RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes.


Journal

BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258

Informations de publication

Date de publication:
06 Jul 2020
Historique:
received: 23 12 2019
accepted: 22 06 2020
entrez: 8 7 2020
pubmed: 8 7 2020
medline: 20 3 2021
Statut: epublish

Résumé

The genus Macrostomum consists of small free-living flatworms and contains Macrostomum lignano, which has been used in investigations of ageing, stem cell biology, bioadhesion, karyology, and sexual selection in hermaphrodites. Two types of mating behaviour occur within this genus. Some species, including M. lignano, mate via reciprocal copulation, where, in a single mating, both partners insert their male copulatory organ into the female storage organ and simultaneously donate and receive sperm. Other species mate via hypodermic insemination, where worms use a needle-like copulatory organ to inject sperm into the tissue of the partner. These contrasting mating behaviours are associated with striking differences in sperm and copulatory organ morphology. Here we expand the genomic resources within the genus to representatives of both behaviour types and investigate whether genes vary in their rate of evolution depending on their putative function. We present de novo assembled transcriptomes of three Macrostomum species, namely M. hystrix, a close relative of M. lignano that mates via hypodermic insemination, M. spirale, a more distantly related species that mates via reciprocal copulation, and finally M. pusillum, which represents a clade that is only distantly related to the other three species and also mates via hypodermic insemination. We infer 23,764 sets of homologous genes and annotate them using experimental evidence from M. lignano. Across the genus, we identify 521 gene families with conserved patterns of differential expression between juvenile vs. adult worms and 185 gene families with a putative expression in the testes that are restricted to the two reciprocally mating species. Further, we show that homologs of putative reproduction-related genes have a higher protein divergence across the four species than genes lacking such annotations and that they are more difficult to identify across the four species, indicating that these genes evolve more rapidly, while genes involved in neoblast function are more conserved. This study improves the genus Macrostomum as a model system, by providing resources for the targeted investigation of gene function in a broad range of species. And we, for the first time, show that reproduction-related genes evolve at an accelerated rate in flatworms.

Sections du résumé

BACKGROUND BACKGROUND
The genus Macrostomum consists of small free-living flatworms and contains Macrostomum lignano, which has been used in investigations of ageing, stem cell biology, bioadhesion, karyology, and sexual selection in hermaphrodites. Two types of mating behaviour occur within this genus. Some species, including M. lignano, mate via reciprocal copulation, where, in a single mating, both partners insert their male copulatory organ into the female storage organ and simultaneously donate and receive sperm. Other species mate via hypodermic insemination, where worms use a needle-like copulatory organ to inject sperm into the tissue of the partner. These contrasting mating behaviours are associated with striking differences in sperm and copulatory organ morphology. Here we expand the genomic resources within the genus to representatives of both behaviour types and investigate whether genes vary in their rate of evolution depending on their putative function.
RESULTS RESULTS
We present de novo assembled transcriptomes of three Macrostomum species, namely M. hystrix, a close relative of M. lignano that mates via hypodermic insemination, M. spirale, a more distantly related species that mates via reciprocal copulation, and finally M. pusillum, which represents a clade that is only distantly related to the other three species and also mates via hypodermic insemination. We infer 23,764 sets of homologous genes and annotate them using experimental evidence from M. lignano. Across the genus, we identify 521 gene families with conserved patterns of differential expression between juvenile vs. adult worms and 185 gene families with a putative expression in the testes that are restricted to the two reciprocally mating species. Further, we show that homologs of putative reproduction-related genes have a higher protein divergence across the four species than genes lacking such annotations and that they are more difficult to identify across the four species, indicating that these genes evolve more rapidly, while genes involved in neoblast function are more conserved.
CONCLUSIONS CONCLUSIONS
This study improves the genus Macrostomum as a model system, by providing resources for the targeted investigation of gene function in a broad range of species. And we, for the first time, show that reproduction-related genes evolve at an accelerated rate in flatworms.

Identifiants

pubmed: 32631219
doi: 10.1186/s12864-020-06862-x
pii: 10.1186/s12864-020-06862-x
pmc: PMC7336406
doi:

Substances chimiques

Helminth Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

462

Subventions

Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : 31003A_162543
Organisme : Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
ID : 310030_184916
Organisme : Austrian Science Fund
ID : P30347
Organisme : Fonds National de la Recherche Luxembourg
ID : 13569708

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Auteurs

Jeremias N Brand (JN)

Department of Environmental Sciences, Zoological Institute, University of Basel, Vesalgasse 1, 4051, Basel, Switzerland. jeremias.brand@unibas.ch.

R Axel W Wiberg (RAW)

Department of Environmental Sciences, Zoological Institute, University of Basel, Vesalgasse 1, 4051, Basel, Switzerland.

Robert Pjeta (R)

Institute of Zoology and Center of Molecular Biosciences Innsbruck, University of Innsbruck, Innsbruck, Austria.

Philip Bertemes (P)

Institute of Zoology and Center of Molecular Biosciences Innsbruck, University of Innsbruck, Innsbruck, Austria.

Christian Beisel (C)

Department of Biosystems Science and Engineering, ETH Zürich, Basel, Switzerland.

Peter Ladurner (P)

Institute of Zoology and Center of Molecular Biosciences Innsbruck, University of Innsbruck, Innsbruck, Austria.

Lukas Schärer (L)

Department of Environmental Sciences, Zoological Institute, University of Basel, Vesalgasse 1, 4051, Basel, Switzerland.

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