Sex-dependent and-independent transcriptional changes during haploid phase gametogenesis in the sugar kelp Saccharina latissima
Autor(a) principal: | |
---|---|
Data de Publicação: | 2019 |
Outros Autores: | , , , |
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. |
id |
RCAP_e1da0ba94ca8f09a4bf585a9ff12c112 |
---|---|
oai_identifier_str |
oai:sapientia.ualg.pt:10400.1/14019 |
network_acronym_str |
RCAP |
network_name_str |
Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) |
repository_id_str |
7160 |
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 instacron:RCAAP |
instname_str |
Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação |
instacron_str |
RCAAP |
institution |
RCAAP |
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 |
repository.mail.fl_str_mv |
|
_version_ |
1799133289953361921 |