Uncovering the Host Range-Lifestyle Relationship in the Endophytic and Anthracnose Pathogenic Genus Colletotrichum

Colletotrichum includes agriculturally and scientifically important pathogens that infect numerous plants. They can also adopt an endophytic lifestyle, refraining from causing disease and/or even promoting plant growth when inoculated on a non-susceptible host. In this manner, the host range of a Colletotrichum fungus can shift, depending on whether it exhibits endophytic or pathogenic lifestyles. Some fungi, such as Colletotrichum tofieldiae, can even shift between pathogenicity and endophytism within the same host depending on the environmental conditions. Here, we aim to disentangle the relationship between lifestyle and host range in Colletotrichum. Specifically, we aim to demonstrate that lifestyle is dependent on the host colonized in many Colletotrichum fungi. We discuss the ways in which pathogenic Colletotrichum species may act endophytically on alternative hosts, how comparative genomics has uncovered candidate molecules (namely effectors, CAZymes, and secondary metabolites) underlying fungal lifestyle, and the merits of using endophytic fungi alongside pathogenic fungi in research, which facilitates the use of reverse genetics to uncover molecular determinants of lifestyle. In particular, we reference the Arabidopsis thaliana-Colletotrichum tofieldiae study system as a model for elucidating the dual roles of plant-fungus interactions, both endophytic and pathogenic, through integrative omics approaches and reverse genetics. This is because C. tofieldiae contains closely related pathogens and endophytes, making it an ideal model for identifying candidate determinants of lifestyle. This approach could identify key molecular targets for effective pathogen management in agriculture. Lastly, we propose a model in which pathogenic lifestyle occupies a different host range than the endophytic lifestyle. This will enhance our understanding of pathogenicity and endophytism in a globally significant fungal genus and lay the groundwork for future research examining molecular determinants of lifestyle in plant-associated fungi.