Large-scale detection and characterization of interchromosomal rearrangements in normozoospermic bulls using massive genotype and phenotype data sets
- Jeanlin Jourdain1,2,
- Harmonie Barasc3,
- Thomas Faraut3,
- Anne Calgaro3,
- Nathalie Bonnet3,
- Camille Marcuzzo4,
- Amandine Suin4,
- Anne Barbat2,
- Chris Hozé1,2,
- Florian Besnard2,5,
- Sébastien Taussat1,2,
- Cécile Grohs2,
- Claire Kuchly4,
- Carole Iampietro4,
- Cécile Donnadieu4,
- Alain Pinton3,
- Didier Boichard2 and
- Aurélien Capitan1,2
- 1Eliance, 75012 Paris, France;
- 2Université Paris-Saclay, INRAE, AgroParisTech, GABI, G2B, 78350 Jouy-en-Josas, France;
- 3GenPhySE, Université de Toulouse, INRAE, ENVT, 31320 Castanet-Tolosan, France;
- 4INRAE, US 1426, GeT-PlaGe, Genotoul, France Génomique, Université Fédérale de Toulouse, 31320 Castanet-Tolosan, France;
- 5Idele, 75012 Paris, France
Abstract
In this paper, we developed a highly sensitive approach to detect interchromosomal rearrangements in cattle by searching for abnormal linkage disequilibrium patterns between markers located on different chromosomes in large paternal half-sib families genotyped as part of routine genomic evaluations. We screened 5571 families of artificial insemination sires from 15 breeds and revealed 13 putative interchromosomal rearrangements, 12 of which were validated by cytogenetic analysis and long-read sequencing. These consisted of one Robertsonian fusion, 10 reciprocal translocations, and the first case of insertional translocation reported in cattle. Taking advantage of the wealth of data available in cattle, we performed a series of complementary analyses to define the exact nature of these rearrangements, investigate their origins, and search for factors that may have favored their occurrence. We also evaluated the risks to the livestock industry and showed significant negative effects on several traits in the sires and in their balanced or aneuploid progeny compared with wild-type controls. Thus, we present the most comprehensive and thorough screen for interchromosomal rearrangements compatible with normal spermatogenesis in livestock species. This approach is readily applicable to any population that benefits from large genotype data sets, and will have direct applications in animal breeding. Finally, it also offers interesting prospects for basic research by allowing the detection of smaller and rarer types of chromosomal rearrangements than GTG banding, which are interesting models for studying gene regulation and the organization of genome structure.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at https://www.genome.org/cgi/doi/10.1101/gr.277787.123.
- Received February 15, 2023.
- Accepted May 19, 2023.
This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see https://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
