-planta transcriptome analyses between the two fungi. This reveals a degree of divergence in their genome sequences and >700 CfE genes (4.34% of CfE whole genes) that are specifically induced in A. thaliana following co-inoculation with CgP. This indicates that large-scale transcriptome reprograming is induced in CfE during its suppression of CgP growth and pathogenesis in the host roots. In particular, strong activation of CfE genes for the biosynthesis and efflux of fungal toxins raises the possibility that CfE outcompetes phytopathogenic fungi with these fungal toxins, thereby conferring plant protection.