Abstract
Eukaryotic chromosomes have phylogenetic persistence. In many taxa, each chromosome has a single functional centromere with essential roles in spindle attachment and segregation. Fusion and fission can generate chromosomes with no or multiple centromeres, leading to genome instability. Groups with holocentric chromosomes (where centromeric function is distributed along each chromosome) might be expected to show karyotypic instability. This is generally not the case, and in Caenorhabditis elegans, it has been proposed that the role of maintenance of a stable karyotype has been transferred to the meiotic pairing centers, which are found at one end of each chromosome. Here, we explore the phylogenetic stability of nematode chromosomes using a new telomere-to-telomere assembly of the rhabditine nematode Oscheius tipulae generated from nanopore long reads. The 60-Mb O. tipulae genome is resolved into six chromosomal molecules. We find the evidence of specific chromatin diminution at all telomeres. Comparing this chromosomal O. tipulae assembly with chromosomal assemblies of diverse rhabditid nematodes, we identify seven ancestral chromosomal elements (Nigon elements) and present a model for the evolution of nematode chromosomes through rearrangement and fusion of these elements. We identify frequent fusion events involving NigonX, the element associated with the rhabditid X chromosome, and thus sex chromosome-associated gene sets differ markedly between species. Despite the karyotypic stability, gene order within chromosomes defined by Nigon elements is not conserved. Our model for nematode chromosome evolution provides a platform for investigation of the tensions between local genome rearrangement and karyotypic evolution in generating extant genome architectures.
Highlights
Linear chromosomes are basic elements of the organization of eukaryotic nuclear genomes
This is generally not the case, and in Caenorhabditis elegans, it has been proposed that the role of maintenance of a stable karyotype has been transferred to the meiotic pairing centers, which are found at one end of each chromosome
We identified loci that are found on the same chromosomal unit in multiple species using a subset of nine genome assemblies that are resolved into chromosomes: Auanema rhodensis (Tandonnet et al 2019), Brugia malayi (Foster et al 2020), Haemonchus contortus (Laing et al 2016), Meloidogyne hapla (Opperman et al 2008), Onchocerca volvulus (Cotton et al 2016), O. tipulae, Pristionchus pacificus (Rodelsperger et al 2017), Steinernema carpocapsae (Serra et al 2019), and Strongyloides ratti (Nemetschke et al 2010b)
Summary
Linear chromosomes are basic elements of the organization of eukaryotic nuclear genomes. The number of chromosomes and the position of orthologous loci on them are generally conserved between closely related species, and conserved karyotypic elements have been identified even between distantly related taxa (Jaillon et al 2004; Putnam et al 2007; Nakatani et al 2007). The evolutionary trajectories of genes, in terms of rate of drift and efficiency of selection, are influenced by their chromosomal location. Genes on sex chromosomes will be exposed as haploid in the heterogametic sex (whether X0, XY, or WZ), and their effective population size will be only 0.75 that of autosomal loci. Gene evolution is shaped by placement within chromosomes, with some regions, such as centromeres and subtelomeric regions experiencing higher rates of per-base and structural change (Rockman and Kruglyak 2009). For some sets of loci, such as HOX and paraHOX loci in most Metazoa, this constraint is evident between organisms that last shared common ancestors hundreds of millions of years ago (Krumlauf 2018)
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