Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories

Abstract

The persistence of large blocks of homologous synteny and a high frequency of breakpoint reuse are distinctive features of mammalian chromosomes that are not well understood in evolutionary terms. To gain a better understanding of the evolutionary forces that affect genome architecture, synteny relationships among 10 amniotes (human, chimp, macaque, rat, mouse, pig, cattle, dog, opossum, and chicken) were compared at <1 human-Mbp resolution. Homologous synteny blocks (HSBs; N = 2233) and chromosome evolutionary breakpoint regions (EBRs; N = 1064) were identified from pairwise comparisons of all genomes. Analysis of the size distribution of HSBs shared in all 10 species' chromosomes (msHSBs) identified three (>20 Mbp) that are larger than expected by chance. Gene network analysis of msHSBs >3 human-Mbp and EBRs <1 Mbp demonstrated that msHSBs are significantly enriched for genes involved in development of the central nervous and other organ systems, whereas EBRs are enriched for genes associated with adaptive functions. In addition, we found EBRs are significantly enriched for structural variations (segmental duplications, copy number variants, and indels), retrotransposed and zinc finger genes, and single nucleotide polymorphisms. These results demonstrate that chromosome breakage in evolution is nonrandom and that HSBs and EBRs are evolving in distinctly different ways. We suggest that natural selection acts on the genome to maintain combinations of genes and their regulatory elements that are essential to fundamental processes of amniote development and biological organization. Furthermore, EBRs may be used extensively to generate new genetic variation and novel combinations of genes and regulatory elements that contribute to adaptive phenotypes.

Advances in Computer Simulation of Genome Evolution: Toward More Realistic Evolutionary Genomics Analysis by Approximate Bayesian Computation

“…The incorporation of these complex models of genome evolution in ABC techniques is not straightforward because different genomic regions may have evolved under different evolutionary histories (e.g., Larkin et al 2009) and may present a region-specific best-fit evolutionary model (Arbiza et al 2011). Thus, the first stage of an ABC methodology oriented to analyze genomic data accounting for complex genome evolution may involve the identification of those genomic regions that could have evolved under a specific evolutionary history and evolutionary process (Fig.…”

Cattle genomics and its implications for future nutritional strategies for dairy cattle

“…For example, Everts-van der Wind et al (2004) reported that evolutionary breakpoints between the cattle and human genomes are significantly enriched for genes. Recently, this observation was confirmed by multi-species genome comparisons (Murphy et al, 2005;Larkin et al, 2009). Subsequently, Larkin et al (2009) have shown that the amniote-specific EBRs are enriched for genes that involve an organism's response to external stimuli.…”

“…Recently, this observation was confirmed by multi-species genome comparisons (Murphy et al, 2005;Larkin et al, 2009). Subsequently, Larkin et al (2009) have shown that the amniote-specific EBRs are enriched for genes that involve an organism's response to external stimuli. In cattle, a cattle-specific EBR is associated with formation of a new bidirectional promoter that may affect control of expression of the CYB5R4 gene.…”

“…Unique genome features formed by cattle during the course of speciation and adaptation are reflected in the genome by gene mutations, sequence losses, duplications and repositions due to multiple chromosomal rearrangements that distinguish the cattle genome from other mammalian genomes and a putative mammalian ancestor (Murphy et al, 2005;The Bovine Genome Sequencing and Analysis Consortium, 2009;Larkin et al, 2009). On the other hand, when compared to other sequenced mammalian genomes, the cattle genome in some chromosomal regions still represents an ancestral organization, allowing for the detection of evolutionary events that happened in the course of genome evolution in other species (Murphy et al, 2005 Zimin et al (2009).…”

“…EBRs may be connected to the speciation due to changes in gene regulation and networks they may cause by moving genes to a new regulatory environment (Larkin et al, 2009) or causing gene duplications or deletions. Therefore, the detection of lineage-specific features formed in the regions of EBRs could facilitate decoding of the lineage-specific genetics and eventually may be used for effective genomic selection in agricultural species.…”