title: Reconstruction of ancestral chromosome architecture and gene repertoire reveals principles of genome evolution in a model yeast genus.
abstract: Reconstructing genome history is complex but necessary to reveal quantitative principles governing genome evolution. Such reconstruction requires recapitulating into a single evolutionary framework the evolution of genome architecture and gene repertoire. Here, we reconstructed the genome history of the genus Lachancea that appeared to cover a continuous evolutionary range from closely related to more diverged yeast species. Our approach integrated the generation of a high-quality genome data set; the development of AnChro, a new algorithm for reconstructing ancestral genome architecture; and a comprehensive analysis of gene repertoire evolution. We found that the ancestral genome of the genus Lachancea contained eight chromosomes and about 5173 protein-coding genes. Moreover, we characterized 24 horizontal gene transfers and 159 putative gene creation events that punctuated species diversification. We retraced all chromosomal rearrangements, including gene losses, gene duplications, chromosomal inversions and translocations at single gene resolution. Gene duplications outnumbered losses and balanced rearrangements with 1503, 929, and 423 events, respectively. Gene content variations between extant species are mainly driven by differential gene losses, while gene duplications remained globally constant in all lineages. Remarkably, we discovered that balanced chromosomal rearrangements could be responsible for up to 14% of all gene losses by disrupting genes at their breakpoints. Finally, we found that nonsynonymous substitutions reached fixation at a coordinated pace with chromosomal inversions, translocations, and duplications, but not deletions. Overall, we provide a granular view of genome evolution within an entire eukaryotic genus, linking gene content, chromosome rearrangements, and protein divergence into a single evolutionary framework.
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Nikolaos
authors.initials: N
authors.lastname: Vakirlis
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France;
authors.forename: Véronique
authors.initials: V
authors.lastname: Sarilar
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Guénola
authors.initials: G
authors.lastname: Drillon
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Aubin
authors.initials: A
authors.lastname: Fleiss
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Nicolas
authors.initials: N
authors.lastname: Agier
authors.affiliation: ISoft, Route de l'Orme, Parc "Les Algorithmes" Bâtiment Euclide, 91190 Saint-Aubin, France;
authors.forename: Jean-Philippe
authors.initials: JP
authors.lastname: Meyniel
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France;
authors.forename: Lou
authors.initials: L
authors.lastname: Blanpain
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Alessandra
authors.initials: A
authors.lastname: Carbone
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France;
authors.forename: Hugo
authors.initials: H
authors.lastname: Devillers
authors.affiliation: CRCM, CNRS, UMR7258, Inserm, U1068; Institut Paoli-Calmettes, Aix-Marseille Université, UM 105, F-13009, Marseille, France;
authors.forename: Kenny
authors.initials: K
authors.lastname: Dubois
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Alexandre
authors.initials: A
authors.lastname: Gillet-Markowska
authors.affiliation: ISoft, Route de l'Orme, Parc "Les Algorithmes" Bâtiment Euclide, 91190 Saint-Aubin, France;
authors.forename: Stéphane
authors.initials: S
authors.lastname: Graziani
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France;
authors.forename: Nguyen
authors.initials: N
authors.lastname: Huu-Vang
authors.affiliation: ISoft, Route de l'Orme, Parc "Les Algorithmes" Bâtiment Euclide, 91190 Saint-Aubin, France;
authors.forename: Marion
authors.initials: M
authors.lastname: Poirel
authors.affiliation: Department of Genetics, Genomics and Microbiology, University of Strasbourg/CNRS, UMR 7156, 67083 Strasbourg, France.
authors.forename: Cyrielle
authors.initials: C
authors.lastname: Reisser
authors.affiliation: CRCM, CNRS, UMR7258, Inserm, U1068; Institut Paoli-Calmettes, Aix-Marseille Université, UM 105, F-13009, Marseille, France;
authors.forename: Jonathan
authors.initials: J
authors.lastname: Schott
authors.affiliation: Department of Genetics, Genomics and Microbiology, University of Strasbourg/CNRS, UMR 7156, 67083 Strasbourg, France.
authors.forename: Joseph
authors.initials: J
authors.lastname: Schacherer
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Ingrid
authors.initials: I
authors.lastname: Lafontaine
authors.affiliation: CRCM, CNRS, UMR7258, Inserm, U1068; Institut Paoli-Calmettes, Aix-Marseille Université, UM 105, F-13009, Marseille, France;
authors.forename: Bertrand
authors.initials: B
authors.lastname: Llorente
authors.affiliation: Micalis Institute, INRA, AgroParisTech, Université Paris-Saclay, 78350 Jouy-en-Josas, France;
authors.forename: Cécile
authors.initials: C
authors.lastname: Neuvéglise
authors.affiliation: Sorbonne Universités, UPMC Univ. Paris 06, CNRS, Institut de Biologie Paris-Seine, Laboratory of Computational and Quantitative Biology, F-75005, Paris, France;
authors.forename: Gilles
authors.initials: G
authors.lastname: Fischer
mesh_terms: D001203:Ascomycota / Q000235:genetics*; D015825:Chromosomes, Fungal / Q000235:genetics*; D019143:Evolution, Molecular; D015321:Gene Rearrangement; D016681:Genome, Fungal; D008957:Models, Genetic; D010802:Phylogeny