A large accessory genome, high recombination rates, and selection of secondary metabolite genes help maintain global distribution and broad host range of the fungal plant pathogen Claviceps purpurea

Abstract

Pangenome analyses are increasingly being utilized to study the evolution of eukaryotic organisms, which is often governed by variable gene content. While pangenomes can provide insight into polymorphic gene content, inferences about the ecological and adaptive potential of such organisms also need to be accompanied by additional supportive genomic analyses. In this study we constructed a pangenome of Claviceps purpurea from 24 genomes and examined the positive selection and recombination landscape of an economically important fungal organism for pharmacology and agricultural research. Together, these analyses revealed that C. purpurea has a relatively large accessory genome ([~] 38%) that is likely maintained by high recombination rates ({rho} = 0.044) and transposon mediated gene duplication. However, due to observations of relatively low transposable element (TE) content (8.8%) and a lack of variability in genome sizes, prolific TE expansion is likely controlled by these high recombination rates, which may additionally be influencing the overall trend of purifying selection across the genome. Despite this trend, we observed a strong positive selection pressure on secondary metabolite genes, particularly within the ergoline biosynthetic cluster where we also revealed that the lpsA1 and lpsA2 genes were the result of a recombination event. These results indicate that secondary metabolites are primary factors affecting the diversification of the species into new ecological niches and help maintain its global distribution and broad host range. These results showcase the use of selection and recombination landscapes to identify mechanisms contributing to pangenome structure and primary factors influencing the evolution of an organism. Author SummaryThe use of genomic data to better understand the lifestyle of a pathogen and its relationship with its host has expanded our ability to investigate the evolutionary history of these organisms. This in turn has allowed us to decipher and understand the ambiguity surrounding the true nature of the fungal plant pathogen Claviceps purpurea. By combining three different types of broad genomic analyses we identified primary factors affecting the evolution and adaptive potential of this pathogen; particularly a large accessory genome, high recombination rates, and positive selection of genes associated with stress tolerance. These factors likely contribute to the pathogens global distribution and broad host range. Furthermore, these findings will influence the direction of future research into optimal control methods.