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2. Analysis of fine-scale mammalian evolutionary breakpoints provides new insight into their relation to genome organisation

Author

Claire Lemaitre, Benjamin Audit, Alain Arneodo, Lamia Zaghloul, Marie-France Sagot, Eric Tannier, Christian Gautier, Université Sciences et Technologies - Bordeaux 1 (UB), Université de Lyon, Baobab, Département PEGASE [LBBE] (PEGASE), Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), An algorithmic view on genomes, cells, and environments (BAMBOO), Inria Grenoble - Rhône-Alpes, Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE), Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS), Laboratoire Joliot Curie, École normale supérieure de Lyon (ENS de Lyon)-Centre National de la Recherche Scientifique (CNRS), Bioinformatique, phylogénie et génomique évolutive (BPGE), Université Sciences et Technologies - Bordeaux 1, and École normale supérieure - Lyon (ENS Lyon)-Centre National de la Recherche Scientifique (CNRS)

Subjects
Genome evolution, lcsh:QH426-470, lcsh:Biotechnology, Genomics, Biology, Genome, Evolution, Molecular, 03 medical and health sciences, 0302 clinical medicine, Intergenic region, lcsh:TP248.13-248.65, [SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Genomics [q-bio.GN], Genetics, Animals, Humans, Gene, 030304 developmental biology, Mammals, Base Composition, 0303 health sciences, Models, Genetic, Genome, Human, Breakpoint, Chromosome Mapping, Chromosome Breakage, Chromosomes, Mammalian, lcsh:Genetics, Evolutionary biology, Human genome, Chromosome breakage, Isochores, 030217 neurology & neurosurgery, Research Article, Biotechnology
Abstract

Background The Intergenic Breakage Model, which is the current model of structural genome evolution, considers that evolutionary rearrangement breakages happen with a uniform propensity along the genome but are selected against in genes, their regulatory regions and in-between. However, a growing body of evidence shows that there exists regions along mammalian genomes that present a high susceptibility to breakage. We reconsidered this question taking advantage of a recently published methodology for the precise detection of rearrangement breakpoints based on pairwise genome comparisons. Results We applied this methodology between the genome of human and those of five sequenced eutherian mammals which allowed us to delineate evolutionary breakpoint regions along the human genome with a finer resolution (median size 26.6 kb) than obtained before. We investigated the distribution of these breakpoints with respect to genome organisation into domains of different activity. In agreement with the Intergenic Breakage Model, we observed that breakpoints are under-represented in genes. Surprisingly however, the density of breakpoints in small intergenes (1 per Mb) appears significantly higher than in gene deserts (0.1 per Mb). More generally, we found a heterogeneous distribution of breakpoints that follows the organisation of the genome into isochores (breakpoints are more frequent in GC-rich regions). We then discuss the hypothesis that regions with an enhanced susceptibility to breakage correspond to regions of high transcriptional activity and replication initiation. Conclusion We propose a model to describe the heterogeneous distribution of evolutionary breakpoints along human chromosomes that combines natural selection and a mutational bias linked to local open chromatin state.

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