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

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...

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Autores principales: Brand, Jeremias N., Wiberg, R. Axel W., Pjeta, Robert, Bertemes, Philip, Beisel, Christian, Ladurner, Peter, Schärer, Lukas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7336406/
https://www.ncbi.nlm.nih.gov/pubmed/32631219
http://dx.doi.org/10.1186/s12864-020-06862-x
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author Brand, Jeremias N.
Wiberg, R. Axel W.
Pjeta, Robert
Bertemes, Philip
Beisel, Christian
Ladurner, Peter
Schärer, Lukas
author_facet Brand, Jeremias N.
Wiberg, R. Axel W.
Pjeta, Robert
Bertemes, Philip
Beisel, Christian
Ladurner, Peter
Schärer, Lukas
author_sort Brand, Jeremias N.
collection PubMed
description 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: 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: 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.
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spelling pubmed-73364062020-07-07 RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes Brand, Jeremias N. Wiberg, R. Axel W. Pjeta, Robert Bertemes, Philip Beisel, Christian Ladurner, Peter Schärer, Lukas BMC Genomics Research Article 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: 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: 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. BioMed Central 2020-07-06 /pmc/articles/PMC7336406/ /pubmed/32631219 http://dx.doi.org/10.1186/s12864-020-06862-x Text en © The Author(s) 2020 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
spellingShingle Research Article
Brand, Jeremias N.
Wiberg, R. Axel W.
Pjeta, Robert
Bertemes, Philip
Beisel, Christian
Ladurner, Peter
Schärer, Lukas
RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes
title RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes
title_full RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes
title_fullStr RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes
title_full_unstemmed RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes
title_short RNA-Seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes
title_sort rna-seq of three free-living flatworm species suggests rapid evolution of reproduction-related genes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7336406/
https://www.ncbi.nlm.nih.gov/pubmed/32631219
http://dx.doi.org/10.1186/s12864-020-06862-x
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