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Genomics of adaptive divergence in Fungi

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Convergent recombination cessation between mating-type genes and centromeres in selfing anther-smut fungi
Publication . Carpentier, Fantin; Rodríguez De La Vega, Ricardo C.; Branco, Sara; Snirc, Alodie; Coelho, Marco A.; Hood, Michael E.; Giraud, Tatiana; UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; Cold Spring Harbor Laboratory Press
The degree of selfing has major impacts on adaptability and is often controlled by molecular mechanisms determining mating compatibility. Changes in compatibility systems are therefore important evolutionary events, but their underlying genomic mechanisms are often poorly understood. Fungi display frequent shifts in compatibility systems, and their small genomes facilitate elucidation of the mechanisms involved. In particular, linkage between the pre- and postmating compatibility loci has evolved repeatedly, increasing the odds of gamete compatibility under selfing. Here, we studied the mating-type chromosomes of two anther-smut fungi with unlinked mating-type loci despite a self-fertilization mating system. Segregation analyses and comparisons of high-quality genome assemblies revealed that these two species displayed linkage between mating-type loci and their respective centromeres. This arrangement renders the same improved odds of gamete compatibility as direct linkage of the two mating-type loci under the automictic mating (intratetrad selfing) of anther-smut fungi. Recombination cessation was found associated with a large inversion in only one of the four linkage events. The lack of trans-specific polymorphism at genes located in nonrecombining regions and linkage date estimates indicated that the events of recombination cessation occurred independently in the two sister species. Our study shows that natural selection can repeatedly lead to similar genomic patterns and phenotypes, and that different evolutionary paths can lead to distinct yet equally beneficial responses to selection. Our study further highlights that automixis and gene linkage to centromeres have important genetic and evolutionary consequences, while being poorly recognized despite being present in a broad range of taxa.
Erratum: Convergent recombination cessation between mating-type genes and centromeres in selfing anther-smut fungi (Genome Research (2019) 29 (944-953) DOI: 10.1101/gr.242578.118)
Publication . Carpentier, Fantin; Rodríguez de la Vega, Ricardo C.; Branco, Sara; Snirc, Alodie; Coelho, Marco A.; Hood, Michael E.; Giraud, Tatiana; UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; Cold Spring Harbor Laboratory Press
The authors would like to correct an error in the phylogenetic tree in Figure 5B. The labels of two species (M. silenes-acaulis and M. violaceum s. str.) were inadvertently interchanged in the initial publication of this article. The corrected figure has been updated in the revised manuscript online. The authors apologize for any confusion this may have caused.
Multiple convergent supergene evolution events in mating-type chromosomes
Publication . Branco, Sara; Carpentier, Fantin; De La Vega, Ricardo C.Rodríguez; Badouin, Hélène; Snirc, Alodie; Le Prieur, Stéphanie; Coelho, Marco A.; De Vienne, Damien M.; Hartmann, Fanny E.; Begerow, Dominik; Hood, Michael E.; Giraud, Tatiana; UCIBIO - Applied Molecular Biosciences Unit; DCV - Departamento de Ciências da Vida; Nature Portfolio
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.

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European Commission

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FP7

Número da atribuição

309403

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