Research output: Contribution to journal › Article › peer-review
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 journal › Article › peer-review
}
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.
PY - 2019/4
Y1 - 2019/4
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 - Биоинформатика
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
KW - RECONSTRUCTION
KW - RETROTRANSPOSONS
KW - REARRANGEMENTS
KW - DEER
KW - CHROMOSOMAL SPECIATION
KW - GENOME EVOLUTION
KW - SEQUENCE
KW - DIVERGENCE
KW - INSIGHTS
KW - INVERSIONS
UR - http://www.scopus.com/inward/record.url?scp=85064042581&partnerID=8YFLogxK
UR - http://www.mendeley.com/research/evolution-gene-regulation-ruminants-differs-between-evolutionary-breakpoint-regions-homologous-synte
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 -
ID: 49509702