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The genomic determinants of adaptive evolution in a fungal pathogen.

ABSTRACT: Unravelling the strength, frequency, and distribution of selective variants along the genome as well as the underlying factors shaping this distribution are fundamental goals of evolutionary biology. Antagonistic host-pathogen coevolution is thought to be a major driver of genome evolution between interacting species. While rapid evolution of pathogens has been documented in several model organisms, the genetic mechanisms of their adaptation are still poorly understood and debated, particularly the role of sexual reproduction. Here, we apply a population genomic approach to infer genome-wide patterns of selection among 13 isolates of Zymoseptoria tritici, a fungal pathogen characterized by extremely high genetic diversity, gene density, and recombination rates. We report that the genome of Z. tritici undergoes a high rate of adaptive substitutions, with 44% of nonsynonymous substitutions being adaptive on average. This fraction reaches 68% in so-called effector genes encoding determinants of pathogenicity, and the distribution of fitness effects differs in this class of genes as they undergo adaptive mutations with stronger positive fitness effects, but also more slightly deleterious mutations. Besides the globally high rate of adaptive substitutions, we report a negative relationship between pN/pS and the fine-scale recombination rate and a strong positive correlation between the rate of adaptive nonsynonymous substitutions (?a) and recombination rate. This result suggests a pervasive role of both background selection and Hill-Robertson interference even in a species with an exceptionally high recombination rate (60 cM/Mb on average). While transposable elements (TEs) have been suggested to contribute to adaptation by creating compartments of fast-evolving genomic regions, we do not find a significant effect of TEs on the rate of adaptive mutations. Overall our study suggests that sexual recombination is a significant driver of genome evolution, even in rapidly evolving organisms subject to recurrent mutations with large positive effects.

SUBMITTER: Grandaubert J

PROVIDER: S-EPMC6546377 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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The genomic determinants of adaptive evolution in a fungal pathogen.

Grandaubert Jonathan J Dutheil Julien Y JY Stukenbrock Eva H EH

Evolution letters 20190501 3

Unravelling the strength, frequency, and distribution of selective variants along the genome as well as the underlying factors shaping this distribution are fundamental goals of evolutionary biology. Antagonistic host-pathogen coevolution is thought to be a major driver of genome evolution between interacting species. While rapid evolution of pathogens has been documented in several model organisms, the genetic mechanisms of their adaptation are still poorly understood and debated, particularly ...[more]

PMID: 31171985

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Project description:BackgroundPowdery mildew, caused by the obligate biotrophic fungus Erysiphe necator, is an economically important disease of grapevines worldwide. Large quantities of fungicides are used for its control, accelerating the incidence of fungicide-resistance. Copy number variations (CNVs) are unbalanced changes in the structure of the genome that have been associated with complex traits. In addition to providing the first description of the large and highly repetitive genome of E. necator, this study describes the impact of genomic structural variation on fungicide resistance in Erysiphe necator.ResultsA shotgun approach was applied to sequence and assemble the genome of five E. necator isolates, and RNA-seq and comparative genomics were used to predict and annotate protein-coding genes. Our results show that the E. necator genome is exceptionally large and repetitive and suggest that transposable elements are responsible for genome expansion. Frequent structural variations were found between isolates and included copy number variation in EnCYP51, the target of the commonly used sterol demethylase inhibitor (DMI) fungicides. A panel of 89 additional E. necator isolates collected from diverse vineyard sites was screened for copy number variation in the EnCYP51 gene and for presence/absence of a point mutation (Y136F) known to result in higher fungicide tolerance. We show that an increase in EnCYP51 copy number is significantly more likely to be detected in isolates collected from fungicide-treated vineyards. Increased EnCYP51 copy numbers were detected with the Y136F allele, suggesting that an increase in copy number becomes advantageous only after the fungicide-tolerant allele is acquired. We also show that EnCYP51 copy number influences expression in a gene-dose dependent manner and correlates with fungal growth in the presence of a DMI fungicide.ConclusionsTaken together our results show that CNV can be adaptive in the development of resistance to fungicides by providing increasing quantitative protection in a gene-dosage dependent manner. The results of this work not only demonstrate the effectiveness of using genomics to dissect complex traits in organisms with very limited molecular information, but also may have broader implications for understanding genomic dynamics in response to strong selective pressure in other pathogens with similar genome architectures.

Dataset Information

The genomic determinants of adaptive evolution in a fungal pathogen.

Publications

The genomic determinants of adaptive evolution in a fungal pathogen.

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