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Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks

Farré, Marta, Kim, Jaebum, Proskuryakova, Anastasia A, Zhang, Yang, Kulemzina, Anastasia I, Li, Qiye, Zhou, Yang, Xiong, Yingqi, Johnson, Jennifer L, Perelman, Polina, and others. (2019) Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks. Genome Research, 29 . pp. 576-589. ISSN 1549-5469. (doi:10.1101/gr.239863.118) (KAR id:72776)

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Abstract

The role of chromosome rearrangements in driving evolution has been a long-standing question of evolutionary biology. Here we focused on ruminants as a model to assess how rearrangements may have contributed to the evolution of gene regulation. Using reconstructed ancestral karyotypes of Cetartiodactyls, Ruminants, Pecorans, and Bovids, we traced patterns of gross chromosome changes. We found that the lineage leading to the ruminant ancestor after the split from other cetartiodactyls, was characterized by mostly intrachromosomal changes while the lineage leading to the pecoran ancestor (including all livestock ruminants) included multiple interchromosomal changes. We observed that the liver cell putative enhancers in the ruminant evolutionary breakpoint regions are highly enriched for DNA sequences under selective constraint acting on lineage-specific transposable elements (TEs) and a set of 25 specific transcription factor (TF) binding motifs associated with recently active TEs. Coupled with gene expression data, we found that genes near ruminant breakpoint regions exhibit more divergent expression profiles among species, particularly in cattle, which is consistent with the phylogenetic origin of these breakpoint regions. Notably, this divergence was significantly greater in genes with enhancers that contain at least one of the 25 specific TF binding motifs and located near bovidae-to-cattle lineage breakpoint regions. Taken together, by combining ancestral karyotype reconstructions with analysis of cis regulatory element and gene expression evolution, our work demonstrated that lineage-specific regulatory elements co-localized with gross chromosome rearrangements may have provided valuable functional modifications that helped to shape ruminant evolution.

Item Type: Article
DOI/Identification number: 10.1101/gr.239863.118
Uncontrolled keywords: ruminants, chromosome rearrangements, ancestral karyotypes, regulatory elements, evolution, School of Biosciences
Divisions: Divisions > Division of Natural Sciences > Biosciences
Depositing User: Marta Farre Belmonte
Date Deposited: 27 Feb 2019 09:52 UTC
Last Modified: 04 Jul 2023 12:46 UTC
Resource URI: https://kar.kent.ac.uk/id/eprint/72776 (The current URI for this page, for reference purposes)

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