Title

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

Authors

Marta Farré, Royal Veterinary College University of London
Jaebum Kim, Konkuk University
Anastasia A. Proskuryakova, Institute of Molecular and Cellular Biology of the Siberian Branch of the RAS
Yang Zhang, Carnegie Mellon University
Anastasia I. Kulemzina, Institute of Molecular and Cellular Biology of the Siberian Branch of the RAS
Qiye Li, China National Genebank
Yang Zhou, China National Genebank
Yingqi Xiong, China National Genebank
Jennifer L. Johnson, University of Illinois Urbana-Champaign
Polina L. Perelman, Institute of Molecular and Cellular Biology of the Siberian Branch of the RAS
Warren E. Johnson, Conservation and Research Center (National Zoo)
Wesley C. Warren, University of Missouri
Anna V. Kukekova, University of Illinois Urbana-Champaign
Guojie Zhang, China National Genebank
Stephen J. O’Brien, Saint Petersburg State UniversityFollow
Oliver A. Ryder, Institute for Conservation Research
Alexander S. Graphodatsky, Institute of Molecular and Cellular Biology of the Siberian Branch of the RAS
Jian Ma, Carnegie Mellon University
Harris A. Lewin, University of California, Davis
Denis M. Larkin, Royal Veterinary College University of London

Document Type

Article

Publication Date

4-1-2019

Publication Title

Genome Research

ISSN

15495469

Volume

29

Issue/No.

4

First Page

576

Last Page

589

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, whereas 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. 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 colocalized with gross chromosome rearrangements may have provided valuable functional modifications that helped to shape ruminant evolution.

NSUWorks Citation

Farré, Marta; Jaebum Kim; Anastasia A. Proskuryakova; Yang Zhang; Anastasia I. Kulemzina; Qiye Li; Yang Zhou; Yingqi Xiong; Jennifer L. Johnson; Polina L. Perelman; Warren E. Johnson; Wesley C. Warren; Anna V. Kukekova; Guojie Zhang; Stephen J. O’Brien; Oliver A. Ryder; Alexander S. Graphodatsky; Jian Ma; Harris A. Lewin; and Denis M. Larkin. 2019. "Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks." Genome Research 29, (4): 576-589. doi:10.1101/gr.239863.118.

DOI

10.1101/gr.239863.118