Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima

Detalhes bibliográficos
Autor(a) principal: Pearson, Gareth
Data de Publicação: 2019
Outros Autores: Martins, Neusa, Madeira, Pedro M., Serrao, Ester, Bartsch, Inka
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.1/14019
Resumo: In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.
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spelling Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissimaComputational biologyGametogenesisHigh-throughput nucleotide sequencingMolecular sequence annotationPhaeophytaSugarsGene expression profilingHaploidyTranscriptomeIn haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.FCTprograms UID/Multi/04326/2019, GENEKELP-PTDC/MAR-EST/6053/2014,MARFOR-Biodiversa/0004/2015, FRH/BPD/122567/2016. Swedish Research Council Formas, Naturvardsverket French National Research Agency (ANR) Spanish Government, FRCT, German Research Foundation (DFG), Pew Marine Fellowship, STSM Grant from the COST Action "Phycomorph" FA1406Public Library of ScienceSapientiaPearson, GarethMartins, NeusaMadeira, Pedro M.Serrao, EsterBartsch, Inka2020-06-16T13:20:48Z20192019-01-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.1/14019eng1932-620310.1371/journal.pone.0219723info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-07-24T10:26:14Zoai:sapientia.ualg.pt:10400.1/14019Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T20:05:05.700496Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
title Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
spellingShingle Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
Pearson, Gareth
Computational biology
Gametogenesis
High-throughput nucleotide sequencing
Molecular sequence annotation
Phaeophyta
Sugars
Gene expression profiling
Haploidy
Transcriptome
title_short Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
title_full Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
title_fullStr Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
title_full_unstemmed Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
title_sort Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
author Pearson, Gareth
author_facet Pearson, Gareth
Martins, Neusa
Madeira, Pedro M.
Serrao, Ester
Bartsch, Inka
author_role author
author2 Martins, Neusa
Madeira, Pedro M.
Serrao, Ester
Bartsch, Inka
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Sapientia
dc.contributor.author.fl_str_mv Pearson, Gareth
Martins, Neusa
Madeira, Pedro M.
Serrao, Ester
Bartsch, Inka
dc.subject.por.fl_str_mv Computational biology
Gametogenesis
High-throughput nucleotide sequencing
Molecular sequence annotation
Phaeophyta
Sugars
Gene expression profiling
Haploidy
Transcriptome
topic Computational biology
Gametogenesis
High-throughput nucleotide sequencing
Molecular sequence annotation
Phaeophyta
Sugars
Gene expression profiling
Haploidy
Transcriptome
description In haplodiplontic lineages, sexual reproduction occurs in haploid parents without meiosis. Although widespread in multicellular lineages such as brown algae (Phaeophyceae), haplodiplontic gametogenesis has been little studied at the molecular level. We addressed this by generating an annotated reference transcriptome for the gametophytic phase of the sugar kelp, Saccharina latissima. Transcriptional profiles of microscopic male and female gametophytes were analysed at four time points during the transition from vegetative growth to gametogenesis. Gametogenic signals resulting from a switch in culture irradiance from red to white light activated a core set of genes in a sex-independent manner, involving rapid activation of ribosome biogenesis, transcription and translation related pathways, with several acting at the post-transcriptional or post-translational level. Additional genes regulating nutrient acquisition and key carbohydrate-energy pathways were also identified. Candidate sex-biased genes under gametogenic conditions had potentially key roles in controlling female- and male-specific gametogenesis. Among these were several sex-biased or -specific E3 ubiquitin-protein ligases that may have important regulatory roles. Females specifically expressed several genes that coordinate gene expression and/or protein degradation, and the synthesis of inositol-containing compounds. Other female-biased genes supported parallels with oogenesis in divergent multicellular lineages, in particular reactive oxygen signalling via an NADPH-oxidase. Males specifically expressed the hypothesised brown algal sex-determining factor. Male-biased expression mainly involved upregulation of genes that control mitotic cell proliferation and spermatogenesis in other systems, as well as multiple flagella-related genes. Our data and results enhance genome-level understanding of gametogenesis in this ecologically and economically important multicellular lineage.
publishDate 2019
dc.date.none.fl_str_mv 2019
2019-01-01T00:00:00Z
2020-06-16T13:20:48Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.1/14019
url http://hdl.handle.net/10400.1/14019
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 1932-6203
10.1371/journal.pone.0219723
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
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