Population genomics of Macrophomina spp. reveals cryptic host specialization and evidence for meiotic recombination

Pennerman, K. K.; Goldman, P.; Dilla-Ermita, C. J.; Ramos, G.; Jaime, J. H.; Lopez-Hernandez, J.; Ramos, J.; Aviles, M.; Borrero, C.; Gomez, A.; Neal, J.; Chilvers, M.; Ortiz, V.; Stukenbrock, E. H.; Goldman, G. H.; Mengistu, A.; Lopez-Nicora, H. D.; Sacher, G. O.; Vaghefi, N.; Kiss, L.; Benz, J. P.; Machado, A. R.; Seijo, T.; Peres, N.; Martin, F. N.; Broome, J.; Ivors, K.; Cole, G. S.; Knapp, S. J.; McFarlane, D. J.; Mattner, S. W.; Gambardella, M.; Henry, P. M.

doi:10.1101/2024.09.03.609457

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bioRxiv · 10.1101/2024.09.03.609457

Population genomics of Macrophomina spp. reveals cryptic host specialization and evidence for meiotic recombination

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Abstract

Knowledge of the factors structuring populations of pathogenic fungi is fundamental to disease management efforts and basic biology. High-quality short-read sequence data were obtained for 463 Macrophomina spp. isolates collected from 91 host plant species and soil in 23 countries. Analyses revealed high diversity, admixture, and equal mating type ratios suggesting on-going recombination. Although most tested isolates could asymptomatically colonize strawberry, only isolates from a single phylogroup caused disease. In addition to strawberry, evidence for host specialization was discovered for soybean, demonstrating this broad host range pathogen contains phylogroups with cryptic specialization. Geography x isolate genotype associations were weak, suggesting these species were frequently trafficked between regions. Re-analysis using genomic data supported current species boundaries, and new molecular markers were designed to specifically identify each species. Contrary to expectations, M. phaseolina should be considered a species with both specialist and generalist populations for which meiosis can increase genetic diversity.

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Pennerman, K. K., Goldman, P., Dilla-Ermita, C. J., Ramos, G., Jaime, J. H., Lopez-Hernandez, J., Ramos, J., Aviles, M., Borrero, C., Gomez, A., Neal, J., Chilvers, M., Ortiz, V., Stukenbrock, E. H., Goldman, G. H., Mengistu, A., Lopez-Nicora, H. D., Sacher, G. O., Vaghefi, N., Kiss, L., Benz, J. P., Machado, A. R., Seijo, T., Peres, N., Martin, F. N., Broome, J., Ivors, K., Cole, G. S., Knapp, S. J., McFarlane, D. J., Mattner, S. W., Gambardella, M., Henry, P. M.. 2024-09-03. Population genomics of Macrophomina spp. reveals cryptic host specialization and evidence for meiotic recombination. https://doi.org/10.1101/2024.09.03.609457

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