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

Marta Farré, 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, Denis M. Larkin

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Pages (from-to)576-589
Number of pages14
JournalGenome Research
Volume29
Issue number4
DOIs
StatePublished - Apr 2019

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Synteny
Ruminants
Genes
DNA Transposable Elements
Chromosomes
Karyotype
Transcription Factors
Gene Expression
Livestock
Regulator Genes
Liver

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)

Cite this

Farré, M., Kim, J., Proskuryakova, A. A., Zhang, Y., Kulemzina, A. I., Li, Q., ... Larkin, D. M. (2019). Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks. Genome Research, 29(4), 576-589. https://doi.org/10.1101/gr.239863.118

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 L.; Johnson, Warren E.; Warren, Wesley C.; Kukekova, Anna V; Zhang, Guojie; O’Brien, Stephen J.; Ryder, Oliver A.; Graphodatsky, Alexander S.; Ma, Jian; Lewin, Harris A.; Larkin, Denis M.

In: Genome Research, Vol. 29, No. 4, 04.2019, p. 576-589.

Research output: Contribution to journalArticle

Farré, M, Kim, J, Proskuryakova, AA, Zhang, Y, Kulemzina, AI, Li, Q, Zhou, Y, Xiong, Y, Johnson, JL, Perelman, PL, Johnson, WE, Warren, WC, Kukekova, AV, Zhang, G, O’Brien, SJ, Ryder, OA, Graphodatsky, AS, Ma, J, Lewin, HA & Larkin, DM 2019, 'Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks', Genome Research, vol. 29, no. 4, pp. 576-589. https://doi.org/10.1101/gr.239863.118
Farré, Marta ; Kim, Jaebum ; Proskuryakova, Anastasia A. ; Zhang, Yang ; Kulemzina, Anastasia I. ; Li, Qiye ; Zhou, Yang ; Xiong, Yingqi ; Johnson, Jennifer L. ; Perelman, Polina L. ; Johnson, Warren E. ; Warren, Wesley C. ; Kukekova, Anna V ; Zhang, Guojie ; O’Brien, Stephen J. ; Ryder, Oliver A. ; Graphodatsky, Alexander S. ; Ma, Jian ; Lewin, Harris A. ; Larkin, Denis M. / Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks. In: Genome Research. 2019 ; Vol. 29, No. 4. pp. 576-589.
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