TY - JOUR

T1 - Evolution of gene regulation in ruminants differs between evolutionary breakpoint regions and homologous synteny blocks

AU - Farré, Marta

AU - Kim, Jaebum

AU - Proskuryakova, Anastasia A.

AU - Zhang, Yang

AU - Kulemzina, Anastasia I.

AU - Li, Qiye

AU - Zhou, Yang

AU - Xiong, Yingqi

AU - Johnson, Jennifer L.

AU - Perelman, Polina L.

AU - Johnson, Warren E.

AU - Warren, Wesley C.

AU - Kukekova, Anna V.

AU - Zhang, Guojie

AU - O’Brien, Stephen J.

AU - Ryder, Oliver A.

AU - Graphodatsky, Alexander S.

AU - Ma, Jian

AU - Lewin, Harris A.

AU - Larkin, Denis M.

N1 - © 2019 Farré et al.; Published by Cold Spring Harbor Laboratory Press.

PY - 2019/4/1

Y1 - 2019/4/1

N2 - 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.

AB - 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.

KW - Animals

KW - Chromosome Breakpoints

KW - DNA Transposable Elements

KW - Enhancer Elements, Genetic

KW - Evolution, Molecular

KW - Karyotype

KW - Protein Binding

KW - Ruminants/genetics

KW - Selection, Genetic

KW - Synteny

KW - Transcription Factors/metabolism

UR - http://www.scopus.com/inward/record.url?scp=85064042581&partnerID=8YFLogxK

U2 - 10.1101/gr.239863.118

DO - 10.1101/gr.239863.118

M3 - Article

C2 - 30760546

AN - SCOPUS:85064042581

VL - 29

SP - 576

EP - 589

JO - Genome Research

JF - Genome Research

SN - 1088-9051

IS - 4

ER -