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Comparative genome analysis of programmed DNA elimination in nematodes

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 somati...

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Autores principales: Wang, Jianbin, Gao, Shenghan, Mostovoy, Yulia, Kang, Yuanyuan, Zagoskin, Maxim, Sun, Yongqiao, Zhang, Bing, White, Laura K., Easton, Alice, Nutman, Thomas B., Kwok, Pui-Yan, Hu, Songnian, Nielsen, Martin K., Davis, Richard E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5741062/
https://www.ncbi.nlm.nih.gov/pubmed/29118011
http://dx.doi.org/10.1101/gr.225730.117
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author Wang, Jianbin
Gao, Shenghan
Mostovoy, Yulia
Kang, Yuanyuan
Zagoskin, Maxim
Sun, Yongqiao
Zhang, Bing
White, Laura K.
Easton, Alice
Nutman, Thomas B.
Kwok, Pui-Yan
Hu, Songnian
Nielsen, Martin K.
Davis, Richard E.
author_facet Wang, Jianbin
Gao, Shenghan
Mostovoy, Yulia
Kang, Yuanyuan
Zagoskin, Maxim
Sun, Yongqiao
Zhang, Bing
White, Laura K.
Easton, Alice
Nutman, Thomas B.
Kwok, Pui-Yan
Hu, Songnian
Nielsen, Martin K.
Davis, Richard E.
author_sort Wang, Jianbin
collection PubMed
description 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.
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spelling pubmed-57410622018-06-01 Comparative genome analysis of programmed DNA elimination in nematodes Wang, Jianbin Gao, Shenghan Mostovoy, Yulia Kang, Yuanyuan Zagoskin, Maxim Sun, Yongqiao Zhang, Bing White, Laura K. Easton, Alice Nutman, Thomas B. Kwok, Pui-Yan Hu, Songnian Nielsen, Martin K. Davis, Richard E. Genome Res Research 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. Cold Spring Harbor Laboratory Press 2017-12 /pmc/articles/PMC5741062/ /pubmed/29118011 http://dx.doi.org/10.1101/gr.225730.117 Text en © 2017 Wang et al.; Published by Cold Spring Harbor Laboratory Press http://creativecommons.org/licenses/by-nc/4.0/ This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genome.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
spellingShingle Research
Wang, Jianbin
Gao, Shenghan
Mostovoy, Yulia
Kang, Yuanyuan
Zagoskin, Maxim
Sun, Yongqiao
Zhang, Bing
White, Laura K.
Easton, Alice
Nutman, Thomas B.
Kwok, Pui-Yan
Hu, Songnian
Nielsen, Martin K.
Davis, Richard E.
Comparative genome analysis of programmed DNA elimination in nematodes
title Comparative genome analysis of programmed DNA elimination in nematodes
title_full Comparative genome analysis of programmed DNA elimination in nematodes
title_fullStr Comparative genome analysis of programmed DNA elimination in nematodes
title_full_unstemmed Comparative genome analysis of programmed DNA elimination in nematodes
title_short Comparative genome analysis of programmed DNA elimination in nematodes
title_sort comparative genome analysis of programmed dna elimination in nematodes
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5741062/
https://www.ncbi.nlm.nih.gov/pubmed/29118011
http://dx.doi.org/10.1101/gr.225730.117
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