Linkage To The Mating-Type Locus Across The Genus Microbotryum: Insights Into Nonrecombining Chromosomes

Department of Biology, Amherst College, Amherst, Massachusetts 01002 Ecologie, Systématique et Evolution, Université Paris-Sud, F-91405 Orsay, France Comparative Genomics Group CRG-Centre for Genomic Regulation, Doctor Aiguader, 88, 08003 Barcelona, Spain Centro de Recursos Microbiológicos, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, 2829-516 Caparica, Portugal INRA, Unité de Recherche Génomique-Info, 78000 Versailles, France Genoscope, Centre National de Séquençage, UMR CNRS 8030, 2 rue Gaston Crémieux, CP 5706, 91507 Evry, France Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142 Department of Biology, Program on Disease Evolution, University of Louisville, Louisville, Kentucky 40292 E-mail: .
Evolution (Impact Factor: 4.61). 06/2012; 66(11). DOI: 10.1111/j.1558-5646.2012.01703.x


Parallels have been drawn between the evolution of nonrecombining regions in fungal mating-type chromosomes and animal and plant sex chromosomes, particularly regarding the stages of recombination cessation forming evolutionary strata of allelic divergence. Currently, evidence and explanations for recombination cessation in fungi are sparse, and the presence of evolutionary strata has been examined in a minimal number of fungal taxa. Here, the basidiomycete genus Microbotryum was used to determine the history of recombination cessation for loci on the mating-type chromosomes. Ancestry of linkage with mating type for 13 loci was assessed across 20 species by a phylogenetic method. No locus was found to exhibit trans-specific polymorphism for alternate alleles as old as the mating pheromone receptor, indicating that ages of linkage to mating type varied among the loci. The ordering of loci in the ancestry of linkage to mating type does not agree with their previously proposed assignments to evolutionary strata. This study suggests that processes capable of influencing divergence between alternate alleles may act at loci in the nonrecombining regions (e.g., gene conversion) and encourages further work to dissect the evolutionary processes acting upon genomic regions that determine mating compatibility

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    • "(Billiard et al., 2012; Nieuwenhuis et al., 2013), and within the region of suppressed recombination in Microbotryum spp. (Petit et al., 2012; Badouin et al., 2015; Fontanillas et al., 2015). Such a linkage of the pre-and post-mating compatibility genes may be advantageous under certain conditions (Nieuwenhuis et al., 2013; Vuilleumier et al., 2013). "
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    ABSTRACT: It is striking that, while central to sexual reproduction, the genomic regions determining sex or mating-types are often characterized by suppressed recombination that leads to a decrease in the efficiency of selection, shelters genetic load, and inevitably contributes to their genic degeneration. Research on model and lesser-explored fungi has revealed similarities in recombination suppression of the genomic regions involved in mating compatibility across eukaryotes, but fungi also provide opposite examples of enhanced recombination in the genomic regions that determine their mating types. These contrasted patterns of genetic recombination (sensu lato, including gene conversion and ectopic recombination) in regions of the genome involved in mating compatibility point to important yet complex processes occurring in their evolution. A number of pieces in this puzzle remain to be solved, in particular on the unclear selective forces that may cause the patterns of recombination, prompting theoretical developments and experimental studies. This review thus points to fungi as a fascinating group for studying the various evolutionary forces at play in the genomic regions involved in mating compatibility.
    Full-text · Article · Jul 2015 · Fungal Biology Reviews
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    • "We built a phylogeny of the Microbotryum species based upon the set of 5,453 POGs from non- MAT chromosomes (fig. 3); genes on the mating-type chromosomes were excluded because they may display trans-specific polymorphism that could blur species relationships (Devier, et al. 2009; Abbate and Hood 2010b; Petit, et al. 2012). The relationships between species were consistent with those reported previously for this fungal genus (Kemler, et al. 2006). "
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    ABSTRACT: Dimorphic mating-type chromosomes in fungi are excellent models for understanding the genomic consequences of recombination suppression. Their suppressed recombination and reduced effective population size are expected to limit the efficacy of natural selection, leading to genomic degeneration. Our aim was to identify the sequences of the mating-type chromosomes (a1 and a2) of the anther smut fungi and to investigate degeneration in their non-recombining regions. We used the haploid a1 Microbotryum lychnidis-dioicae reference genome sequence. The a1 and a2 mating-type chromosomes were both isolated electrophoretically and sequenced. Integration with restriction-digest optical maps identified regions of recombination and non-recombination in the mating-type chromosomes. Genome sequence data was also obtained for twelve other Microbotryum species. We found strong evidence of degeneration across the genus in the non-recombining regions of the mating-type chromosomes, with significantly higher rates of non-synonymous substitution (dN/dS) than in non-mating-type chromosomes or in recombining regions of the mating-type chromosomes. The non-recombining regions of the mating-type chromosomes also showed high transposable element content, weak gene expression and gene losses. The levels of degeneration did not differ between the a1 and a2 mating-type chromosomes, consistent with the lack of homogametic/heterogametic asymmetry between them, and contrasting with X/Y or Z/W sex chromosomes. © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    Full-text · Article · Dec 2014
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    • "For the a2 mating type, SAP PCR was not possible, and thus sequencing was performed to determine which genotype was successful. For the a2 mating type, the locus 236, linked to the sex chromosome [61], was sequenced and ambiguous peaks on the chromatograms were analyzed to determine which a2 species was present. Due to difficulties in genotyping, only 522 of 999 infected plants were genotyped (Table 2). "
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    ABSTRACT: Hybridization and reproductive isolation are central to the origin and maintenance of species, and especially for sympatric species, gene flow is often inhibited through barriers that depend upon mating compatibility factors. The anther-smut fungi (genus Microbotryum) serve as models for speciation in the face of sympatry, and previous studies have tested for but not detected assortative mating. In addition, post-mating barriers are indicated by reduced fitness of hybrids, but sources of those barriers (i.e. ecological maladaptation or genetic incompatibilities) have not yet been detected. Here, backcrossing experiments, specifically controlling for the fungal species origins of the mating compatibility factors, were used to investigate reproductive isolation in the recently-derived species Microbotryum lychnidis-dioicae and Microbotryum silenes-dioicae. Assortative mating was detected during backcrossing and was manifested by the preferential conjugation of the hybrid-produced gametes with non-hybrid gametes containing mating compatibility factors from the same parental species. Patterns of post-mating performance supported either a level of extrinsic isolation mechanism, where backcross progeny with a higher proportion of the pathogen genome adapted to the particular host environment were favored, or an infection advantage attributed to greater genetic contribution to the hybrid from the M. lychnidis-dioicae genome. The use of controlled backcrossing experiments reveals significant species-specific mating type effects on conjugations between recently-derived sister species, which are likely to play important roles in both maintaining species separation and the nature of hybrids lineages that emerge in sympatry between Microbotryum species.
    Full-text · Article · Oct 2013 · BMC Evolutionary Biology
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