Evolution of host range is associated with carbohydrate and protein metabolism in Colletotrichum spp.

Colletotrichum spp. cause anthracnose disease on a wide range of agronomically important plant species and exhibit a broad diversity of host range, host specificity and reproductive behaviors. We leveraged the growing number of genome sequences available for Colletotrichum spp. and performed a comparative analysis of gene content to find associations with host range and host specificity. The predicted protein sequences from each species were classified into protein families using a variety of tools. Hierarchical clustering of gene family and functional domain assignments, and phylogenetic analyses revealed lineage specific losses of secreted carbohydrate-active enzymes (CAZymes) and protease encoding genes in species that have narrow host range as well as expansions of these families in the acutatum and gloeosporioides species complexes. Members of these species complexes are broad host range pathogens, suggesting that the higher number in CAZy and protease diversity may be associated with the ability to infect multiple host species. This result highlights the similarity in both secretomes and whole proteomes of these species complexes and suggests that their gene family content, especially their repertoires of CAZymes and peptidases are the product of recent, lineage specific expansions of these families independently in each species complex. Interestingly, phylogenetic analyses of the CAZyme and peptidase families revealed that, in contrast to our expectations, gene loss in other Colletotrichum species is as important, if not more important force driving the evolution of gene family size. These results are consistent with the idea that different lifestyles, hosts and host tissues present different types of carbohydrate substrates to the pathogen this is reflected by each species’ CAZyme and peptidase repertoire.