A large accessory genome and high recombination rates may influence global distribution and broad host range of the fungal plant pathogen Claviceps purpurea

Authors: WYKA, STEPHEN - Colorad0 State University; MONDO, STEPHEN - Energy Joint Genome Institute; LIU, MIAO - Agriculture And Agri-Food Canada; NALAM, V - Colorado State University; Broders, Kirk

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/21/2022
Publication Date: 2/10/2022
Citation: Wyka, S., Mondo, S., Liu, M., Nalam, V., Broders, K. 2022. A large accessory genome and high recombination rates may influence global distribution and broad host range of the fungal plant pathogen Claviceps purpurea. PLoS Pathogens. 17(2). Article e0263496. https://doi.org/10.1371/journal.pone.0263496.
DOI: https://doi.org/10.1371/journal.pone.0263496

Interpretive Summary: The cereal crop pathogen, Claviceps purpurea, which causes ergot on grain heads, poses a significant threat to agriculture and food safety due to various toxic alkaloids present in the sexual fruiting bodies which can cause severe ergot poisoning in humans and livestock. Due to these serious health concerns, the USDA has placed strict regulations on the amount of “ergoty” grain that can be accepted for food and livestock feed with varying thresholds existing for select grain types. C. purpurea is known for its wide host range, infecting a number of grass species including barley, rye, and wheat, and sporadic nature of disease epidemics. There are limited control measures available as fungicide application has proven ineffective and despite the best efforts of plant breeders, no resistance genes have been identified in barley, rye, or wheat to prevent infection by C. purpurea. The lack of host resistance may be a result of C. purpurea evolving as a defensive mutualist with native grasses as they are allowed to colonize the plant ovaries and impart anti-herbivory and increased cytokinin production resulting in increased seed biomass. To better understand the evolutionary history of this fungus we conducted a population genomic analysis of 24 C. pupurea genomes from multiple hosts and geographic regions in order to understand the evolution of genes involved with the infection process such as effectors and secondary metabolites, many of which are also toxic to humans and livestock. We observed limited selection on effector genes, but a strong positive selection pressure on secondary metabolite genes. These results indicate that secondary metabolites, and not effectors, 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 indicate that options for host resistance targets are limited in the pathogen population, so future control strategies will need to focus on cultural control strategies, as crop rotation, eliminating alternative hosts on field margins, and certified clean seed, all of which will reduce initial inoculum sources of this pathogen.

Technical Abstract: Pangenome analyses are increasingly being utilized to study the evolution of eukaryotic organisms. 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%), high recombination rates (' = 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 may be controlled by frequent recombination. We additionally identified that within the ergoline biosynthetic cluster the lpsA1 and lpsA2 were the result of a recombination event. However, the high recombination rates observed in C. purpurea may be influencing an overall trend of purifying selection across the genome. 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.