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Genome Res. 2019 Feb 13. doi: 10.1101/gr.239863.118. [Epub ahead of print]

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

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Royal Veterinary College, University of London, London NW1 0TU, United Kingdom.
Department of Biomedical Science and Engineering, Konkuk University, Seoul 05029, Korea.
Institute of Molecular and Cellular Biology, SB RAS, Novosibirsk 630090, Russia.
Synthetic Biology Unit, Novosibirsk State University, Novosibirsk 630090, Russia.
Computational Biology Department, School of Computer Science, Carnegie Mellon University, Pittsburgh, Pennsylvania 15213, USA.
China National GeneBank, BGI-Shenzhen, Shenzhen 518083, China.
Department of Animal Sciences, College of Agricultural, Consumer and Environmental Sciences, University of Illinois at Urbana-Champaign, Urbana, Illinois 61801, USA.
Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, Virginia 22630, USA.
Walter Reed Biosystematics Unit, Museum Support Center, Smithsonian Institution, Suitland, Maryland 20746, USA.
Bond Life Sciences Center, University of Missouri, Columbia, Missouri 63201, USA.
State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China.
Centre for Social Evolution, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark.
Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, St. Petersburg 199004, Russia.
Guy Harvey Oceanographic Center, Halmos College of Natural Sciences and Oceanography, Nova Southeastern University, Fort Lauderdale, Florida 33004, USA.
Institute for Conservation Research, San Diego Zoo, Escondido, California 92027, USA.
Department of Evolution and Ecology and the UC Davis Genome Center, University of California, Davis, California 95616, USA.
The Federal Research Center Institute of Cytology and Genetics, The Siberian Branch of the Russian Academy of Sciences (ICG SB RAS), Novosibirsk 630090, Russia.
Contributed equally


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.


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