The Molecular Machinery of Gametogenesis in Geodia Demosponges (Porifera): Evolutionary Origins of a Conserved Toolkit across Animals
| Main Authors: | Koutsouveli, Vasiliki, Cárdenas, Paco, Santodomingo, Nadiezhda, Marina, Anabel, Morato, Esperanza, Rapp, Hans Tore, Riesgo, Ana |
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| Format: | Article |
| Terbitan: |
, 2020
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| Subjects: | |
| Online Access: |
https://zenodo.org/record/4057100 |
| ctrlnum |
4057100 |
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| fullrecord |
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<dc schemaLocation="http://www.openarchives.org/OAI/2.0/oai_dc/ http://www.openarchives.org/OAI/2.0/oai_dc.xsd"><creator>Koutsouveli, Vasiliki</creator><creator>Cárdenas, Paco</creator><creator>Santodomingo, Nadiezhda</creator><creator>Marina, Anabel</creator><creator>Morato, Esperanza</creator><creator>Rapp, Hans Tore</creator><creator>Riesgo, Ana</creator><date>2020-07-16</date><description>ABSTRACT
All animals are capable of undergoing gametogenesis. The ability of forming haploid cells from diploid cells through meiosis and recombination appeared early in eukaryotes, whereas further gamete differentiation is mostly a metazoan signature. Morphologically, the gametogenic process presents many similarities across animal taxa, but little is known about its conservation at the molecular level. Porifera are the earliest divergent animals and therefore are an ideal phylum to understand evolution of the gametogenic toolkits. Although sponge gametogenesis is well known at the histological level, the molecular toolkits for gamete production are largely unknown. Our goal was to identify the genes and their expression levels which regulate oogenesis and spermatogenesis in five gonochoristic and oviparous species of the genus Geodia, using both RNAseq and proteomic analyses. In the early stages of both female and male gametogenesis, genes involved in germ cell fate and cell-renewal were upregulated. Then, molecular signals involved in retinoic acid pathway could trigger the meiotic processes. During later stages of oogenesis, female sponges expressed genes involved in cell growth, vitellogenesis, and extracellular matrix reassembly, which are conserved elements of oocyte maturation in Metazoa. Likewise, in spermatogenesis, genes regulating the whole meiotic cycle, chromatin compaction, and flagellum axoneme formation, that are common across Metazoa were overexpressed in the sponges. Finally, molecular signals possibly related to sperm capacitation were identified during late stages of spermatogenesis for the first time in Porifera. In conclusion, the activated molecular toolkit during gametogenesis in sponges was remarkably similar to that deployed during gametogenesis in vertebrates.</description><description>ACKNOWLEDGEMENTS
We would like to thank Dr Nathan Kenny for his useful bioinformatic advice and Dr Cristina Díez-Vives for her useful advice in R. Furthermore, we would like to thank María Conejero for her important help in thin sectioning and Kathrin Busch, Asimenia Gavriilidou, Karin Steffen, Dr Francisca Carvalho, Dr Joana Xavier, and Dr Nathan Kenny for their essential help and support during sample collection. Finally, we would like to thank the reviewers for their thorough work and their contribution to the massive improvement of this manuscript. This work was supported by the H2020 EU Framework Programme for Research and Innovation Project SponGES (Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach toward their preservation and sustainable exploitation) (Grant Agreement No. 679849). This document reflects only the authors' view and the Executive Agency for Small and Medium-sized Enterprises (EASME) is not responsible for any use that may be made of the information it contains. This work is dedicated to our beloved collaborator, coordinator of the SponGES project and coauthor of this manuscript, Hans Tore Rapp, who will always stay in our memories.</description><identifier>https://zenodo.org/record/4057100</identifier><identifier>10.1093/molbev/msaa183</identifier><identifier>oai:zenodo.org:4057100</identifier><relation>info:eu-repo/grantAgreement/EC/H2020/679849/</relation><relation>url:https://academic.oup.com/mbe/advance-article/doi/10.1093/molbev/msaa183/5872533</relation><relation>url:https://oup.silverchair-cdn.com/oup/backfile/Content_public/Journal/mbe/PAP/10.1093_molbev_msaa183/2/msaa183_supplementary_data.zip?Expires=1604298954&Signature=0uB6jpHnFWxFdjnc8Va2KS7bAwX7oXkEN3mS17q4fkKpdyGQQAIFLn06y37MBtRdwz0~mWWU~BDVX1~vVlpMp3H5y2uAY5fjRhNXbJWmEWnAdnep5revbOKnjGVxm8PDNdjY26kt6w2LDNEdMm769~qFHia3o4Hc351Us0gPaQAjZED7MzDLrZolEOh1Vg3OevxVcer-J3SZBxjPCcxgY09jxmYlIPbnf~0GgM~tDmwVi9eWLFdCPedYV19xZlvTk2TtEZsU6MBh8Tzeb7p1L3loFNSzsNGTt3Fh7V12G~KLTwAUg2FDHGiRcQDLw0o1Q4ly1XwdkWQvD19v6O5MTA__&Key-Pair-Id=APKAIE5G5CRDK6RD3PGA</relation><relation>url:https://zenodo.org/communities/sponges</relation><rights>info:eu-repo/semantics/openAccess</rights><rights>https://creativecommons.org/licenses/by/4.0/legalcode</rights><source>Molecular Biology and Evolution</source><subject>oogenesis</subject><subject>spermatogenesis</subject><subject>evolution</subject><subject>Porifera</subject><subject>transcriptomics</subject><subject>proteomics</subject><subject>European Union (EU)</subject><subject>Horizon 2020</subject><subject>Grant Agreement No 679849</subject><subject>Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation</subject><subject>SponGES</subject><title>The Molecular Machinery of Gametogenesis in Geodia Demosponges (Porifera): Evolutionary Origins of a Conserved Toolkit across Animals</title><type>Journal:Article</type><type>Journal:Article</type><recordID>4057100</recordID></dc>
|
| format |
Journal:Article Journal |
| author |
Koutsouveli, Vasiliki Cárdenas, Paco Santodomingo, Nadiezhda Marina, Anabel Morato, Esperanza Rapp, Hans Tore Riesgo, Ana |
| title |
The Molecular Machinery of Gametogenesis in Geodia Demosponges (Porifera): Evolutionary Origins of a Conserved Toolkit across Animals |
| publishDate |
2020 |
| topic |
oogenesis spermatogenesis evolution Porifera transcriptomics proteomics European Union (EU) Horizon 2020 Grant Agreement No 679849 Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach towards their preservation and sustainable exploitation SponGES |
| url |
https://zenodo.org/record/4057100 |
| contents |
ABSTRACT
All animals are capable of undergoing gametogenesis. The ability of forming haploid cells from diploid cells through meiosis and recombination appeared early in eukaryotes, whereas further gamete differentiation is mostly a metazoan signature. Morphologically, the gametogenic process presents many similarities across animal taxa, but little is known about its conservation at the molecular level. Porifera are the earliest divergent animals and therefore are an ideal phylum to understand evolution of the gametogenic toolkits. Although sponge gametogenesis is well known at the histological level, the molecular toolkits for gamete production are largely unknown. Our goal was to identify the genes and their expression levels which regulate oogenesis and spermatogenesis in five gonochoristic and oviparous species of the genus Geodia, using both RNAseq and proteomic analyses. In the early stages of both female and male gametogenesis, genes involved in germ cell fate and cell-renewal were upregulated. Then, molecular signals involved in retinoic acid pathway could trigger the meiotic processes. During later stages of oogenesis, female sponges expressed genes involved in cell growth, vitellogenesis, and extracellular matrix reassembly, which are conserved elements of oocyte maturation in Metazoa. Likewise, in spermatogenesis, genes regulating the whole meiotic cycle, chromatin compaction, and flagellum axoneme formation, that are common across Metazoa were overexpressed in the sponges. Finally, molecular signals possibly related to sperm capacitation were identified during late stages of spermatogenesis for the first time in Porifera. In conclusion, the activated molecular toolkit during gametogenesis in sponges was remarkably similar to that deployed during gametogenesis in vertebrates. ACKNOWLEDGEMENTS We would like to thank Dr Nathan Kenny for his useful bioinformatic advice and Dr Cristina Díez-Vives for her useful advice in R. Furthermore, we would like to thank María Conejero for her important help in thin sectioning and Kathrin Busch, Asimenia Gavriilidou, Karin Steffen, Dr Francisca Carvalho, Dr Joana Xavier, and Dr Nathan Kenny for their essential help and support during sample collection. Finally, we would like to thank the reviewers for their thorough work and their contribution to the massive improvement of this manuscript. This work was supported by the H2020 EU Framework Programme for Research and Innovation Project SponGES (Deep-sea Sponge Grounds Ecosystems of the North Atlantic: an integrated approach toward their preservation and sustainable exploitation) (Grant Agreement No. 679849). This document reflects only the authors' view and the Executive Agency for Small and Medium-sized Enterprises (EASME) is not responsible for any use that may be made of the information it contains. This work is dedicated to our beloved collaborator, coordinator of the SponGES project and coauthor of this manuscript, Hans Tore Rapp, who will always stay in our memories. |
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