Heterogeneous Conservation of Dlx Paralog Co-Expression in Jawed Vertebrates
Publication Date
June 28, 2013
Journal
PLOS ONE
Authors
Mélanie Debiais Thibaud, Cushla J. Metcalfe, Jacob Pollack, Isabelle Germon, et al
Volume
8
Issue
6
Pages
e68182
DOI
https://dx.plos.org/10.1371/journal.pone.0068182
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0068182
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/23840829
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3695995
Europe PMC
http://europepmc.org/abstract/MED/23840829
Web of Science
000321148400172
Scopus
84879517955
Mendeley
http://www.mendeley.com/research/heterogeneous-conservation-dlx-paralog-coexpression-jawed-vertebrates
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Mendeley | Further Information

{"title"=>"Heterogeneous Conservation of Dlx Paralog Co-Expression in Jawed Vertebrates", "type"=>"journal", "authors"=>[{"first_name"=>"Mélanie", "last_name"=>"Debiais-Thibaud", "scopus_author_id"=>"13407244500"}, {"first_name"=>"Cushla J.", "last_name"=>"Metcalfe", "scopus_author_id"=>"7005470532"}, {"first_name"=>"Jacob", "last_name"=>"Pollack", "scopus_author_id"=>"55765799300"}, {"first_name"=>"Isabelle", "last_name"=>"Germon", "scopus_author_id"=>"23008482900"}, {"first_name"=>"Marc", "last_name"=>"Ekker", "scopus_author_id"=>"7005882094"}, {"first_name"=>"Michael", "last_name"=>"Depew", "scopus_author_id"=>"9733450300"}, {"first_name"=>"Patrick", "last_name"=>"Laurenti", "scopus_author_id"=>"6603982065"}, {"first_name"=>"Véronique", "last_name"=>"Borday-Birraux", "scopus_author_id"=>"23007684400"}, {"first_name"=>"Didier", "last_name"=>"Casane", "scopus_author_id"=>"6601969481"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"doi"=>"10.1371/journal.pone.0068182", "issn"=>"19326203", "sgr"=>"84879517955", "scopus"=>"2-s2.0-84879517955", "pui"=>"369209168", "pmid"=>"23840829", "isbn"=>"1932-6203"}, "id"=>"b6ed293e-8c22-3288-8a16-67ce9c146ac7", "abstract"=>"BACKGROUND: The Dlx gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred before jawed vertebrates diversified. It includes at least three bigene pairs sharing conserved regulatory sequences in tetrapods and teleost fish, but has been only partially characterized in chondrichthyans, the third major group of jawed vertebrates. Here we take advantage of developmental and molecular tools applied to the shark Scyliorhinus canicula to fill in the gap and provide an overview of the evolution of the Dlx family in the jawed vertebrates. These results are analyzed in the theoretical framework of the DDC (Duplication-Degeneration-Complementation) model. RESULTS: The genomic organisation of the catshark Dlx genes is similar to that previously described for tetrapods. Conserved non-coding elements identified in bony fish were also identified in catshark Dlx clusters and showed regulatory activity in transgenic zebrafish. Gene expression patterns in the catshark showed that there are some expression sites with high conservation of the expressed paralog(s) and other expression sites with events of paralog sub-functionalization during jawed vertebrate diversification, resulting in a wide variety of evolutionary scenarios within this gene family. CONCLUSION: Dlx gene expression patterns in the catshark show that there has been little neo-functionalization in Dlx genes over gnathostome evolution. In most cases, one tandem duplication and two rounds of vertebrate genome duplication have led to at least six Dlx coding sequences with redundant expression patterns followed by some instances of paralog sub-functionalization. Regulatory constraints such as shared enhancers, and functional constraints including gene pleiotropy, may have contributed to the evolutionary inertia leading to high redundancy between gene expression patterns.", "link"=>"http://www.mendeley.com/research/heterogeneous-conservation-dlx-paralog-coexpression-jawed-vertebrates", "reader_count"=>25, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>5, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>4, "Researcher"=>7, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>4, "Student > Postgraduate"=>1, "Student > Master"=>5, "Other"=>1, "Student > Bachelor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>19, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>19}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>1}}, "reader_count_by_country"=>{"Brazil"=>1, "United Kingdom"=>2, "France"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1106449"], "description"=>"<p>Target gene name and stage of development are indicated on each panel. Transverse sections through whole-mount hybridized embryos at stage 25, dorsal to the top, at the level of the telencephalon (<b>A–C</b>) or more posterior through the diencephalon (<b>D–F</b>). <i>Dlx1</i>, <i>Dlx2</i> and <i>Dlx5</i> are expressed in scattered cells of the telencephalon (arrowhead in <b>A–C</b>) and of the diencephalon (arrow in <b>A</b> and <b>D–F</b>). Note expression of <i>Dlx1</i> in scattered cells of the head mesenchyme at the mandibular level, interpreted as cranial neural crest cells (cnc). Scale bars: 50 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis"], "article_id"=>735744, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g009", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dlx_gene_expression_during_brain_development_in_the_catshark_/735744", "title"=>"<i>Dlx</i> gene expression during brain development in the catshark.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106444"], "description"=>"<p>The blue circle represents the hypothetical apparition of <i>Dlx</i> expression in this structure and blue cross indicates loss of expression for both <i>Dlx</i> genes of a cluster. A tilted bar indicates when only one gene of a cluster has lost expression in his structure. Genes for which expression is known to be positive are written black while genes for which no expression has been recorded are indicated in grey.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "genes", "paired", "sensory", "placodes", "vesicles"], "article_id"=>735739, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g007", "stats"=>{"downloads"=>1, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_scenario_for_the_expression_of_Dlx_genes_in_developing_paired_sensory_placodes_A_and_vesicles_B_/735739", "title"=>"Evolutionary scenario for the expression of <i>Dlx</i> genes in developing paired sensory placodes (A) and vesicles (B).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106443"], "description"=>"<p>Target gene name is indicated in each box, developmental stage is indicated in each panel. <b>A–F</b>: lateral views of whole-mount hybridized embryos, anterior to the left, dorsal to the top. <b>A1, B1, C1–4, D1–4, E1–4, F1–4</b>: transverse sections, dorsal to the top. <b>A1</b>, <b>B1</b> are taken at the level of section plan #1 in panel A, showing the otic vesicle (otv); <b>C1–F1</b> are taken at the level of section plan #1 in panel C, showing the olfactory placode (olp); <b>C2–F2</b> are taken at the level of section plan #2 in panel C, showing the otic vesicle; <b>C3–F3</b> are taken at the level of section plan #3 in panel C, showing the presumptive pectoral fin bud (pf, arrows, higher magnification in the bottom right corner in F4); <b>C4–F4</b> are taken at the level of section plan #4 in panel C, showing the median fin fold (mff, asterisk) and the <i>analia genitalia</i> (ag, double arrowheads,except in F4). Other legends as in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068182#pone-0068182-g005\" target=\"_blank\">Figure 5</a>. Scale bars: A–F: 400 µm; A1, B1, C1–4, D1–4, E1–4, F1–4∶100 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "catshark"], "article_id"=>735738, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g006", "stats"=>{"downloads"=>0, "page_views"=>5, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dlx_gene_expression_during_early_organogenesis_in_the_catshark_stage_24_25_/735738", "title"=>"<i>Dlx</i> gene expression during early organogenesis in the catshark (stage 24–25).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106456"], "description"=>"<p>Catshark CNE length and similarity defined through comparison to the mouse (<i>Mus musculus</i>) and zebrafish (<i>Danio rerio</i>) intergenic sequences.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "cne", "defined", "zebrafish", "intergenic"], "article_id"=>735751, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.t001", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Catshark_CNE_length_and_similarity_defined_through_comparison_to_the_mouse_Mus_musculus_and_zebrafish_Danio_rerio_intergenic_sequences_/735751", "title"=>"Catshark CNE length and similarity defined through comparison to the mouse (<i>Mus musculus</i>) and zebrafish (<i>Danio rerio</i>) intergenic sequences.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106457"], "description"=>"<div><p>Background</p><p>The <i>Dlx</i> gene family encodes transcription factors involved in the development of a wide variety of morphological innovations that first evolved at the origins of vertebrates or of the jawed vertebrates. This gene family expanded with the two rounds of genome duplications that occurred before jawed vertebrates diversified. It includes at least three bigene pairs sharing conserved regulatory sequences in tetrapods and teleost fish, but has been only partially characterized in chondrichthyans, the third major group of jawed vertebrates. Here we take advantage of developmental and molecular tools applied to the shark <i>Scyliorhinus canicula</i> to fill in the gap and provide an overview of the evolution of the <i>Dlx</i> family in the jawed vertebrates. These results are analyzed in the theoretical framework of the DDC (Duplication-Degeneration-Complementation) model.</p><p>Results</p><p>The genomic organisation of the catshark <i>Dlx</i> genes is similar to that previously described for tetrapods. Conserved non-coding elements identified in bony fish were also identified in catshark <i>Dlx</i> clusters and showed regulatory activity in transgenic zebrafish. Gene expression patterns in the catshark showed that there are some expression sites with high conservation of the expressed paralog(s) and other expression sites with events of paralog sub-functionalization during jawed vertebrate diversification, resulting in a wide variety of evolutionary scenarios within this gene family.</p><p>Conclusion</p><p><i>Dlx</i> gene expression patterns in the catshark show that there has been little neo-functionalization in <i>Dlx</i> genes over gnathostome evolution. In most cases, one tandem duplication and two rounds of vertebrate genome duplication have led to at least six <i>Dlx</i> coding sequences with redundant expression patterns followed by some instances of paralog sub-functionalization. Regulatory constraints such as shared enhancers, and functional constraints including gene pleiotropy, may have contributed to the evolutionary inertia leading to high redundancy between gene expression patterns.</p></div>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "heterogeneous", "paralog", "co-expression", "jawed", "vertebrates"], "article_id"=>735752, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182", "stats"=>{"downloads"=>1, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Heterogeneous_Conservation_of_Dlx_Paralog_Co_Expression_in_Jawed_Vertebrates/735752", "title"=>"Heterogeneous Conservation of <i>Dlx</i> Paralog Co-Expression in Jawed Vertebrates", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106455"], "description"=>"<p>Positive expression is shown with a +. Stage of expression indicated in first column. +fold indicates when expression is found restricted to the folding part of an organ. mff: median fin fold; NCC: neural crest cells; nne: non-neural ectoderm; olp: olfactory placode; olv: olfactory vesicle; otp: otic placode; otv: otic vesicle; pf: pectoral fin; Pres.: presumptive. Asterisk is for specific <i>lateral</i> expression of <i>Dlx1</i> and <i>Dlx2</i>.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "patterns", "15", "st25"], "article_id"=>735750, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.t002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Summary_of_Dlx_expression_patterns_between_stage_st_15_and_st25_in_the_catshark_/735750", "title"=>"Summary of <i>Dlx</i> expression patterns between stage (st) 15 and st25 in the catshark.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106433"], "description"=>"<p>For each bigene cluster, exons are indicated as white boxes with associated number (from 1: first exon, to 3: last exon). Transcribed sequences are indicated as blue arrows, conserved non-coding elements as orange circles. Unsequenced regions are shown as dashed lines.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "catshark"], "article_id"=>735729, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Genomic_organization_of_the_Dlx_gene_family_in_the_catshark_Scyliorhinus_canicula_/735729", "title"=>"Genomic organization of the <i>Dlx</i> gene family in the catshark <i>Scyliorhinus canicula</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106451"], "description"=>"<p><b>A–E</b>: lateral views of whole-mount embryos, anterior is to the top, dorsal to the right, between stage 17 and 21. <b>F</b>: schematic of the head for embryo in panel B with location (blue colored) of the various streams of migrating neural crest cells: trigeminal (tg) stream separated in the premandibular (pm) and the mandiblar (m) streams; hyoid (h) stream; branchial (b) stream. <b>G–K</b> are transverse sections made on the embryo shown in panel B. The section level is located on panel F: G =  section 1(S1) to K =  section 5 (S5). <b>A</b>: stage 17, expression is restricted to the neural crest cells both at the cranial and trunk level. <b>B</b>: streams of cranial neural crest cells migrate ventrally: <i>Dlx2</i> expression detected in the various cranial neural crest streams and most posteriorly in the trunk neural crest cells (tnc). <b>D, E</b>: after migration, <i>Dlx2</i>-positive cells are found in the mesenchyme of branchial arches (ba). ba1: first branchial arch, ba2: second branchial arch, oc: optic vesicle, nt: neural tube. Scale bars: A–E: 200 µm; G–K: 100 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "neural", "crest", "cells"], "article_id"=>735746, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g011", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dlx2_expression_in_neural_crest_cells_in_the_catshark_/735746", "title"=>"<i>Dlx2</i> expression in neural crest cells in the catshark.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106432"], "description"=>"<p>Phylogenetic relationships between chordate <i>Dlx</i> gene family members including: the single amphioxus Amphi-Dll gene <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068182#pone.0068182-Holland1\" target=\"_blank\">[36]</a>; the three <i>Ciona Dlx</i> genes: <i>Ciona-DllA</i> and <i>Ciona-DllB</i> forming a bigene cluster and single <i>Ciona-DllC </i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068182#pone.0068182-Caracciolo1\" target=\"_blank\">[35]</a>; six <i>Dlx</i> genes from the mouse (<i>Mus musculus</i>, noted <i>Mm</i>) and catshark (<i>Scyliorhinus canicula</i>, noted <i>Sc</i>) organized as three bigene clusters: <i>Dlx1</i>–<i>Dlx2</i>, <i>Dlx3</i>–<i>Dlx4</i>, <i>Dlx5</i>–<i>Dlx6</i>. Zebrafish <i>dlx</i> genes are figured as three bigene clusters plus additional single genes (originating from the teleost-specific whole genome duplication): <i>dlx1a</i>-<i>dlx2a</i> plus <i>dlx2b</i>, <i>dlx3b</i>-<i>dlx4b</i> plus <i>dlx4a</i>, <i>dlx5a</i>-<i>dlx6a</i>. The first tandem duplication is mapped as a brown square (TD), the two vertebrate rounds of genome duplication are mapped as yellow squares annotated R1 and R2, the grey dashed line separates an early phase of <i>Dlx</i> paralog divergence before gnathostome diversification from the later phase occurring during gnathostome lineages divergence.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "extant", "chordate"], "article_id"=>735728, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_events_leading_to_the_extant_chordate_Dlx_gene_family_/735728", "title"=>"Evolutionary events leading to the extant chordate <i>Dlx</i> gene family.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106446"], "description"=>"<p>See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068182#pone-0068182-g004\" target=\"_blank\">Figure 4</a> for legends.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "genes", "median", "fin"], "article_id"=>735741, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g008", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_scenario_for_the_expression_of_Dlx_genes_in_fins_limbs_A_median_fin_fold_B_and_analia_genitalia_C_/735741", "title"=>"Evolutionary scenario for the expression of <i>Dlx</i> genes in fins/limbs (A), median fin fold (B) and <i>analia</i>-<i>genitalia</i> (C).", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106442"], "description"=>"<p>Target gene name is indicated on top of each column, stage of development is indicated on top of each box. <b>A–D</b>, <b>A</b>′<b>–D</b>′: lateral views of whole-mount embryos; <b>A–D</b> dorsal to the top, anterior to the left; <b>A</b>′<b>–D</b>′ are anterior to the top, dorsal to the right. <b>A1–3, B1–3, C1–3, D1–3, A</b>′<b>1–3, B</b>′<b>1–3, C</b>′<b>1–3, D</b>′<b>1–3</b> are transverse sections with dorsal to the top; <b>A1–D1</b> go across the presumptive olfactory placode (black arrow) as located by section plan #1 on the A panel; <b>A2–D2</b> go across the presumptive otic placode (double arrowhead), plan #2 on the A panel; <b>A3–D3</b> go across the trunk with developing median fin fold (asterisk), plan #3 on the A panel; <b>A</b>′<b>1–D</b>′<b>1</b> go across the olfactory placode (olp) and lens placode (arrowhead), plan #1 on the A′ panel; <b>A</b>′<b>2–D</b>′<b>2</b> go across the folding otic vesicle (otv), plan #2 on the A′ panel; <b>A</b>′<b>3–D</b>′<b>3</b> go across the trunk with developing median fin fold (mff), plan #3 on the A′ panel. ce: cephalic epithelium; cv : cephalic vesicle; fb: forebrain; lm: lateral mesoderm; n: notochord; nt: neural tube; oc: optic cup; rb: rhombencephalon. Scale bars: A–D, A′–D′: 200 µm; A1–3, B1–3, C1–3, D1–3∶50 µm; A′1–3, B′1–3, C′1–3, D′1–3∶100 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "patterns", "17", "21"], "article_id"=>735737, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g005", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dlx_gene_expression_patterns_at_stage_17_and_21_in_the_catshark_/735737", "title"=>"<i>Dlx</i> gene expression patterns at stage 17 and 21 in the catshark.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106454"], "description"=>"<p><b>A–C</b>: GFP expression under catshark I12b regulation at 24 hpf (A, lateral view, dorsal to the top, anterior to the left) and 56 hpf (B, lateral view oriented as A; C: ventral view, anterior to the left). <b>D–F</b>: GFP expression under catshark I56i regulation at similar stage with similar orientation. The dashed line separates the telencephalon (arrowhead, with expression) from the diencephalon (no expression). Scale bar: 100 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "transgenic", "gfp", "zebrafish", "embryos", "catshark", "cne"], "article_id"=>735749, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g013", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Transient_transgenic_expression_of_GFP_in_zebrafish_embryos_under_catshark_CNE_regulation_/735749", "title"=>"Transient transgenic expression of GFP in zebrafish embryos under catshark CNE regulation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106436"], "description"=>"<p>Genes for which expression is known to be positive are written black while genes for which no expression has been recorded are indicated in grey. The blue circle represents the hypothetical apparition of <i>Dlx</i> expression in this structure and blue cross indicates loss of expression for both <i>Dlx</i> genes of a bigene cluster. Teleost duplicates in the zebrafish were pooled together to simplify the analysis.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "genes", "neural"], "article_id"=>735731, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_scenario_for_the_expression_of_Dlx_genes_at_the_neural_plate_border_in_chordates_/735731", "title"=>"Evolutionary scenario for the expression of <i>Dlx</i> genes at the neural plate border in chordates.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106453"], "description"=>"<p>See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068182#pone-0068182-g004\" target=\"_blank\">Figure 4</a> for legends.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "genes", "premigrating", "migrating", "neural", "crest"], "article_id"=>735748, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g012", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_scenario_for_the_expression_of_Dlx_genes_in_premigrating_and_migrating_neural_crest_cells_/735748", "title"=>"Evolutionary scenario for the expression of <i>Dlx</i> genes in premigrating and migrating neural crest cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106450"], "description"=>"<p>See <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0068182#pone-0068182-g004\" target=\"_blank\">Figure 4</a> for legends.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "genes", "anterior"], "article_id"=>735745, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g010", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Evolutionary_scenario_for_the_expression_of_Dlx_genes_in_anterior_brain_/735745", "title"=>"Evolutionary scenario for the expression of <i>Dlx</i> genes in anterior brain.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106435"], "description"=>"<p>Target gene name and developmental stage are indicated for each box. Expression is evidenced by blue precipitate in cells of the non-neural ectoderm, both extra-embryonic ectoderm (ee) and embryonic ectoderm (e), including at the border of the neural plate (np, arrowhead). <b>A–C</b>: <i>Dlx3</i>, <i>Dlx4</i>, <i>Dlx5</i> expression patterns at stage 15, <i>in toto</i>; <b>D–G</b>: sections taken from embryo in C showing histological details of <i>Dlx5</i> expression pattern at stage 15. <b>H–J</b>: <i>Dlx6</i> expression pattern at stage 15. <b>K–M</b>: <i>Dlx6</i> expression pattern at stage 16. <b>A–C, H</b>: whole-mount dorsal views, anterior to the top. <b>D–G, I, J, L, M</b>: serial transverse sections, dorsal to the top; <b>D–G</b> from embryo in panel C, <b>D</b>: section 1 to <b>G</b>: section 4. <b>I–J</b> from embryo in panel H, section 1 =  panel I, section 2 =  panel J, with expression restricted to the ectoderm at the neural plate border. <b>K</b>: lateral view, dorsal to the right, anterior to the top, with location of the transverse sections, section 1 in panel L, section 2 in panel M. n: notochord; en: endoderm; lm: lateral mesoderm; y: yolk. Scale bars: A–C, H, K: 200 µm, D–G, I, J, L, M: 100 µm.</p>", "links"=>[], "tags"=>["developmental biology", "morphogenesis", "Body plan organization", "Organism development", "organogenesis", "embryology", "Evolutionary developmental biology", "Evolutionary biology", "Forms of evolution", "macroevolution", "Organismal evolution", "Animal evolution", "Comparative genomics", "genomics", "Genome expression analysis", "patterns", "neurulation"], "article_id"=>735730, "categories"=>["Biological Sciences"], "users"=>["Mélanie Debiais-Thibaud", "Cushla J. Metcalfe", "Jacob Pollack", "Isabelle Germon", "Marc Ekker", "Michael Depew", "Patrick Laurenti", "Véronique Borday-Birraux", "Didier Casane"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068182.g003", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Dlx_gene_expression_patterns_during_neurulation_stage_15_16_in_the_catshark_/735730", "title"=>"<i>Dlx</i> gene expression patterns during neurulation (stage 15–16) in the catshark.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:30:50"}

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  • {"unique-ip"=>"3", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"3"}
  • {"unique-ip"=>"4", "full-text"=>"3", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"4"}
  • {"unique-ip"=>"5", "full-text"=>"9", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"1", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"5"}
  • {"unique-ip"=>"4", "full-text"=>"2", "pdf"=>"2", "scanned-summary"=>"0", "scanned-page-browse"=>"0", "figure"=>"0", "supp-data"=>"0", "cited-by"=>"0", "year"=>"2019", "month"=>"8"}

Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Developmental biology", "average_usage"=>[275, 472, 605, 720, 822, 921, 1013, 1106, 1200, 1289, 1378, 1459, 1531]}, {"subject_area"=>"/Biology and life sciences/Evolutionary biology", "average_usage"=>[302, 488, 607, 717, 832, 931, 1024, 1117, 1212, 1302, 1389, 1469, 1535]}, {"subject_area"=>"/Biology and life sciences/Neuroscience", "average_usage"=>[261, 444, 554, 655, 748, 834, 923, 1004, 1089, 1170, 1244, 1315, 1380]}, {"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}]}
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