Evolutionary genomic analysis of the charcoal rot fungus macrophomina phaseolina for improved disease management under climate change

Global agricultural production is threatened by several diseases caused by fungal pathogens. Recently increased efforts to characterize genomic diversity in fungal pathogens and the availability of large-scale ecological datasets offer new opportunities for understanding pathogen adaptation. The twin lenses of population genomics and adaptive evolution are powerful frameworks to interpret this data because of characteristics of fungal pathogens in agroecosystems that allow for their rapid evolution. The environment, biotic and abiotic, is a major driver for the evolution of plant pathogens and greatly influences disease outcomes. Macrophomina phaseolina causes charcoal rot in many important economic and subsistence crops worldwide. Charcoal rot significantly reduces yield and seed quality of soybean and dry bean and has been recognized as a warm climate-driven disease of increasing concern for crop production under global climate change. Therefore, this dissertation investigated the genetic structure and adaptive potential of M. phaseolina to understand how this pathogen responds to hosts, fungicides, and climate and how to best manage and predict charcoal rot disease.To this end, I first characterized the genetic diversity and genotype-environment associations in M. phaseolina filling in fundamental knowledge of population structure and shedding light on climate adaptation. Population genomic analyses of 95 M. phaseolina isolates from soybean and dry bean across the continental US, Puerto Rico, and Colombia revealed geographic structure and diversification associated to climate. Phylogenomic and clustering approaches differentiated isolates into two main clades of the US and Colombian-Puerto Rican origins and five divergent genetic clusters within these clades. I identified a predominantly clonal structure in the US and a semi-clonal structure in Colombia and Puerto Rico. Limited genetic differentiation between isolates of soybean and dry bean origins was observed. Estimations of the independent contributions of neutral population structure, space, and climate to genetic variation, revealed that climate significantly contributes to genetic variation between genetic clusters. Genotype-environment associations implicated several genomic regions in M. phaseolina adaptation to climate and the loci significantly associated with multivariate climate were found near to genes related to fungal stress responses.Information on the efficacy of newer fungicides chemistries for charcoal rot management is lacking. Therefore, I characterized the in-vitro fungicide sensitivity of M. phaseolina to three major chemical classes of single-site fungicides, succinate dehydrogenase inhibitors (SDHI; boscalid) dicarboximides (iprodione) and demethylation inhibitors (DMI; prothioconazole). This study found no isolates in the US, Colombia or Puerto Rico that were insensitive to any of the fungicides tested. Isolates were most sensitive to prothioconazole indicating its potential use for charcoal rot management. Next, mutations in the fungicides target protein genes were investigated. No mutations that associated to levels of sensitivity to boscalid, iprodione and prothioconazole were found among our isolate collection. Finally, a preliminary ecoclimatic suitability model was developed and used to project the climatic suitability of M. phaseolina at a global scale. Importantly, this model predicted areas of high climatic suitability which may be at increased risk of disease.Results from this dissertation work inform and improve charcoal rot management strategies through better understanding of M. phaseolina genetic structure and adaptive potential, in-vitro efficacy of single-site fungicides and potential disease outcomes under a changing climate. Additionally, this research is expected to contribute to applied issues surrounding plant disease risk prediction, and more broadly predicting short-term evolution of M. phaseolina across climates. Ultimately, this research will lead to better understanding of disease outcomes and more efficient management of plant pathogens considering adaptive responses under a changing climate.