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Population genomics of the maize pathogen Ustilago maydis: demographic history and role of virulence clusters in adaptation

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Haider,  Muhammad Bilal
Research Group Molecular Systems Evolution, Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;
IMPRS for Evolutionary Biology, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Dutheil,  Julien Y.
Research Group Molecular Systems Evolution, Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Max Planck Society;

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Citation

Schweizer, G., Haider, M. B., Barroso, G. V., Rossel, N., Munch, K., Kahmann, R., et al. (2021). Population genomics of the maize pathogen Ustilago maydis: demographic history and role of virulence clusters in adaptation. Genome Biology and Evolution, 13(5): evab073. doi:10.1093/gbe/evab073.


Cite as: https://hdl.handle.net/21.11116/0000-000A-185A-7
Abstract
The tight interaction between pathogens and their hosts results in
reciprocal selective forces that impact the genetic diversity of the
interacting species. The footprints of this selection differ between
pathosystems because of distinct life-history traits, demographic
histories, or genome architectures. Here, we studied the genome-wide
patterns of genetic diversity of 22 isolates of the causative agent of
the corn smut disease, Ustilago maydis, originating from five locations
in Mexico, the presumed center of origin of this species. In this
species, many genes encoding secreted effector proteins reside in
so-called virulence clusters in the genome, an arrangement that is so
far not found in other filamentous plant pathogens. Using a combination
of population genomic statistical analyses, we assessed the
geographical, historical, and genome-wide variation of genetic diversity
in this fungal pathogen. We report evidence of two partially admixed
subpopulations that are only loosely associated with geographic origin.
Using the multiple sequentially Markov coalescent model, we inferred the
demographic history of the two pathogen subpopulations over the last 0.5
Myr. We show that both populations experienced a recent strong
bottleneck starting around 10,000years ago, coinciding with the assumed
time of maize domestication. Although the genome average genetic
diversity is low compared with other fungal pathogens, we estimated that
the rate of nonsynonymous adaptive substitutions is three times higher
in genes located within virulence clusters compared with nonclustered
genes, including nonclustered effector genes. These results highlight
the role that these singular genomic regions play in the evolution of
this pathogen.