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

Abstract 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 p...

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Main Authors: Christopher Kraus, Philipp H. Schiffer, Hiroshi Kagoshima, Hideaki Hiraki, Theresa Vogt, Michael Kroiher, Yuji Kohara, Einhard Schierenberg
Format: Article
Language:English
Published: BMC 2017-10-01
Series:EvoDevo
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13227-017-0081-y
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spelling doaj-ab25f77e55fa439e9631fc3844c9e3502020-11-25T00:49:44ZengBMCEvoDevo2041-91392017-10-018111710.1186/s13227-017-0081-yDifferences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatusChristopher Kraus0Philipp H. Schiffer1Hiroshi Kagoshima2Hideaki Hiraki3Theresa Vogt4Michael Kroiher5Yuji Kohara6Einhard Schierenberg7Zoologisches Institut, Universität zu KölnZoologisches Institut, Universität zu KölnNational Institute of GeneticsNational Institute of GeneticsZoologisches Institut, Universität zu KölnZoologisches Institut, Universität zu KölnNational Institute of GeneticsZoologisches Institut, Universität zu KölnAbstract 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.http://link.springer.com/article/10.1186/s13227-017-0081-yNematodeCaenorhabditisParthenogenesisEmbryogenesisPolarityChromosome
collection DOAJ
language English
format Article
sources DOAJ
author Christopher Kraus
Philipp H. Schiffer
Hiroshi Kagoshima
Hideaki Hiraki
Theresa Vogt
Michael Kroiher
Yuji Kohara
Einhard Schierenberg
spellingShingle Christopher Kraus
Philipp H. Schiffer
Hiroshi Kagoshima
Hideaki Hiraki
Theresa Vogt
Michael Kroiher
Yuji Kohara
Einhard Schierenberg
Differences in the genetic control of early egg development and reproduction between C. elegans and its parthenogenetic relative D. coronatus
EvoDevo
Nematode
Caenorhabditis
Parthenogenesis
Embryogenesis
Polarity
Chromosome
author_facet Christopher Kraus
Philipp H. Schiffer
Hiroshi Kagoshima
Hideaki Hiraki
Theresa Vogt
Michael Kroiher
Yuji Kohara
Einhard Schierenberg
author_sort Christopher Kraus
title 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_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_sort differences in the genetic control of early egg development and reproduction between c. elegans and its parthenogenetic relative d. coronatus
publisher BMC
series EvoDevo
issn 2041-9139
publishDate 2017-10-01
description Abstract 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.
topic Nematode
Caenorhabditis
Parthenogenesis
Embryogenesis
Polarity
Chromosome
url http://link.springer.com/article/10.1186/s13227-017-0081-y
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