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Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus

BACKGROUND: The free-living nematode Diploscapter coronatus is the closest known relative of Caenorhabditis elegans with parthenogenetic reproduction. It shows several developmental idiosyncracies, for example concerning the mode of reproduction, embryonic axis formation and early cleavage pattern (...

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Autores principales: Kraus, Christopher, Schiffer, Philipp H., Kagoshima, Hiroshi, Hiraki, Hideaki, Vogt, Theresa, Kroiher, Michael, Kohara, Yuji, Schierenberg, Einhard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5648466/
https://www.ncbi.nlm.nih.gov/pubmed/29075433
http://dx.doi.org/10.1186/s13227-017-0081-y
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author Kraus, Christopher
Schiffer, Philipp H.
Kagoshima, Hiroshi
Hiraki, Hideaki
Vogt, Theresa
Kroiher, Michael
Kohara, Yuji
Schierenberg, Einhard
author_facet Kraus, Christopher
Schiffer, Philipp H.
Kagoshima, Hiroshi
Hiraki, Hideaki
Vogt, Theresa
Kroiher, Michael
Kohara, Yuji
Schierenberg, Einhard
author_sort Kraus, Christopher
collection PubMed
description BACKGROUND: The free-living nematode Diploscapter coronatus is the closest known relative of Caenorhabditis elegans with parthenogenetic reproduction. It shows several developmental idiosyncracies, for example concerning the mode of reproduction, embryonic axis formation and early cleavage pattern (Lahl et al. in Int J Dev Biol 50:393–397, 2006). Our recent genome analysis (Hiraki et al. in BMC Genomics 18:478, 2017) provides a solid foundation to better understand the molecular basis of developmental idiosyncrasies in this species in an evolutionary context by comparison with selected other nematodes. Our genomic data also yielded indications for the view that D. coronatus is a product of interspecies hybridization. RESULTS: In a genomic comparison between D. coronatus, C. elegans, other representatives of the genus Caenorhabditis and the more distantly related Pristionchus pacificus and Panagrellus redivivus, certain genes required for central developmental processes in C. elegans like control of meiosis and establishment of embryonic polarity were found to be restricted to the genus Caenorhabditis. The mRNA content of early D. coronatus embryos was sequenced and compared with similar stages in C. elegans and Ascaris suum. We identified 350 gene families transcribed in the early embryo of D. coronatus but not in the other two nematodes. Looking at individual genes transcribed early in D. coronatus but not in C. elegans and A. suum, we found that orthologs of most of these are present in the genomes of the latter species as well, suggesting heterochronic shifts with respect to expression behavior. Considerable genomic heterozygosity and allelic divergence lend further support to the view that D. coronatus may be the result of an interspecies hybridization. Expression analysis of early acting single-copy genes yields no indication for silencing of one parental genome. CONCLUSIONS: Our comparative cellular and molecular studies support the view that the genus Caenorhabditis differs considerably from the other studied nematodes in its control of development and reproduction. The easy-to-culture parthenogenetic D. coronatus, with its high-quality draft genome and only a single chromosome when haploid, offers many new starting points on the cellular, molecular and genomic level to explore alternative routes of nematode development and reproduction. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13227-017-0081-y) contains supplementary material, which is available to authorized users.
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spelling pubmed-56484662017-10-26 Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus Kraus, Christopher Schiffer, Philipp H. Kagoshima, Hiroshi Hiraki, Hideaki Vogt, Theresa Kroiher, Michael Kohara, Yuji Schierenberg, Einhard EvoDevo Research BACKGROUND: The free-living nematode Diploscapter coronatus is the closest known relative of Caenorhabditis elegans with parthenogenetic reproduction. It shows several developmental idiosyncracies, for example concerning the mode of reproduction, embryonic axis formation and early cleavage pattern (Lahl et al. in Int J Dev Biol 50:393–397, 2006). Our recent genome analysis (Hiraki et al. in BMC Genomics 18:478, 2017) provides a solid foundation to better understand the molecular basis of developmental idiosyncrasies in this species in an evolutionary context by comparison with selected other nematodes. Our genomic data also yielded indications for the view that D. coronatus is a product of interspecies hybridization. RESULTS: In a genomic comparison between D. coronatus, C. elegans, other representatives of the genus Caenorhabditis and the more distantly related Pristionchus pacificus and Panagrellus redivivus, certain genes required for central developmental processes in C. elegans like control of meiosis and establishment of embryonic polarity were found to be restricted to the genus Caenorhabditis. The mRNA content of early D. coronatus embryos was sequenced and compared with similar stages in C. elegans and Ascaris suum. We identified 350 gene families transcribed in the early embryo of D. coronatus but not in the other two nematodes. Looking at individual genes transcribed early in D. coronatus but not in C. elegans and A. suum, we found that orthologs of most of these are present in the genomes of the latter species as well, suggesting heterochronic shifts with respect to expression behavior. Considerable genomic heterozygosity and allelic divergence lend further support to the view that D. coronatus may be the result of an interspecies hybridization. Expression analysis of early acting single-copy genes yields no indication for silencing of one parental genome. CONCLUSIONS: Our comparative cellular and molecular studies support the view that the genus Caenorhabditis differs considerably from the other studied nematodes in its control of development and reproduction. The easy-to-culture parthenogenetic D. coronatus, with its high-quality draft genome and only a single chromosome when haploid, offers many new starting points on the cellular, molecular and genomic level to explore alternative routes of nematode development and reproduction. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13227-017-0081-y) contains supplementary material, which is available to authorized users. BioMed Central 2017-10-18 /pmc/articles/PMC5648466/ /pubmed/29075433 http://dx.doi.org/10.1186/s13227-017-0081-y Text en © The Author(s) 2017 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Kraus, Christopher
Schiffer, Philipp H.
Kagoshima, Hiroshi
Hiraki, Hideaki
Vogt, Theresa
Kroiher, Michael
Kohara, Yuji
Schierenberg, Einhard
Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus
title Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus
title_full Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus
title_fullStr Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus
title_full_unstemmed Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus
title_short Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus
title_sort differences in the genetic control of early egg development and reproduction between c. elegans and its parthenogenetic relative d. coronatus
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5648466/
https://www.ncbi.nlm.nih.gov/pubmed/29075433
http://dx.doi.org/10.1186/s13227-017-0081-y
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