Genus-Wide Comparative Genome Analyses ofColletotrichumSpecies Reveal Specific Gene Family Losses and Gains during Adaptation to Specific Infection Lifestyles

Abstract

Members from Colletotrichum genus adopt a diverse range of lifestyles during infection of plants and represent a group of agriculturally devastating pathogens. In this study, we present the draft genome of Colletotrichum incanum from the spaethianum clade of Colletotrichum and the comparative analyses with five other Colletotrichum species from distinct lineages. We show that the C. incanum strain, originally isolated from Japanese daikon radish, is able to infect both eudicot plants, such as certain ecotypes of the eudicot Arabidopsis, and monocot plants, such as lily. Being closely related to Colletotrichum species both in the graminicola clade, whose members are restricted strictly to monocot hosts, and to the destructivum clade, whose members are mostly associated with dicot infections, C. incanum provides an interesting model system for comparative genomics to study how fungal pathogens adapt to monocot and dicot hosts. Genus-wide comparative genome analyses reveal that Colletotrichum species have tailored profiles of their carbohydrate-degrading enzymes according to their infection lifestyles. In addition, we show evidence that positive selection acting on secreted and nuclear localized proteins that are highly conserved may be important in adaptation to specific hosts or ecological niches.

A comparative genomic analysis of putative pathogenicity genes in the host-specific sibling species Colletotrichum graminicola and Colletotrichum sublineola

“…Magnaporthe oryzae, where the deletion of secreted effector genes seems to be common, and to play an important role in the evolution of new races [121, 122]. However, comparisons with genome assemblies of the five closely related species within the graminicolous clade, accessed from JGI (http://genome.jgi.doe.gov/), suggests a more important role for deletion of effector genes, as well as other classes of genes, in speciation and host species adaptation, a finding that has also been reported by others based on comparative analyses of a wider range of Colletotrichum genera [25, 64]. …”

“…Wall structures of maize and sorghum do not appear to differ very much [95, 96], so it is possible that some of these enzymes are targeted by plant defense mechanisms, which has driven their diversification [97]. Similar categories of CAZYmes were also evolving rapidly among a larger group of more distantly related genera of Colletotrichum fungi [25, 64]. …”

“…Our approach was based on previous studies that have shown that gene gain and loss is associated with host range in many plant pathogens, including Colletotrichum [25, 64]. However, we do not mean to suggest that products of conserved genes don’t also play important roles, either alone or in combination with non-conserved gene products, in host specialization.…”

“…Many are predicted to be secreted, or targeted to the nucleus or the mitochondria, and may interact with specific host factors to suppress or avoid host defenses, or to establish biotrophic hyphae or nutritional access. Similar categories of proteins were found to be rapidly evolving among several more distantly related Colletotrichum genera, suggesting that these categories play important roles in niche adaptation across the entire genus [64]. …”

Genetic map‐guided genome assembly reveals a virulence‐governing minichromosome in the lentil anthracnose pathogen Colletotrichum lentis

“…A total of 11 436 protein‐coding gene models was predicted in the genome of C. lentis (Tables , S2), lower than that reported for other sequenced Colletotrichum species, such as C. graminicola (12 006), C. orbiculare (13 479), C. fioriniae (13 759), C. higginsianum (14 651) and C. gloeosporioides (15 469). The number of gene models in C. lentis is comparable with that of C. incanum , whose genome contains 11 852 gene models (Gan et al ., ).…”