Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction

Stolonization in syllid annelids is a unique mode of reproduction among animals. During the breeding season, a structure resembling the adult but containing only gametes, called stolon, is formed generally at the posterior end of the animal. When stolons mature, they detach from the adult and gamete...

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Autores: Álvarez Campos, Patricia, Kenny, Nathan J., Verdes, Aida, Fernández, Rosa, Novo, Marta, Giribet, Gonzalo, Riesgo, Ana
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2019
País:España
Institución:Universitat Pompeu Fabra
Repositorio:Repositorio Digital de la UPF
OAI Identifier:oai:repositori.upf.edu:10230/44053
Acceso en línea:http://hdl.handle.net/10230/44053
http://dx.doi.org/10.1093/gbe/evy265
Access Level:acceso abierto
Palabra clave:Transcriptomics
Stolonizing syllids
Reproduction
Hormonal control
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spelling Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproductionÁlvarez Campos, PatriciaKenny, Nathan J.Verdes, AidaFernández, RosaNovo, MartaGiribet, GonzaloRiesgo, AnaTranscriptomicsStolonizing syllidsReproductionHormonal controlStolonization in syllid annelids is a unique mode of reproduction among animals. During the breeding season, a structure resembling the adult but containing only gametes, called stolon, is formed generally at the posterior end of the animal. When stolons mature, they detach from the adult and gametes are released into the water column. The process is synchronized within each species, and it has been reported to be under environmental and endogenous control, probably via endocrine regulation. To further understand reproduction in syllids and to elucidate the molecular toolkit underlying stolonization, we generated Illumina RNA-seq data from different tissues of reproductive and nonreproductive individuals of Syllis magdalena and characterized gene expression during the stolonization process. Several genes involved in gametogenesis (ovochymase, vitellogenin, testis-specific serine/threonine-kinase), immune response (complement receptor 2), neuronal development (tyrosine-protein kinase Src42A), cell proliferation (alpha-1D adrenergic receptor), and steroid metabolism (hydroxysteroid dehydrogenase 2) were found differentially expressed in the different tissues and conditions analyzed. In addition, our findings suggest that several neurohormones, such as methyl farnesoate, dopamine, and serotonin, might trigger stolon formation, the correct maturation of gametes and the detachment of stolons when gametogenesis ends. The process seems to be under circadian control, as indicated by the expression patterns of r-opsins. Overall, our results shed light into the genes that orchestrate the onset of gamete formation and improve our understanding of how some hormones, previously reported to be involved in reproduction and metamorphosis processes in other invertebrates, seem to also regulate reproduction via stolonization.This research received funding from the European Union’s (European Atomic Energy Community’s) Seventh Framework Program (FP7/2007–2013; FP7/2007–2011) under grant agreement 227799 to P.A.-C. Sequencing and analyses were conducted with internal MCZ funds to G.G. and with the support of the Center for Systems Biology and the Research Computing group, both from the Faculty of Arts and Sciences (Harvard University), and with internal funds from the Department of Life Sciences (Natural History Museum of London) to AR. One anonymous reviewer and Associate Editor Mandë Holford provided constructive criticism which helped to improve this study.Oxford University Press202020202019info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfapplication/pdfhttp://hdl.handle.net/10230/44053http://dx.doi.org/10.1093/gbe/evy265reponame:Repositorio Digital de la UPFinstname:Universitat Pompeu FabraInglésGenome Biol Evol. 2019; 11(1):295-318info:eu-repo/grantAgreement/EC/FP7/227799© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.http://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:repositori.upf.edu:10230/440532026-06-12T07:21:37Z
dc.title.none.fl_str_mv Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
title Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
spellingShingle Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
Álvarez Campos, Patricia
Transcriptomics
Stolonizing syllids
Reproduction
Hormonal control
title_short Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
title_full Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
title_fullStr Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
title_full_unstemmed Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
title_sort Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction
dc.creator.none.fl_str_mv Álvarez Campos, Patricia
Kenny, Nathan J.
Verdes, Aida
Fernández, Rosa
Novo, Marta
Giribet, Gonzalo
Riesgo, Ana
author Álvarez Campos, Patricia
author_facet Álvarez Campos, Patricia
Kenny, Nathan J.
Verdes, Aida
Fernández, Rosa
Novo, Marta
Giribet, Gonzalo
Riesgo, Ana
author_role author
author2 Kenny, Nathan J.
Verdes, Aida
Fernández, Rosa
Novo, Marta
Giribet, Gonzalo
Riesgo, Ana
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv Transcriptomics
Stolonizing syllids
Reproduction
Hormonal control
topic Transcriptomics
Stolonizing syllids
Reproduction
Hormonal control
description Stolonization in syllid annelids is a unique mode of reproduction among animals. During the breeding season, a structure resembling the adult but containing only gametes, called stolon, is formed generally at the posterior end of the animal. When stolons mature, they detach from the adult and gametes are released into the water column. The process is synchronized within each species, and it has been reported to be under environmental and endogenous control, probably via endocrine regulation. To further understand reproduction in syllids and to elucidate the molecular toolkit underlying stolonization, we generated Illumina RNA-seq data from different tissues of reproductive and nonreproductive individuals of Syllis magdalena and characterized gene expression during the stolonization process. Several genes involved in gametogenesis (ovochymase, vitellogenin, testis-specific serine/threonine-kinase), immune response (complement receptor 2), neuronal development (tyrosine-protein kinase Src42A), cell proliferation (alpha-1D adrenergic receptor), and steroid metabolism (hydroxysteroid dehydrogenase 2) were found differentially expressed in the different tissues and conditions analyzed. In addition, our findings suggest that several neurohormones, such as methyl farnesoate, dopamine, and serotonin, might trigger stolon formation, the correct maturation of gametes and the detachment of stolons when gametogenesis ends. The process seems to be under circadian control, as indicated by the expression patterns of r-opsins. Overall, our results shed light into the genes that orchestrate the onset of gamete formation and improve our understanding of how some hormones, previously reported to be involved in reproduction and metamorphosis processes in other invertebrates, seem to also regulate reproduction via stolonization.
publishDate 2019
dc.date.none.fl_str_mv 2019
2020
2020
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10230/44053
http://dx.doi.org/10.1093/gbe/evy265
url http://hdl.handle.net/10230/44053
http://dx.doi.org/10.1093/gbe/evy265
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv Genome Biol Evol. 2019; 11(1):295-318
info:eu-repo/grantAgreement/EC/FP7/227799
dc.rights.none.fl_str_mv http://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Oxford University Press
publisher.none.fl_str_mv Oxford University Press
dc.source.none.fl_str_mv reponame:Repositorio Digital de la UPF
instname:Universitat Pompeu Fabra
instname_str Universitat Pompeu Fabra
reponame_str Repositorio Digital de la UPF
collection Repositorio Digital de la UPF
repository.name.fl_str_mv
repository.mail.fl_str_mv
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