Gametogenesis in the Pacific Oyster Crassostrea gigas: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes
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{"title"=>"Gametogenesis in the Pacific oyster Crassostrea gigas: A microarrays-based analysis identifies sex and stage specific genes", "type"=>"journal", "authors"=>[{"first_name"=>"Nolwenn M.", "last_name"=>"Dheilly", "scopus_author_id"=>"26040598500"}, {"first_name"=>"Christophe", "last_name"=>"Lelong", "scopus_author_id"=>"6603928639"}, {"first_name"=>"Arnaud", "last_name"=>"Huvet", "scopus_author_id"=>"6602946281"}, {"first_name"=>"Kristell", "last_name"=>"Kellner", "scopus_author_id"=>"7004773144"}, {"first_name"=>"Marie Pierre", "last_name"=>"Dubos", "scopus_author_id"=>"6603413284"}, {"first_name"=>"Guillaume", "last_name"=>"Riviere", "scopus_author_id"=>"8868170600"}, {"first_name"=>"Pierre", "last_name"=>"Boudry", "scopus_author_id"=>"7003723972"}, {"first_name"=>"Pascal", "last_name"=>"Favrel", "scopus_author_id"=>"6603014881"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84860759773", "pmid"=>"22590533", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pui"=>"364774436", "issn"=>"19326203", "scopus"=>"2-s2.0-84860759773", "doi"=>"10.1371/journal.pone.0036353"}, "id"=>"73717874-c271-36d4-a5a1-ec85856b4b00", "abstract"=>"BACKGROUND: The Pacific oyster Crassostrea gigas (Mollusca, Lophotrochozoa) is an alternative and irregular protandrous hermaphrodite: most individuals mature first as males and then change sex several times. Little is known about genetic and phenotypic basis of sex differentiation in oysters, and little more about the molecular pathways regulating reproduction. We have recently developed and validated a microarray containing 31,918 oligomers (Dheilly et al., 2011) representing the oyster transcriptome. The application of this microarray to the study of mollusk gametogenesis should provide a better understanding of the key factors involved in sex differentiation and the regulation of oyster reproduction.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Gene expression was studied in gonads of oysters cultured over a yearly reproductive cycle. Principal component analysis and hierarchical clustering showed a significant divergence in gene expression patterns of males and females coinciding with the start of gonial mitosis. ANOVA analysis of the data revealed 2,482 genes differentially expressed during the course of males and/or females gametogenesis. The expression of 434 genes could be localized in either germ cells or somatic cells of the gonad by comparing the transcriptome of female gonads to the transcriptome of stripped oocytes and somatic tissues. Analysis of the annotated genes revealed conserved molecular mechanisms between mollusks and mammals: genes involved in chromatin condensation, DNA replication and repair, mitosis and meiosis regulation, transcription, translation and apoptosis were expressed in both male and female gonads. Most interestingly, early expressed male-specific genes included bindin and a dpy-30 homolog and female-specific genes included foxL2, nanos homolog 3, a pancreatic lipase related protein, cd63 and vitellogenin. Further functional analyses are now required in order to investigate their role in sex differentiation in oysters.\\n\\nCONCLUSIONS/SIGNIFICANCE: This study allowed us to identify potential markers of early sex differentiation in the oyster C. gigas, an alternative hermaphrodite mollusk. We also provided new highly valuable information on genes specifically expressed by mature spermatozoids and mature oocytes.", "link"=>"http://www.mendeley.com/research/gametogenesis-pacific-oyster-crassostrea-gigas-microarraysbased-analysis-identifies-sex-stage-specif-2", "reader_count"=>39, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>4, "Researcher"=>6, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>12, "Other"=>2, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>4, "Researcher"=>6, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>12, "Other"=>2, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Environmental Science"=>3, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>31, "Chemistry"=>1}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>31}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>3}}, "reader_count_by_country"=>{"Brazil"=>2, "Mexico"=>4, "South Africa"=>1, "France"=>1, "New Caledonia"=>1, "Croatia"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/641552"], "description"=>"<p>Expression of 14 genes was measured in individual gonad samples from Site 1 (Locmariaquer, Brittany, France) and Site 2 (Baie des Veys, Normandy, France). Are displayed, expression profiles obtained by real time qPCR (histograms, left axe) and microarray (crosses, right axe). Vertical bars represent standard deviation for microarray data (doted line) and real time qPCR (plain line). mRNA expression levels of the 14 genes estimated by real-time qPCR are relative to <i>gapdh</i> (expressed in AU). Microarray data are expressed in log center reduced normalized values. Are displayed, expression profiles obtained for a gene more expressed in stage 0 and stage 1 : <i>unc-93 like protein</i> [Genbank 686276], three genes that increase in expression over the course of both male and female gametogenesis: <i>protein regulator of cytokinesis 1</i> (<i>prc1</i>) [Genbank AM861527], <i>bloom syndrome protein homolog</i> (<i>mus309</i>) [Genbank AM859057], <i>G2/Mitotic-specific cyclin-B</i> (<i>cyclin B</i>) [Genbank CU683817], <i>centromere protein F</i> (<i>cenpf</i>) [GenbankAM862170], four genes that increase in expression over the course of spermatogenesis: two unknown proteins [Genbanks AM864807 and AM857898], hypothetical protein <i>BRAFLDRAFT_118409</i> (<i>bindin</i>) [Genbank EF219429] and <i>histone H4</i> [Genbank DW713865], and five genes that increase in expression over the course of oogenesis : <i>vitellogenin-2</i> (<i>vit-2</i>) [Genbank CX069168], <i>vitellogenin-6</i> (<i>vit-6</i>) [Genbank AB084783], <i>forkhead box L2</i> (<i>foxL2</i>) [Genbank AM860211], <i>nanos homolog 3</i> (<i>nanos3</i>) [Genbank CU994694] and <i>regulator of chromosome condensation</i> (<i>rcc1</i>) [Genbank CU996984]. The patterns of transcripts abundance detected for these genes in the array and by real time qPCR showed extremely similar profiles (R<sup>2</sup> = 0.80). For microarray, only Site 1 samples are shown. Developmental stage (St3: stage 3; St2: stage 2; St1: stage 1; St0: stage 0) and sex (M: male and F: female) are indicated at the bottom of each figure. Bars represent standard deviation.</p>", "links"=>[], "tags"=>["molecular biology", "marine and aquatic sciences", "Computational biology", "physiology", "developmental biology", "mathematics"], "article_id"=>312036, "categories"=>["Molecular Biology", "Inorganic Chemistry", "Developmental Biology", "Mathematics", "Physiology", "Biological Sciences"], "users"=>["Nolwenn M. Dheilly", "Christophe Lelong", "Arnaud Huvet", "Kristell Kellner", "Marie-Pierre Dubos", "Guillaume Riviere", "Pierre Boudry", "Pascal Favrel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036353.g005", "stats"=>{"downloads"=>3, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_profile_of_selected_genes_/312036", "title"=>"Expression profile of selected genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-09 00:33:56"}
  • {"files"=>["https://ndownloader.figshare.com/files/330711", "https://ndownloader.figshare.com/files/330744", "https://ndownloader.figshare.com/files/330874", "https://ndownloader.figshare.com/files/330897"], "description"=>"<div><h3>Background</h3><p>The Pacific oyster <em>Crassostrea gigas</em> (Mollusca, Lophotrochozoa) is an alternative and irregular protandrous hermaphrodite: most individuals mature first as males and then change sex several times. Little is known about genetic and phenotypic basis of sex differentiation in oysters, and little more about the molecular pathways regulating reproduction. We have recently developed and validated a microarray containing 31,918 oligomers (Dheilly et al., 2011) representing the oyster transcriptome. The application of this microarray to the study of mollusk gametogenesis should provide a better understanding of the key factors involved in sex differentiation and the regulation of oyster reproduction.</p> <h3>Methodology/Principal Findings</h3><p>Gene expression was studied in gonads of oysters cultured over a yearly reproductive cycle. Principal component analysis and hierarchical clustering showed a significant divergence in gene expression patterns of males and females coinciding with the start of gonial mitosis. ANOVA analysis of the data revealed 2,482 genes differentially expressed during the course of males and/or females gametogenesis. The expression of 434 genes could be localized in either germ cells or somatic cells of the gonad by comparing the transcriptome of female gonads to the transcriptome of stripped oocytes and somatic tissues. Analysis of the annotated genes revealed conserved molecular mechanisms between mollusks and mammals: genes involved in chromatin condensation, DNA replication and repair, mitosis and meiosis regulation, transcription, translation and apoptosis were expressed in both male and female gonads. Most interestingly, early expressed male-specific genes included <em>bindin</em> and a <em>dpy-30</em> homolog and female-specific genes included <em>foxL2</em>, <em>nanos homolog 3</em>, a <em>pancreatic lipase related protein</em>, <em>cd63</em> and <em>vitellogenin.</em> Further functional analyses are now required in order to investigate their role in sex differentiation in oysters.</p> <h3>Conclusions/Significance</h3><p>This study allowed us to identify potential markers of early sex differentiation in the oyster <em>C. gigas</em>, an alternative hermaphrodite mollusk. We also provided new highly valuable information on genes specifically expressed by mature spermatozoids and mature oocytes.</p> </div>", "links"=>[], "tags"=>["gametogenesis", "pacific", "oyster", "microarrays-based", "identifies", "genes"], "article_id"=>125305, "categories"=>["Molecular Biology", "Inorganic Chemistry", "Developmental Biology", "Mathematics", "Physiology", "Biological Sciences"], "users"=>["Nolwenn M. Dheilly", "Christophe Lelong", "Arnaud Huvet", "Kristell Kellner", "Marie-Pierre Dubos", "Guillaume Riviere", "Pierre Boudry", "Pascal Favrel"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0036353.s001", "https://dx.doi.org/10.1371/journal.pone.0036353.s002", "https://dx.doi.org/10.1371/journal.pone.0036353.s003", "https://dx.doi.org/10.1371/journal.pone.0036353.s004"], "stats"=>{"downloads"=>15, "page_views"=>18, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Gametogenesis_in_the_Pacific_Oyster_Crassostrea_gigas_A_Microarrays_Based_Analysis_Identifies_Sex_and_Stage_Specific_Genes/125305", "title"=>"Gametogenesis in the Pacific Oyster <em>Crassostrea gigas</em>: A Microarrays-Based Analysis Identifies Sex and Stage Specific Genes", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-05-09 01:28:25"}
  • {"files"=>["https://ndownloader.figshare.com/files/641442"], "description"=>"<p>A/Hierarchical clustering obtained using Pearson’s correlation on the 434 genes differentially expressed in stage 3 females gonads and stripped stage 3 oocytes (T test, p<0.01, adjusted Bonferroni’s correction; rows) and on the 17 transcriptomic profiles of stage 3 female gonads (columns). Two sample branches are observed, clustering the 4 individual stage 3 female gonads (St3F) and the 6 pools of stage 3 female gonads (Gl3F for individuals from site 1 and Gc3F for individuals from site 2) together on a first and the 7 stripped stage 3 oocytes (LQ and HQ) together on a second branch. Two clusters of genes are observed, grouping genes more expressed in whole stage 3 female gonads apart from genes more expressed in stripped stage 3 oocytes. Genes more expressed in whole stage 3 female gonads are predicted to be expressed by somatic tissues, in contrast with genes significantly more expressed in stripped oocytes. Color represents the transformed normalized Cy3 log value obtained for each sample. The variations in transcript abundance are depicted with a color scale, in which shades of red represent higher gene expression and shades of green represent lower gene expression. B/Expression profiles of 2 genes expressed in somatic cells: <i>forkhead box L2</i> (<i>foxL2</i>) [Genbank AM860211] and <i>vitellogenin 6</i> [Genbank AB084783]; and of 4 genes expressed in oocytes: <i>forkhead box Q2</i> (<i>foxQ2</i>) [Genbank AM865563], <i>SWI/SNF-related matrix-associated actin-dependent regulator of chromatin</i> A1 (<i>smarc A1</i>) [Genbank AM869433], <i>DNA methyltransferase</i> (<i>dnmt</i>) [Genbank CU994437], and <i>insulin receptor</i> (<i>insulin Rc</i>) [Genbank AJ535669] as measured by microarray analysis. A and B/Microarray data are expressed in log center reduced normalized values.</p>", "links"=>[], "tags"=>["somatic"], "article_id"=>311925, "categories"=>["Molecular Biology", "Inorganic Chemistry", "Developmental Biology", "Mathematics", "Physiology", "Biological Sciences"], "users"=>["Nolwenn M. Dheilly", "Christophe Lelong", "Arnaud Huvet", "Kristell Kellner", "Marie-Pierre Dubos", "Guillaume Riviere", "Pierre Boudry", "Pascal Favrel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036353.g004", "stats"=>{"downloads"=>3, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Germ_cell_versus_somatic_gene_expression_/311925", "title"=>"Germ cell versus somatic gene expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-09 00:32:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/641063"], "description"=>"<p>3D Score plot using the first 3PCs identified by principal components analysis of all 31,918 transcripts in the 32 individual oyster gonads sampled from Site 1.</p>", "links"=>[], "tags"=>["molecular biology", "marine and aquatic sciences", "Computational biology", "physiology", "developmental biology", "mathematics"], "article_id"=>311538, "categories"=>["Molecular Biology", "Inorganic Chemistry", "Developmental Biology", "Mathematics", "Physiology", "Biological Sciences"], "users"=>["Nolwenn M. Dheilly", "Christophe Lelong", "Arnaud Huvet", "Kristell Kellner", "Marie-Pierre Dubos", "Guillaume Riviere", "Pierre Boudry", "Pascal Favrel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036353.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Principal_component_analysis_/311538", "title"=>"Principal component analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-09 00:25:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/641734"], "description"=>"<p>Genes differentially expressed during gametogenesis and their expression in somatic cells or oocytes.</p>", "links"=>[], "tags"=>["differentially", "gametogenesis", "somatic", "cells"], "article_id"=>312214, "categories"=>["Molecular Biology", "Inorganic Chemistry", "Developmental Biology", "Mathematics", "Physiology", "Biological Sciences"], "users"=>["Nolwenn M. Dheilly", "Christophe Lelong", "Arnaud Huvet", "Kristell Kellner", "Marie-Pierre Dubos", "Guillaume Riviere", "Pierre Boudry", "Pascal Favrel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036353.t001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genes_differentially_expressed_during_gametogenesis_and_their_expression_in_somatic_cells_or_oocytes_/312214", "title"=>"Genes differentially expressed during gametogenesis and their expression in somatic cells or oocytes.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-05-09 00:36:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/641300"], "description"=>"<p>Hierarchical clustering obtained using Pearson’s correlation on the 32 unique transcriptomic profiles of gonads (columns). Clusters of the 2,482 differentially expressed genes (rows) have been obtained with k means clustering using Pearson’s correlation. Individual gonad samples from the same developmental stage and sex grouped together. St3: stage 3; St2: stage 2; St1: stage 1; St0: stage 0. Genes showing similar expression profiles clustered together. Four main groups are identified: stage 0: genes more expressed at early gonadogenesis stages (stage 0 and stage 1); Males and females: genes that vary in expression over the course of both male and female gametogenesis; Male: genes that increase in expression over the course of spermatogenesis; Female: genes that increase in expression over the course of oogenesis. Color represents the transformed normalized Cy3 log value obtained for each sample. The variations in transcript abundance are depicted with a color scale, in which shades of red represent higher gene expression and shades of green represent lower gene expression.</p>", "links"=>[], "tags"=>["clusters", "genes", "differentially"], "article_id"=>311780, "categories"=>["Molecular Biology", "Inorganic Chemistry", "Developmental Biology", "Mathematics", "Physiology", "Biological Sciences"], "users"=>["Nolwenn M. Dheilly", "Christophe Lelong", "Arnaud Huvet", "Kristell Kellner", "Marie-Pierre Dubos", "Guillaume Riviere", "Pierre Boudry", "Pascal Favrel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036353.g003", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heat_map_of_clusters_of_genes_differentially_expressed_during_gametogenesis_/311780", "title"=>"Heat map of clusters of genes differentially expressed during gametogenesis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-09 00:29:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/641157"], "description"=>"<p>Hierarchical clustering obtained using Pearson’s correlation on the 77 genes differentially expressed in males and females (T test, p<0.01, adjusted Bonferroni’s correction, rows) and on all individual gonad samples (columns). Three sample branches are observed, mainly clustering stage 0 individuals, males, or females. Two gene branches are observed, clustering genes more expressed in males (cluster 1∶9 genes) or in females (cluster 2∶68 genes). Color represents the transformed normalized Cy3 log value obtained for each sample. The variations in transcript abundance are depicted with a color scale, in which shades of red represent higher gene expression and shades of green represent lower gene expression. St3: stage 3; St2: stage 2; St1: stage 1; St0: stage 0.</p>", "links"=>[], "tags"=>["molecular biology", "marine and aquatic sciences", "Computational biology", "physiology", "developmental biology", "mathematics"], "article_id"=>311634, "categories"=>["Molecular Biology", "Inorganic Chemistry", "Developmental Biology", "Mathematics", "Physiology", "Biological Sciences"], "users"=>["Nolwenn M. Dheilly", "Christophe Lelong", "Arnaud Huvet", "Kristell Kellner", "Marie-Pierre Dubos", "Guillaume Riviere", "Pierre Boudry", "Pascal Favrel"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0036353.g002", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Heat_map_of_sex_specific_genes_/311634", "title"=>"Heat map of sex specific genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-05-09 00:27:14"}

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Relative Metric

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Net::HTTPTooManyRequests

Source
Scopus
Time
2019-08-27 21:08:18 UTC
Target URL
https://api.elsevier.com/content/search/index:SCOPUS?query=DOI(10.1371%2Fjournal.pone.0036353)
Trace

/app/models/concerns/networkable.rb:21:in `get_result'
/app/models/source.rb:165:in `get_data'
/app/models/retrieval_status.rb:47:in `perform_get_data'
/app/jobs/source_job.rb:52:in `block (2 levels) in perform'
/app/jobs/source_job.rb:51:in `block in perform'
/app/jobs/source_job.rb:35:in `each'
/app/jobs/source_job.rb:35:in `perform'