Comparative genome analysis of programmed DNA elimination in nematodes

Jianbin Wang, Shenghan Gao, Yulia Mostovoy, Yuanyuan Kang, Maxim Zagoskin, Yongqiao Sun, Bing Zhang, Laura K. White, Alice Easton, Thomas B. Nutman, Pui Yan Kwok, Songnian Hu, Martin K. Nielsen, Richard E. Davis

Research output: Contribution to journalArticlepeer-review

55 Scopus citations

Abstract

Programmed DNA elimination is a developmentally regulated process leading to the reproducible loss of specific genomic sequences. DNA elimination occurs in unicellular ciliates and a variety of metazoans, including invertebrates and vertebrates. In metazoa, DNA elimination typically occurs in somatic cells during early development, leaving the germline genome intact. Reference genomes for metazoa that undergo DNA elimination are not available. Here, we generated germline and somatic reference genome sequences of the DNA eliminating pig parasitic nematode Ascaris suum and the horse parasite Parascaris univalens. In addition, we carried out in-depth analyses of DNA elimination in the parasitic nematode of humans, Ascaris lumbricoides, and the parasitic nematode of dogs, Toxocara canis. Our analysis of nematode DNA elimination reveals that in all species, repetitive sequences (that differ among the genera) and germline-expressed genes (approximately 1000-2000 or 5%-10% of the genes) are eliminated. Thirty-five percent of these eliminated genes are conserved among these nematodes, defining a core set of eliminated genes that are preferentially expressed during spermatogenesis. Our analysis supports the view that DNA elimination in nematodes silences germline-expressed genes. Over half of the chromosome break sites are conserved between Ascaris and Parascaris, whereas only 10% are conserved in the more divergent T. canis. Analysis of the chromosomal breakage regions suggests a sequence-independent mechanism for DNA breakage followed by telomere healing, with the formation of more accessible chromatin in the break regions prior to DNA elimination. Our genome assemblies and annotations also provide comprehensive resources for analysis of DNA elimination, parasitology research, and comparative nematode genome and epigenome studies.

Original languageEnglish
Pages (from-to)2001-2014
Number of pages14
JournalGenome Research
Volume27
Issue number12
DOIs
StatePublished - Dec 2017

Bibliographical note

Funding Information:
We thank Richard Komuniecki, Jeff Myers, and Routh Packing Co. for their support and hospitality in collecting Ascaris material and Mark Johnson and Jay Hesselberth for comments on the manuscript. S.G. was supported in part by the China Scholarship Council (201604910424). This work was supported in part by National Institutes of Health grants to R.E.D. (AI049558 and AI114054) and to J.W. (AI125869).

Publisher Copyright:
© 2017 Wang et al.

ASJC Scopus subject areas

  • Genetics
  • Genetics(clinical)

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