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  • 1
    Online Resource
    Online Resource
    Multiple convergent supergene evolution events in mating-type chromosomes
    Springer Science and Business Media LLC ; 2018
    In:  Nature Communications Vol. 9, No. 1 ( 2018-05-21)
    Details
    In: Nature Communications, Springer Science and Business Media LLC, Vol. 9, No. 1 ( 2018-05-21)
    Abstract: Convergent adaptation provides unique insights into the predictability of evolution and ultimately into processes of biological diversification. Supergenes (beneficial gene linkage) are striking examples of adaptation, but little is known about their prevalence or evolution. A recent study on anther-smut fungi documented supergene formation by rearrangements linking two key mating-type loci, controlling pre- and post-mating compatibility. Here further high-quality genome assemblies reveal four additional independent cases of chromosomal rearrangements leading to regions of suppressed recombination linking these mating-type loci in closely related species. Such convergent transitions in genomic architecture of mating-type determination indicate strong selection favoring linkage of mating-type loci into cosegregating supergenes. We find independent evolutionary strata (stepwise recombination suppression) in several species, with extensive rearrangements, gene losses, and transposable element accumulation. We thus show remarkable convergence in mating-type chromosome evolution, recurrent supergene formation, and repeated evolution of similar phenotypes through different genomic changes.
    Type of Medium: Online Resource
    ISSN: 2041-1723
    URL: Article
    DOI: 10.1038/s41467-018-04380-9
    Language: English
    Publisher: Springer Science and Business Media LLC
    Publication Date: 2018
    detail.hit.zdb_id: 2553671-0
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  • 2
    Online Resource
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    Recombination suppression and evolutionary strata around mating‐type loci in fungi: documenting patterns and understanding evolutionary and mechanistic causes
    Wiley ; 2021
    In:  New Phytologist Vol. 229, No. 5 ( 2021-03), p. 2470-2491
    Details
    In: New Phytologist, Wiley, Vol. 229, No. 5 ( 2021-03), p. 2470-2491
    Abstract: Genomic regions determining sexual compatibility often display recombination suppression, as occurs in sex chromosomes, plant self‐incompatibility loci and fungal mating‐type loci. Regions lacking recombination can extend beyond the genes determining sexes or mating types, by several successive steps of recombination suppression. Here we review the evidence for recombination suppression around mating‐type loci in fungi, sometimes encompassing vast regions of the mating‐type chromosomes. The suppression of recombination at mating‐type loci in fungi has long been recognized and maintains the multiallelic combinations required for correct compatibility determination. We review more recent evidence for expansions of recombination suppression beyond mating‐type genes in fungi (‘evolutionary strata’), which have been little studied and may be more pervasive than commonly thought. We discuss testable hypotheses for the ultimate (evolutionary) and proximate (mechanistic) causes for such expansions of recombination suppression, including (1) antagonistic selection, (2) association of additional functions to mating‐type, such as uniparental mitochondria inheritance, (3) accumulation in the margin of nonrecombining regions of various factors, including deleterious mutations or transposable elements resulting from relaxed selection, or neutral rearrangements resulting from genetic drift. The study of recombination suppression in fungi could thus contribute to our understanding of recombination suppression expansion across a broader range of organisms.
    Type of Medium: Online Resource
    ISSN: 0028-646X , 1469-8137
    URL: Issue
    URL: Article
    DOI: 10.1111/nph.v229.5
    DOI: 10.1111/nph.17039
    Language: English
    Publisher: Wiley
    Publication Date: 2021
    detail.hit.zdb_id: 208885-X
    detail.hit.zdb_id: 1472194-6
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  • 3
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    Understanding Adaptation, Coevolution, Host Specialization, and Mating System in Castrating Anther-Smut Fungi by Combining Population and Comparative Genomics
    Annual Reviews ; 2019
    In:  Annual Review of Phytopathology Vol. 57, No. 1 ( 2019-08-25), p. 431-457
    Details
    In: Annual Review of Phytopathology, Annual Reviews, Vol. 57, No. 1 ( 2019-08-25), p. 431-457
    Abstract: Anther-smut fungi provide a powerful system to study host–pathogen specialization and coevolution, with hundreds of Microbotryum species specialized on diverse Caryophyllaceae plants, castrating their hosts through manipulation of the hosts’ reproductive organs to facilitate disease transmission. Microbotryum fungi have exceptional genomic characteristics, including dimorphic mating-type chromosomes, that make this genus anexcellent model for studying the evolution of mating systems and their influence on population genetics structure and adaptive potential. Important insights into adaptation, coevolution, host specialization, and mating system evolution have been gained using anther-smut fungi, with new insights made possible by the recent advent of genomic approaches. We illustrate with Microbotryum case studies how using a combination of comparative genomics, population genomics, and transcriptomics approaches enables the integration of different evolutionary perspectives across different timescales. We also highlight current challenges and suggest future studies that will contribute to advancing our understanding of the mechanisms underlying adaptive processes in populations of fungal pathogens.
    Type of Medium: Online Resource
    ISSN: 0066-4286 , 1545-2107
    URL: Issue
    URL: Article
    DOI: 10.1146/phyto.2019.57.issue-1
    DOI: 10.1146/annurev-phyto-082718-095947
    RVK:
    WA 15000
    Language: English
    Publisher: Annual Reviews
    Publication Date: 2019
    detail.hit.zdb_id: 1473792-9
    SSG: 12
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  • 4
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    Higher Gene Flow in Sex-Related Chromosomes than in Autosomes during Fungal Divergence
    Oxford University Press (OUP) ; 2020
    In:  Molecular Biology and Evolution Vol. 37, No. 3 ( 2020-03-01), p. 668-682
    Details
    In: Molecular Biology and Evolution, Oxford University Press (OUP), Vol. 37, No. 3 ( 2020-03-01), p. 668-682
    Abstract: Nonrecombining sex chromosomes are widely found to be more differentiated than autosomes among closely related species, due to smaller effective population size and/or to a disproportionally large-X effect in reproductive isolation. Although fungal mating-type chromosomes can also display large nonrecombining regions, their levels of differentiation compared with autosomes have been little studied. Anther-smut fungi from the Microbotryum genus are castrating pathogens of Caryophyllaceae plants with largely nonrecombining mating-type chromosomes. Using whole genome sequences of 40 fungal strains, we quantified genetic differentiation among strains isolated from the geographically overlapping North American species and subspecies of Silene virginica and S. caroliniana. We inferred that gene flow likely occurred at the early stages of divergence and then completely stopped. We identified large autosomal genomic regions with chromosomal inversions, with higher genetic divergence than the rest of the genomes and highly enriched in selective sweeps, supporting a role of rearrangements in preventing gene flow in genomic regions involved in ecological divergence. Unexpectedly, the nonrecombining mating-type chromosomes showed lower divergence than autosomes due to higher gene flow, which may be promoted by adaptive introgressions of less degenerated mating-type chromosomes. The fact that both mating-type chromosomes are always heterozygous and nonrecombining may explain such patterns that oppose to those found for XY or ZW sex chromosomes. The specific features of mating-type chromosomes may also apply to the UV sex chromosomes determining sexes at the haploid stage in algae and bryophytes and may help test general hypotheses on the evolutionary specificities of sex-related chromosomes.
    Type of Medium: Online Resource
    ISSN: 0737-4038 , 1537-1719
    URL: Article
    DOI: 10.1093/molbev/msz252
    Language: English
    Publisher: Oxford University Press (OUP)
    Publication Date: 2020
    detail.hit.zdb_id: 2024221-9
    SSG: 12
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  • 5
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    Genome‐wide evidence for divergent selection between populations of a major agricultural pathogen
    Wiley ; 2018
    In:  Molecular Ecology Vol. 27, No. 12 ( 2018-06), p. 2725-2741
    Details
    In: Molecular Ecology, Wiley, Vol. 27, No. 12 ( 2018-06), p. 2725-2741
    Abstract: The genetic and environmental homogeneity in agricultural ecosystems is thought to impose strong and uniform selection pressures. However, the impact of this selection on plant pathogen genomes remains largely unknown. We aimed to identify the proportion of the genome and the specific gene functions under positive selection in populations of the fungal wheat pathogen Zymoseptoria tritici . First, we performed genome scans in four field populations that were sampled from different continents and on distinct wheat cultivars to test which genomic regions are under recent selection. Based on extended haplotype homozygosity and composite likelihood ratio tests, we identified 384 and 81 selective sweeps affecting 4% and 0.5% of the 35 Mb core genome, respectively. We found differences both in the number and the position of selective sweeps across the genome between populations. Using a XtX‐based outlier detection approach, we identified 51 extremely divergent genomic regions between the allopatric populations, suggesting that divergent selection led to locally adapted pathogen populations. We performed an outlier detection analysis between two sympatric populations infecting two different wheat cultivars to identify evidence for host‐driven selection. Selective sweep regions harboured genes that are likely to play a role in successfully establishing host infections. We also identified secondary metabolite gene clusters and an enrichment in genes encoding transporter and protein localization functions. The latter gene functions mediate responses to environmental stress, including interactions with the host. The distinct gene functions under selection indicate that both local host genotypes and abiotic factors contributed to local adaptation.
    Type of Medium: Online Resource
    ISSN: 0962-1083 , 1365-294X
    URL: Issue
    URL: Article
    DOI: 10.1111/mec.2018.27.issue-12
    DOI: 10.1111/mec.14711
    RVK:
    WA 15000
    Language: English
    Publisher: Wiley
    Publication Date: 2018
    detail.hit.zdb_id: 2020749-9
    detail.hit.zdb_id: 1126687-9
    SSG: 12
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  • 6
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    The complex genomic basis of rapid convergent adaptation to pesticides across continents in a fungal plant pathogen
    Wiley ; 2021
    In:  Molecular Ecology Vol. 30, No. 21 ( 2021-11), p. 5390-5405
    Details
    In: Molecular Ecology, Wiley, Vol. 30, No. 21 ( 2021-11), p. 5390-5405
    Abstract: Convergent evolution leads to identical phenotypic traits in different species or populations. Convergence can be driven by standing variation allowing selection to favour identical alleles in parallel or the same mutations can arise independently. However, the molecular basis of such convergent adaptation remains often poorly resolved. Pesticide resistance in agricultural ecosystems is a hallmark of convergence in phenotypic traits. Here, we analyse the major fungal pathogen Zymoseptoria tritici causing serious losses on wheat and with fungicide resistance emergence across several continents. We sampled three population pairs each from a different continent spanning periods early and late in the application of fungicides. To identify causal loci for resistance, we combined knowledge from molecular genetics work and performed genome‐wide association studies (GWAS) on a global set of isolates. We discovered yet unknown factors in azole resistance including a gene encoding membrane associated functions. We found strong support for the “hotspot” model of resistance evolution with convergent changes in a small set of loci but additional loci showed more population‐specific allele frequency changes. Genome‐wide scans of selection showed that half of all known resistance loci were overlapping a selective sweep region. Hence, the application of fungicides was one of the major selective agents acting on the pathogen over the past decades. Furthermore, loci identified through GWAS showed the highest overlap with selective sweep regions underlining the importance to map phenotypic trait variation in evolving populations. Our population genomic analyses highlighted that both de novo mutations and gene flow contributed to convergent pesticide adaptation.
    Type of Medium: Online Resource
    ISSN: 0962-1083 , 1365-294X
    URL: Issue
    URL: Article
    DOI: 10.1111/mec.v30.21
    DOI: 10.1111/mec.15737
    RVK:
    WA 15000
    Language: English
    Publisher: Wiley
    Publication Date: 2021
    detail.hit.zdb_id: 2020749-9
    detail.hit.zdb_id: 1126687-9
    SSG: 12
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  • 7
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    Machine-learning predicts genomic determinants of meiosis-driven structural variation in a eukaryotic pathogen
    Springer Science and Business Media LLC ; 2021
    In:  Nature Communications Vol. 12, No. 1 ( 2021-06-10)
    Details
    In: Nature Communications, Springer Science and Business Media LLC, Vol. 12, No. 1 ( 2021-06-10)
    Abstract: Species harbor extensive structural variation underpinning recent adaptive evolution. However, the causality between genomic features and the induction of new rearrangements is poorly established. Here, we analyze a global set of telomere-to-telomere genome assemblies of a fungal pathogen of wheat to establish a nucleotide-level map of structural variation. We show that the recent emergence of pesticide resistance has been disproportionally driven by rearrangements. We use machine learning to train a model on structural variation events based on 30 chromosomal sequence features. We show that base composition and gene density are the major determinants of structural variation. Retrotransposons explain most inversion, indel and duplication events. We apply our model to Arabidopsis thaliana and show that our approach extends to more complex genomes. Finally, we analyze complete genomes of haploid offspring in a four-generation pedigree. Meiotic crossover locations are enriched for new rearrangements consistent with crossovers being mutational hotspots. The model trained on species-wide structural variation accurately predicts the position of 〉 74% of newly generated variants along the pedigree. The predictive power highlights causality between specific sequence features and the induction of chromosomal rearrangements. Our work demonstrates that training sequence-derived models can accurately identify regions of intrinsic DNA instability in eukaryotic genomes.
    Type of Medium: Online Resource
    ISSN: 2041-1723
    URL: Article
    DOI: 10.1038/s41467-021-23862-x
    Language: English
    Publisher: Springer Science and Business Media LLC
    Publication Date: 2021
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  • 8
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    A population-level invasion by transposable elements triggers genome expansion in a fungal pathogen
    eLife Sciences Publications, Ltd ; 2021
    In:  eLife Vol. 10 ( 2021-09-16)
    Details
    In: eLife, eLife Sciences Publications, Ltd, Vol. 10 ( 2021-09-16)
    Abstract: Genome evolution is driven by the activity of transposable elements (TEs). The spread of TEs can have deleterious effects including the destabilization of genome integrity and expansions. However, the precise triggers of genome expansions remain poorly understood because genome size evolution is typically investigated only among deeply divergent lineages. Here, we use a large population genomics dataset of 284 individuals from populations across the globe of Zymoseptoria tritici , a major fungal wheat pathogen. We built a robust map of genome-wide TE insertions and deletions to track a total of 2456 polymorphic loci within the species. We show that purifying selection substantially depressed TE frequencies in most populations, but some rare TEs have recently risen in frequency and likely confer benefits. We found that specific TE families have undergone a substantial genome-wide expansion from the pathogen’s center of origin to more recently founded populations. The most dramatic increase in TE insertions occurred between a pair of North American populations collected in the same field at an interval of 25 years. We find that both genome-wide counts of TE insertions and genome size have increased with colonization bottlenecks. Hence, the demographic history likely played a major role in shaping genome evolution within the species. We show that both the activation of specific TEs and relaxed purifying selection underpin this incipient expansion of the genome. Our study establishes a model to recapitulate TE-driven genome evolution over deeper evolutionary timescales.
    Type of Medium: Online Resource
    ISSN: 2050-084X
    URL: Article
    DOI: 10.7554/eLife.69249
    Language: English
    Publisher: eLife Sciences Publications, Ltd
    Publication Date: 2021
    detail.hit.zdb_id: 2687154-3
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  • 9
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    Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments
    Springer Science and Business Media LLC ; 2021
    In:  The ISME Journal Vol. 15, No. 5 ( 2021-05), p. 1402-1419
    Details
    In: The ISME Journal, Springer Science and Business Media LLC, Vol. 15, No. 5 ( 2021-05), p. 1402-1419
    Abstract: The adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding of how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used genome-wide association mapping coupled with genetic correlation analyses. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified negative genetic correlations among traits related to host colonization and survival in stressful environments. Such genetic constraints indicate that pleiotropic effects could limit the pathogen’s ability to cause host damage. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.
    Type of Medium: Online Resource
    ISSN: 1751-7362 , 1751-7370
    URL: Article
    DOI: 10.1038/s41396-020-00859-w
    Language: English
    Publisher: Springer Science and Business Media LLC
    Publication Date: 2021
    detail.hit.zdb_id: 2299378-2
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  • 10
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    A fungal wheat pathogen evolved host specialization by extensive chromosomal rearrangements
    Springer Science and Business Media LLC ; 2017
    In:  The ISME Journal Vol. 11, No. 5 ( 2017-5), p. 1189-1204
    Details
    In: The ISME Journal, Springer Science and Business Media LLC, Vol. 11, No. 5 ( 2017-5), p. 1189-1204
    Type of Medium: Online Resource
    ISSN: 1751-7362 , 1751-7370
    URL: Article
    DOI: 10.1038/ismej.2016.196
    Language: English
    Publisher: Springer Science and Business Media LLC
    Publication Date: 2017
    detail.hit.zdb_id: 2299378-2
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