Chromosome fusion and programmed DNA elimination shape karyotypes of nematodes.

An increasing number of metazoans undergo programmed DNA elimination (PDE), where a significant amount of DNA is selectively lost from the somatic genome during development. In some nematodes, PDE leads to the removal and remodeling of the ends of all germline chromosomes. In several species, PDE also generates internal breaks that lead to sequence loss and increased numbers of somatic chromosomes. The biological significance of these karyotype changes associated with PDE and the origin and evolution of nematode PDE remain largely unknown. Here, we assembled the single germline chromosome of the nematode Parascaris univalens and compared the karyotypes, chromosomal gene organization, and PDE features among other nematodes. We show that PDE in Parascaris converts an XX/XY sex-determination system in the germline into an XX/XO system in the somatic cells. Comparisons of Ascaris , Parascaris , and Baylisascaris ascarid chromosomes suggest that PDE existed in the ancestor of these nematodes, and their current distinct germline karyotypes were derived from fusion events of smaller ancestral chromosomes. The DNA breaks involved in PDE resolve these fused germline chromosomes into their pre-fusion karyotypes. These karyotype changes may lead to alterations in genome architecture and gene expression in the somatic cells. Cytological and genomic analyses further suggest that satellite DNA and the heterochromatic chromosome arms are dynamic and may play a role during meiosis. Overall, our results show that chromosome fusion and PDE have been harnessed in these ascarids to sculpt their karyotypes, altering the genome organization and serving specific functions in the germline and somatic cells. [Display omitted] • Complete genomes reveal karyotype differences in the Parascaris germline and soma • Current ascarid germline chromosomes are derived from fusion of smaller chromosomes • PDE converts distinct germline karyotypes to the same somatic karyotype in ascarids • PDE provides a means for organisms to benefit from both fused and split chromosomes Chromosome fusion and fission change karyotypes; they are prevalent in nematodes with holocentric chromosomes. Simmons et al. show some parasitic nematodes, including the unichromosomal Parascaris univalens , use programmed DNA elimination (PDE) to split evolutionarily fused germline chromosomes to restore their ancestral karyotype in somatic cells. [ABSTRACT FROM AUTHOR]