Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (Shh, Ihh and Dhh) in Vertebrates
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{"title"=>"Evolutionary genomics and adaptive evolution of the hedgehog gene family (Shh, Ihh and Dhh) in vertebrates", "type"=>"journal", "authors"=>[{"first_name"=>"Joana", "last_name"=>"Pereira", "scopus_author_id"=>"57193624968"}, {"first_name"=>"Warren E.", "last_name"=>"Johnson", "scopus_author_id"=>"55506064900"}, {"first_name"=>"Stephen J.", "last_name"=>"O'Brien", "scopus_author_id"=>"7402355306"}, {"first_name"=>"Erich D.", "last_name"=>"Jarvis", "scopus_author_id"=>"35414140800"}, {"first_name"=>"Guojie", "last_name"=>"Zhang", "scopus_author_id"=>"55572538400"}, {"first_name"=>"M. Thomas P.", "last_name"=>"Gilbert", "scopus_author_id"=>"7202762494"}, {"first_name"=>"Vitor", "last_name"=>"Vasconcelos", "scopus_author_id"=>"7004649080"}, {"first_name"=>"Agostinho", "last_name"=>"Antunes", "scopus_author_id"=>"7102537544"}], "year"=>2014, "source"=>"PLoS ONE", "identifiers"=>{"pui"=>"601098024", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "doi"=>"10.1371/journal.pone.0074132", "scopus"=>"2-s2.0-84920130334", "pmid"=>"25549322", "sgr"=>"84920130334"}, "id"=>"29ba6051-12e1-3c90-82c5-e1cf0b610201", "abstract"=>"The Hedgehog (Hh) gene family codes for a class of secreted proteins composed of two active domains that act as signalling molecules during embryo development, namely for the development of the nervous and skeletal systems and the formation of the testis cord. While only one Hh gene is found typically in invertebrate genomes, most vertebrates species have three (Sonic hedgehog--Shh; Indian hedgehog--Ihh; and Desert hedgehog--Dhh), each with different expression patterns and functions, which likely helped promote the increasing complexity of vertebrates and their successful diversification. In this study, we used comparative genomic and adaptive evolutionary analyses to characterize the evolution of the Hh genes in vertebrates following the two major whole genome duplication (WGD) events. To overcome the lack of Hh-coding sequences on avian publicly available databases, we used an extensive dataset of 45 avian and three non-avian reptilian genomes to show that birds have all three Hh paralogs. We find suggestions that following the WGD events, vertebrate Hh paralogous genes evolved independently within similar linkage groups and under different evolutionary rates, especially within the catalytic domain. The structural regions around the ion-binding site were identified to be under positive selection in the signaling domain. These findings contrast with those observed in invertebrates, where different lineages that experienced gene duplication retained similar selective constraints in the Hh orthologs. Our results provide new insights on the evolutionary history of the Hh gene family, the functional roles of these paralogs in vertebrate species, and on the location of mutational hotspots.", "link"=>"http://www.mendeley.com/research/evolutionary-genomics-adaptive-evolution-hedgehog-gene-family-shh-ihh-dhh-vertebrates", "reader_count"=>44, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>6, "Professor"=>5}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>3, "Researcher"=>5, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>13, "Student > Postgraduate"=>1, "Student > Master"=>7, "Other"=>1, "Student > Bachelor"=>6, "Professor"=>5}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>12, "Agricultural and Biological Sciences"=>22, "Medicine and Dentistry"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>1, "Linguistics"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>22}, "Computer Science"=>{"Computer Science"=>1}, "Linguistics"=>{"Linguistics"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>12}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"United States"=>1, "South Africa"=>1}, "group_count"=>2}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1857459"], "description"=>"<p>The hedgehog proteins are composed by two main domains: the Hedge (N-terminal) and Hog (C-terminal) domains. The Hedge domain forms the HhN portion of the Hh proteins (together with the signaling sequence, SS) that is separated from the rest of protein by an auto-cleavage reaction preformed by the Hog domain <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Lee1\" target=\"_blank\">[4]</a>. The Hog domain forms the HhC portion of the Hh proteins and shares similarity with self-splicing Inteins on the Hint module <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Burglin2\" target=\"_blank\">[22]</a>. The auto-cleavage reaction occurs on a GCF (glycine-cysteine-phenylalanine) motif that forms the boundary between the two main parts of the Hh proteins, with the cysteine residue initiating a nucleophilic attack on the carbonyl carbon of the preceding residue, the glycine <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Beachy1\" target=\"_blank\">[5]</a>. The sterol-recognition region (SRR) forms the C-terminal region of the Hog domain and binds a cholesterol moiety that acts as an electron donor on a second nucleophilic attack that results in the cleavage of the bound between the glycine and cystein residues and in the attachment of the cholesterol moiety to the glycine residue <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Beachy1\" target=\"_blank\">[5]</a>. After auto-cleavage, the sterified HhN fragment is further palmitoylated on the cystein residue immediately after the SS region <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Chamoun1\" target=\"_blank\">[13]</a> and leaves the endoplasmic reticulum (ER) for later export <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Chen3\" target=\"_blank\">[11]</a>.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281650, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structural_features_of_the_Hh_proteins_/1281650", "title"=>"Structural features of the Hh proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857463"], "description"=>"<p>Information for all vertebrate and invertebrate species listed on Genomicus 64.01 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Muffato1\" target=\"_blank\">[37]</a>. A dotted line between two genes is equivalent to a gap in the alignment, i.e. the two genes are neighbors in this species but not in the reference species, where their orthologs are separated by one or more genes. On the other hand, a large white space indicates that the genes are found on the subject genome but are located on different chromosomes/scaffolds. A question mark (?) indicates that the syntenic relationship is not known. Genes outlined by a black line where found using Genomicus 64.01 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Flicek1\" target=\"_blank\">[38]</a> and genes outlined by a grey line were found by blast searches over the GenBank <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Benson1\" target=\"_blank\">[42]</a> and Ensembl <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Flicek1\" target=\"_blank\">[38]</a> databases. The absence of a gene represents that that gene is not annotated on Genomicus 64.01 and was not found by blast searches.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281654, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Illustrative_representation_of_the_presence_of_Hh_and_syntenic_related_genes_in_vertebrates_according_to_Genomicus_64_01_37_and_the_GenBank_42_and_Ensembl_38_databases_/1281654", "title"=>"Illustrative representation of the presence of <i>Hh</i> and syntenic related genes in vertebrates according to Genomicus 64.01 [37] and the GenBank [42] and Ensembl [38] databases.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857467"], "description"=>"<p>(A) The tetrapod <i>LMBR1L–Dhh-RHEBL1-MLL2</i> gene cluster is found on the scaffold GL343198.1 scaffold of the <i>A. carolinensis</i> assembly (anoCar 2.0 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Alfldi1\" target=\"_blank\">[105]</a>), and a similar cluster is also found on the 373.1 scaffold of the <i>F. peregrinus</i> genome assembly. (B) The four main <i>C. mydas</i> scaffolds show great homology for specific regions of the lizard GL343198.1 scaffold, (C) six on the <i>F. peregrinus</i> genome, and (d) on <i>G. Gallus</i> genome homology is found on two macrochromosomes, a linkage group and the Un_random chromosome. (e) The 429 and 439 <i>C. mydas</i> scaffold have high homology with a great part of the chicken E22C19W28_E50C23 linkage group and several random regions of the chicken Un_random chromosome. (F) The 350.1 and 373.1 <i>F. peregrinus</i>scaffold have high homology with several random regions of the <i>G. gallus</i> Un_random chromosome. (E) Hits for the <i>F. peregrinus</i> cluster are found on <i>G. gallus</i> genome mainly for the <i>MLL2</i> gene.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281658, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Homology_between_the_Anolis_carolinensis_Dhh_gene_synteny_and_the_Chelonia_mydas_Falcon_peregrinus_and_Gallus_gallus_genomes_using_nucleotide_information_/1281658", "title"=>"Homology between the <i>Anolis carolinensis Dhh</i> gene synteny and the <i>Chelonia mydas, Falcon peregrinus</i> and <i>Gallus gallus</i> genomes, using nucleotide information.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857469"], "description"=>"<p>(<b>A</b>) The phylogenetic tree was constructed using Maximum Likelihood (PhyML <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Guindon1\" target=\"_blank\">[83]</a>) and Bayesian inference (MrBayes <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Huelsenbeck1\" target=\"_blank\">[84]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Ronquist1\" target=\"_blank\">[85]</a>) algorithms, with supporting values as branch labels (ML/Bayesian). The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. The post-duplication branches tested with the branch model implemented in PAML <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Yang1\" target=\"_blank\">[46]</a> are represented in bold and the faster evolving ones are coloured red. (B) The degree of similarity between Hh proteins and (C) the evolutionary distances between <i>Hh</i> coding sequences, inferred using MEGA 5 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Tamura1\" target=\"_blank\">[77]</a>, and (D) the type I functional divergence coefficient values (θ<sub>I</sub>) between Hh proteins, inferred using DIVERGE 2.0 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Gu4\" target=\"_blank\">[60]</a>, are shown.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281660, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_relationship_of_Hh_coding_sequences_/1281660", "title"=>"Phylogenetic relationship of <i>Hh</i> coding sequences.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857470"], "description"=>"<p>Sliding windown analysis of the dN/dS ratio applying the SLAC and FEL methods <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-KosakovskyPond1\" target=\"_blank\">[49]</a> for the three vertebrate <i>Hh</i> paralogs, represented as a mobile mean with a period of 3. The phylogenetic relationship between each group and the mean omega value (ω) for each branch calculated with PAML v4.3 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Yang1\" target=\"_blank\">[46]</a> are shown. The Hh proteins domains are displayed as annotated for the Hh, Dhh, Ihh and Shh proteins on the GenBank <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Benson1\" target=\"_blank\">[42]</a> and UniProt <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Krzywinski1\" target=\"_blank\">[113]</a> databases.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281661, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differences_in_the_selection_pattern_of_the_three_vertebrate_Hh_paralogs_/1281661", "title"=>"Differences in the selection pattern of the three vertebrate <i>Hh</i> paralogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857471"], "description"=>"<p>Two different signifcance levels are shown: (Z-score > |1.64|) to detect significant selective signatures and (Z-score > |3.09|) to detect strong selective signatures. Amino acid properties are classified as chemical (C), structural (S) and other (O), according to da Fonseca <i>et al.</i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-daFonseca1\" target=\"_blank\">[54]</a>.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281662, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Amino_acid_properties_under_positive_red_and_negative_green_selection_in_vertebrate_Hh_coding_sequences_/1281662", "title"=>"Amino acid properties under positive (red) and negative (green) selection in vertebrate <i>Hh</i> coding sequences.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857473"], "description"=>"<p>Sliding window analysis for the Z-scores calculated for categories 7 and 8 using TreeSAAP <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Woolley1\" target=\"_blank\">[56]</a> for the three vertebrate <i>Hh</i> paralogs, showing the phylogenetic relationship between each group.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281664, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differences_on_the_amino_acid_isoelectric_point_property_selection_pattern_for_the_three_vertebrate_Hh_paralogs_/1281664", "title"=>"Differences on the amino acid isoelectric point property selection pattern for the three vertebrate <i>Hh</i> paralogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857474"], "description"=>"<p>Posterior probability for predicting critical amino acid residues for the functional divergence between the three vertebrate members of the Hh family. The arrows point to the residues with P(S<sub>1</sub>|S<sub>0</sub>) >0.91 and their position on the Hh proteins primary structure.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281665, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Type_I_functional_divergence_over_the_vertebrate_Hh_paralogs_/1281665", "title"=>"Type I functional divergence over the vertebrate Hh paralogs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857478"], "description"=>"<p>(A) Tridimensional representation of Hedge (PDB: 3HO5) and Hog (Shh modelled by homology) domains, coloured according to key identified regions. A straight orange line denotes how both domains may be linked in the pro-protein. Key residues important for binding and forming the catalytic site are represented in yellow spheres, numbered according to the human Shh protein <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-McLellan1\" target=\"_blank\">[72]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Krzywinski1\" target=\"_blank\">[113]</a>, <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Magrane1\" target=\"_blank\">[114]</a>. (B) Tridimensional arrangement of negatively and positively selected regions across the Hedge (HhN) and Hog (HhC) domains. Proteins (ShhN: PDB 3HO5, DhhN: PDB 2WFR; IhhN: PDB 3K7G) represented in grey cartoon with transparent surface. Calcium ions are not represented on the IhhN peptide due to the absence of the ions on the PDB file. Negatively selected sites (green) identified with FEL, positively selected regions for the amino acid isoelectric point property (orange) and positively selected sites (red) identified with TreeSAAP are shown for each paralog domain. A dashed circle denotes the position of the zinc/calcium binding site and the catalytic site.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281669, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g009"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Tridimensional_arrangement_of_negatively_and_positively_regions_in_the_Hedge_domain_of_vertebrate_Hedgehog_proteins_/1281669", "title"=>"Tridimensional arrangement of negatively and positively regions in the Hedge domain of vertebrate Hedgehog proteins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857480"], "description"=>"<p>A dotted line between two genes is equivalent means these two genes are neighbors in this species but not in the reference species, where their orthologs are separated by one or more genes. The 3<sup>rd</sup> WGD duplication in the teleost lineage is not represented.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281671, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.g010"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Illustrative_representation_of_the_evolution_of_the_LMBR1L_Dhh_RHEBL1_MLL2_linkage_group_evolution_in_vertebrates_and_their_paralogs_on_the_synteny_of_vertebrate_Shh_and_Ihh_genes_/1281671", "title"=>"Illustrative representation of the evolution of the LMBR1L–Dhh-RHEBL1-MLL2 linkage group evolution in vertebrates and their paralogs on the synteny of vertebrate <i>Shh</i> and <i>Ihh</i> genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857481"], "description"=>"<p>Likelihood parameter estimates under lineage-specific model of post-duplication branches of <i>Hh</i> vertebrate paralogs, branch calculated with PAML v4.3 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Delport1\" target=\"_blank\">[51]</a>.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281672, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.t001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Likelihood_parameter_estimates_under_lineage_specific_model_of_post_duplication_branches_of_Hh_vertebrate_paralogs_branch_calculated_with_PAML_v4_3_51_/1281672", "title"=>"Likelihood parameter estimates under lineage-specific model of post-duplication branches of <i>Hh</i> vertebrate paralogs, branch calculated with PAML v4.3 [51].", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857482"], "description"=>"<p>An asterisk (*) marks the accepted model.</p><p>Likelihood parameter estimates under site-specific models of <i>Hh</i> vertebrate paralogs, branch calculated with PAML v4.3 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0074132#pone.0074132-Delport1\" target=\"_blank\">[51]</a>.</p>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281673, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.t002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Likelihood_parameter_estimates_under_site_specific_models_of_Hh_vertebrate_paralogs_branch_calculated_with_PAML_v4_3_51_/1281673", "title"=>"Likelihood parameter estimates under site-specific models of <i>Hh</i> vertebrate paralogs, branch calculated with PAML v4.3 [51].", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2014-12-30 02:59:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/1857493", "https://ndownloader.figshare.com/files/1857494", "https://ndownloader.figshare.com/files/1857495", "https://ndownloader.figshare.com/files/1857496", "https://ndownloader.figshare.com/files/1857497", "https://ndownloader.figshare.com/files/1857498"], "description"=>"<div><p>The Hedgehog (<i>Hh</i>) gene family codes for a class of secreted proteins composed of two active domains that act as signalling molecules during embryo development, namely for the development of the nervous and skeletal systems and the formation of the testis cord. While only one <i>Hh</i> gene is found typically in invertebrate genomes, most vertebrates species have three (Sonic hedgehog – <i>Shh</i>; Indian hedgehog – <i>Ihh</i>; and Desert hedgehog – <i>Dhh</i>), each with different expression patterns and functions, which likely helped promote the increasing complexity of vertebrates and their successful diversification. In this study, we used comparative genomic and adaptive evolutionary analyses to characterize the evolution of the <i>Hh</i> genes in vertebrates following the two major whole genome duplication (WGD) events. To overcome the lack of <i>Hh</i>-coding sequences on avian publicly available databases, we used an extensive dataset of 45 avian and three non-avian reptilian genomes to show that birds have all three <i>Hh</i> paralogs. We find suggestions that following the WGD events, vertebrate <i>Hh</i> paralogous genes evolved independently within similar linkage groups and under different evolutionary rates, especially within the catalytic domain. The structural regions around the ion-binding site were identified to be under positive selection in the signaling domain. These findings contrast with those observed in invertebrates, where different lineages that experienced gene duplication retained similar selective constraints in the <i>Hh</i> orthologs. Our results provide new insights on the evolutionary history of the <i>Hh</i> gene family, the functional roles of these paralogs in vertebrate species, and on the location of mutational hotspots.</p></div>", "links"=>[], "tags"=>["expression patterns", "Hh gene", "Hedgehog Gene Family", "testis cord", "findings contrast", "Evolutionary Genomics", "gene family codes", "genome duplication", "WGD events", "Hh gene family", "Hh paralogous genes", "Gene duplication", "linkage groups", "Hh genes", "Hh orthologs", "invertebrate genomes", "embryo development", "Adaptive Evolution", "Hh paralogs", "vertebrates species", "hedgehog"], "article_id"=>1281684, "categories"=>["Biological Sciences"], "users"=>["Joana Pereira", "Warren E. Johnson", "Stephen J. O’Brien", "Erich D. Jarvis", "Guojie Zhang", "M. Thomas P. Gilbert", "Vitor Vasconcelos", "Agostinho Antunes"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0074132.s001", "https://dx.doi.org/10.1371/journal.pone.0074132.s002", "https://dx.doi.org/10.1371/journal.pone.0074132.s003", "https://dx.doi.org/10.1371/journal.pone.0074132.s004", "https://dx.doi.org/10.1371/journal.pone.0074132.s005", "https://dx.doi.org/10.1371/journal.pone.0074132.s006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Evolutionary_Genomics_and_Adaptive_Evolution_of_the_Hedgehog_Gene_Family_Shh_Ihh_and_Dhh_in_Vertebrates/1281684", "title"=>"Evolutionary Genomics and Adaptive Evolution of the Hedgehog Gene Family (<i>Shh, Ihh and Dhh</i>) in Vertebrates", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2014-12-30 02:59:22"}

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Relative Metric

{"start_date"=>"2014-01-01T00:00:00Z", "end_date"=>"2014-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Computational biology", "average_usage"=>[341, 529]}, {"subject_area"=>"/Biology and life sciences/Evolutionary biology", "average_usage"=>[333]}]}
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