Natural Selection on Coding and Noncoding DNA Sequences Is Associated with Virulence Genes in a Plant Pathogenic Fungus

Abstract

Natural selection leaves imprints on DNA, offering the opportunity to identify functionally important regions of the genome. Identifying the genomic regions affected by natural selection within pathogens can aid in the pursuit of effective strategies to control diseases. In this study, we analyzed genome-wide patterns of selection acting on different classes of sequences in a worldwide sample of eight strains of the model plant-pathogenic fungus Colletotrichum graminicola. We found evidence of selective sweeps, balancing selection, and positive selection affecting both protein-coding and noncoding DNA of pathogenicity-related sequences. Genes encoding putative effector proteins and secondary metabolite biosynthetic enzymes show evidence of positive selection acting on the coding sequence, consistent with an Arms Race model of evolution. The 5′ untranslated regions (UTRs) of genes coding for effector proteins and genes upregulated during infection show an excess of high-frequency polymorphisms likely the consequence of balancing selection and consistent with the Red Queen hypothesis of evolution acting on these putative regulatory sequences. Based on the findings of this work, we propose that even though adaptive substitutions on coding sequences are important for proteins that interact directly with the host, polymorphisms in the regulatory sequences may confer flexibility of gene expression in the virulence processes of this important plant pathogen.

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

“…There was transcript evidence for only one of them (Additional file 5: Table S4). The apparent low number of strain-specific SSPs in C. graminicola is consistent with an earlier report [120] that suggested that differences in expression may be more important than presence-absence polymorphisms for pathotype identity.…”

A highly conserved metalloprotease effector enhances virulence in the maize anthracnose fungus Colletotrichum graminicola

“…Interestingly, our previous genome‐wide survey of selection in C. graminicola did not detect positive selection in the coding sequence of these genes. Instead, we found evidence of positive selection in the flanking non‐coding parts of the gene, suggesting selection for the transcriptional profile (Rech et al ., ).…”

Subtle genetic population structure in Pacific halibut Hippoglossus stenolepis

“…Both loci differentiated samples from the Aleutian Islands from other samples. It is unclear if the EST s linked to the loci used in this study are under selection, but many studies have identified natural selection operating on markers linked to coding regions in other organisms (Bustamante et al ., ; Elmer et al ., ; Rech et al ., ). The results from this analysis suggest that selection may contribute to differentiation of Aleutian Island samples and further investigation is warranted.…”