Genome Architecture and Evolution of a Unichromosomal Asexual Nematode

Hélène Fradin, Karin Kiontke, Charles Zegar, Michelle Gutwein, Jessica Lucas, Mikhail Kovtun, David L. Corcoran, L. Ryan Baugh, David H.A. Fitch, Fabio Piano, Kristin C. Gunsalus

Research output: Contribution to journalArticle

Abstract

Asexual reproduction in animals, though rare, is the main or exclusive mode of reproduction in some long-lived lineages. The longevity of asexual clades may be correlated with the maintenance of heterozygosity by mechanisms that rearrange genomes and reduce recombination. Asexual species thus provide an opportunity to gain insight into the relationship between molecular changes, genome architecture, and cellular processes. Here we report the genome sequence of the parthenogenetic nematode Diploscapter pachys with only one chromosome pair. We show that this unichromosomal architecture is shared by a long-lived clade of asexual nematodes closely related to the genetic model organism Caenorhabditis elegans. Analysis of the genome assembly reveals that the unitary chromosome arose through fusion of six ancestral chromosomes, with extensive rearrangement among neighboring regions. Typical nematode telomeres and telomeric protection-encoding genes are lacking. Most regions show significant heterozygosity; homozygosity is largely concentrated to one region and attributed to gene conversion. Cell-biological and molecular evidence is consistent with the absence of key features of meiosis I, including synapsis and recombination. We propose that D. pachys preserves heterozygosity and produces diploid embryos without fertilization through a truncated meiosis. As a prelude to functional studies, we demonstrate that D. pachys is amenable to experimental manipulation by RNA interference. By genome sequencing, Fradin et al. discover that the single chromosome in an asexual group of nematodes resulted from a fusion of six ancestral chromosomal domains. Due to the lack of recombination between alleles at most loci, high heterozygosity has evolved, providing one explanation for the unexpected longevity of this asexual lineage.

Original languageEnglish (US)
Pages (from-to)2928-2939.e6
JournalCurrent Biology
Volume27
Issue number19
DOIs
StatePublished - Oct 9 2017

Keywords

  • Diploscapter pachys
  • Protorhabditis group
  • asexual reproduction
  • chromosome fusion
  • evolution
  • genome sequence
  • meiosis
  • nematode
  • parthenogenesis
  • telomere

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Fingerprint Dive into the research topics of 'Genome Architecture and Evolution of a Unichromosomal Asexual Nematode'. Together they form a unique fingerprint.

  • Cite this

    Fradin, H., Kiontke, K., Zegar, C., Gutwein, M., Lucas, J., Kovtun, M., Corcoran, D. L., Baugh, L. R., Fitch, D. H. A., Piano, F., & Gunsalus, K. C. (2017). Genome Architecture and Evolution of a Unichromosomal Asexual Nematode. Current Biology, 27(19), 2928-2939.e6. https://doi.org/10.1016/j.cub.2017.08.038