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...
| Authors: | ; ; ; ; ; ; |
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| Format: | Article |
| Status: | Published version |
| Publication date: | 2019 |
| Country: | España |
| Institution: | Universitat Pompeu Fabra |
| Repository: | Repositorio Digital de la UPF |
| OAI Identifier: | oai:repositori.upf.edu:10230/44053 |
| Online Access: | http://hdl.handle.net/10230/44053 http://dx.doi.org/10.1093/gbe/evy265 |
| Access Level: | Open access |
| Keyword: | Transcriptomics Stolonizing syllids Reproduction Hormonal control |
| _version_ | 1878738415107702784 |
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| author | Álvarez Campos, Patricia |
| author2 | Kenny, Nathan J. Verdes, Aida Fernández, Rosa Novo, Marta Giribet, Gonzalo Riesgo, Ana |
| author2_role | author author author author author author |
| author_browse | Fernández, Rosa Giribet, Gonzalo Kenny, Nathan J. Novo, Marta Riesgo, Ana Verdes, Aida Álvarez Campos, Patricia |
| author_facet | Álvarez Campos, Patricia Kenny, Nathan J. Verdes, Aida Fernández, Rosa Novo, Marta Giribet, Gonzalo Riesgo, Ana |
| author_role | author |
| collection | Repositorio Digital de la UPF |
| 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. |
| eu_rights_str_mv | openAccess |
| format | article |
| id | ES_aea2b47e0711edf3bd2c8d4e180f9adc |
| institution | Universitat Pompeu Fabra |
| instname_str | Universitat Pompeu Fabra |
| network_acronym_str | ES |
| network_name_str | España |
| oai_identifier_str | oai:repositori.upf.edu:10230/44053 |
| publishDate | 2019 |
| publishDateSort | 2019 |
| publisher | Oxford University Press |
| publisherStr | Oxford University Press |
| reponame_str | Repositorio Digital de la UPF |
| spelling | Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction Álvarez Campos, Patricia Kenny, Nathan J. Verdes, Aida Fernández, Rosa Novo, Marta Giribet, Gonzalo Riesgo, Ana Transcriptomics Stolonizing syllids Reproduction Hormonal control 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. 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 Press http://hdl.handle.net/10230/44053 http://dx.doi.org/10.1093/gbe/evy265 |
| spellingShingle | Delegating sex: differential gene expression in stolonizing syllids uncovers the hormonal control of reproduction Álvarez Campos, Patricia Transcriptomics Stolonizing syllids Reproduction Hormonal control |
| status_str | publishedVersion |
| title | 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_short | 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 |
| topic | Transcriptomics Stolonizing syllids Reproduction Hormonal control |
| topic_facet | Transcriptomics Stolonizing syllids Reproduction Hormonal control |
| url | http://hdl.handle.net/10230/44053 http://dx.doi.org/10.1093/gbe/evy265 |