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

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.

Analysis of muntjac deer genome and chromatin architecture reveals rapid karyotype evolution

“…In both assemblies, over 92% of contig sequence is anchored to chromosomes. Compared with publicly available assemblies 17,18 , the assemblies described here represent a hundredfold improvement in scaffold N50 length and severalfold improvement in contig N50 length. As typical for short-read assemblies, our muntjac assemblies are largely complete with respect to genic sequences (see below) but likely underrepresent repetitive sequences such as pericentromeric heterochromatin and repetitive subtelomeric regions, precluding further analysis of the sequence at fusions sites.…”

“…Building on these pioneering cytogenetic efforts, we set out to explore muntjac karyotype evolution using genome sequence comparisons. To this end, we produced the first chromosome-scale assemblies of both M. muntjak and M. reevesi , described below, with contiguity metrics that surpass those of earlier draft assemblies 17 , 18 . For comparative purposes, we leveraged published chromosome-scale assemblies of Bos taurus (cow) 19 and Cervus elaphus (red deer) 20 as well as a sub-chromosome assembly of Rangifer tarandus (reindeer) 21 to map karyotype changes across the cervid lineage.…”

Chromosome-scale genome assemblies of aphids reveal extensively rearranged autosomes and long-term conservation of the X chromosome

“…Chromosomes may undergo extensive rearrangement via inversions, translocations, fusions and fissions (Eichler and Sankoff 2003). These macro-mutations can have dramatic consequences by altering gene regulation (Farré et al 2019;Stewart and Rogers 2019) and modifying local recombination rates (Farré et al 2013;Martin et al 2019), and they are implicated in key evolutionary processes such as adaptation and speciation (Rieseberg 2001;Kirkpatrick and Barton 2006;Chang et al 2013;Guerrero and Kirkpatrick 2014;Fuller et al 2019;Wellband et al 2019). Chromosome-scale genome assemblies are required to study such macro-mutations, and recent advances in genome assembly have reinvigorated the field (e.g.…”

Comparative Chromosome Mapping of Musk Ox and the X Chromosome among Some Bovidae Species

“…The use of high-resolution dromedary probes [5] and BAC mapping [9,15] has provided increased precision with respect to syntenic segments orientation relative to centromeres and inversions. Proposed ancestral Bovidae and pecoran karyotypes were imputed based on genomic [16] and cytogenetic data [5,16,17]. Although the diploid chromosome number of Bovidae species ranges from 30 to 60, the number of autosomal arms in karyotypes is stable at 58 for most karyotyped species [18].…”