Insights into the Evolution of the CSP Gene Family through the Integration of Evolutionary Analysis and Comparative Protein Modeling
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{"title"=>"Insights into the Evolution of the CSP Gene Family through the Integration of Evolutionary Analysis and Comparative Protein Modeling", "type"=>"journal", "authors"=>[{"first_name"=>"Jonna", "last_name"=>"Kulmuni", "scopus_author_id"=>"35603494500"}, {"first_name"=>"Heli", "last_name"=>"Havukainen", "scopus_author_id"=>"26530633900"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84878393035", "sgr"=>"84878393035", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0063688", "pmid"=>"23723994", "isbn"=>"1932-6203", "pui"=>"369024860"}, "id"=>"78cce6ea-f9f8-3de4-991e-164523c5cf03", "abstract"=>"Insect chemical communication and chemosensory systems rely on proteins coded by several gene families. Here, we have combined protein modeling with evolutionary analysis in order to study the evolution and structure of chemosensory proteins (CSPs) within arthropods and, more specifically, in ants by using the data available from sequenced genomes. Ants and other social insects are especially interesting model systems for the study of chemosensation, as they communicate in a highly complex social context and much of their communication relies on chemicals. Our ant protein models show how this complexity has shaped CSP evolution; the proteins are highly modifiable by their size, surface charge and binding pocket. Based on these findings, we divide ant CSPs into three groups: typical insect CSPs, an ancient 5-helical CSP and hymenopteran CSPs with a small binding pocket, and suggest that these groups likely serve different functions. The hymenopteran CSPs have duplicated repeatedly in individual ant lineages. In these CSPs, positive selection has driven surface charge changes, an observation which has possible implications for the interaction between CSPs and ligands or odorant receptors. Our phylogenetic analysis shows that within the Arthropoda the only highly conserved gene is the ancient 5-helical CSP, which is likely involved in an essential ubiquitous function rather than chemosensation. During insect evolution, the 6-helical CSPs have diverged and perform chemosensory functions among others. Our results contribute to the general knowledge of the structural differences between proteins underlying chemosensation and highlight those protein properties which have been affected by adaptive evolution.", "link"=>"http://www.mendeley.com/research/insights-evolution-csp-gene-family-through-integration-evolutionary-analysis-comparative-protein-mod", "reader_count"=>30, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>4, "Other"=>1, "Student > Bachelor"=>1, "Unspecified"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>8, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>4, "Other"=>1, "Student > Bachelor"=>1, "Unspecified"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>2, "Agricultural and Biological Sciences"=>24, "Neuroscience"=>1, "Computer Science"=>1}, "reader_count_by_subdiscipline"=>{"Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>24}, "Computer Science"=>{"Computer Science"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>2}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"Chile"=>1}, "group_count"=>0}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1068764", "https://ndownloader.figshare.com/files/1068765", "https://ndownloader.figshare.com/files/1068766", "https://ndownloader.figshare.com/files/1068767"], "description"=>"<div><p>Insect chemical communication and chemosensory systems rely on proteins coded by several gene families. Here, we have combined protein modeling with evolutionary analysis in order to study the evolution and structure of chemosensory proteins (CSPs) within arthropods and, more specifically, in ants by using the data available from sequenced genomes. Ants and other social insects are especially interesting model systems for the study of chemosensation, as they communicate in a highly complex social context and much of their communication relies on chemicals. Our ant protein models show how this complexity has shaped CSP evolution; the proteins are highly modifiable by their size, surface charge and binding pocket. Based on these findings, we divide ant CSPs into three groups: typical insect CSPs, an ancient 5-helical CSP and hymenopteran CSPs with a small binding pocket, and suggest that these groups likely serve different functions. The hymenopteran CSPs have duplicated repeatedly in individual ant lineages. In these CSPs, positive selection has driven surface charge changes, an observation which has possible implications for the interaction between CSPs and ligands or odorant receptors. Our phylogenetic analysis shows that within the Arthropoda the only highly conserved gene is the ancient 5-helical CSP, which is likely involved in an essential ubiquitous function rather than chemosensation. During insect evolution, the 6-helical CSPs have diverged and perform chemosensory functions among others. Our results contribute to the general knowledge of the structural differences between proteins underlying chemosensation and highlight those protein properties which have been affected by adaptive evolution.</p></div>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "csp", "evolutionary", "comparative"], "article_id"=>707674, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0063688.s001", "https://dx.doi.org/10.1371/journal.pone.0063688.s002", "https://dx.doi.org/10.1371/journal.pone.0063688.s003", "https://dx.doi.org/10.1371/journal.pone.0063688.s004"], "stats"=>{"downloads"=>3, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Insights_into_the_Evolution_of_the_CSP_Gene_Family_through_the_Integration_of_Evolutionary_Analysis_and_Comparative_Protein_Modeling_/707674", "title"=>"Insights into the Evolution of the CSP Gene Family through the Integration of Evolutionary Analysis and Comparative Protein Modeling", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-05-28 02:07:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/1068759"], "description"=>"<p>(A) Left, molecular model of CSP7 shows a “crown” of charged residues (circled). The crown is formed by the positive loop between helices 3 and 4, and by the negative charge between helices 5 and 6. The ant-specific proteins (right) all have this crown. Positively charged residues (K, R) are shown in blue and negatively charged (D, E) in red. (B) The ten residues under positive selection (shown as sticks on the peptide backbone) mostly map on the surface. L87 and L91 are the only binding residues under positive selection. K58 and A66 are located near the “crown” and have various combinations of positive charge and hydrophobicity in the ant-specific CSPs. The N and C termini are indicated.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "csps", "similarities", "concentrated"], "article_id"=>707669, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063688.g003", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Ant_specific_CSPs_share_similarities_with_CSP7_and_positive_selection_in_them_is_concentrated_on_the_surface_/707669", "title"=>"Ant-specific CSPs share similarities with CSP7, and positive selection in them is concentrated on the surface.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-28 02:07:49"}
  • {"files"=>["https://ndownloader.figshare.com/files/1068758"], "description"=>"<p>The N-terminus is indicated. The 34 binding-residues are shown as sticks. Certain binding-residues of interest are indicated in each CSP. (A) Residues within 5 Å of the ligands in the ligand-bound <i>M. brassicae</i> structure (PDB-ID: 1N8V) were considered as binding-residues. The bromo-dodecanol ligands are visualized inside the pocket. (B) The model of CSP1 shown here represents a binding pocket of a non-ligand bound typical CSP protein. (C) The binding pocket of CSP5 is likely enlarged due to the lack of helix 6 and mutations that reduce the size of the binding-residues (A44, Q54, A58 V67 and V36). (D) The binding pocket of CSP7 model is crowded by large binding-residues. For example, F50 and W28 are larger than the corresponding amino acid residues in other, typical CSPs.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "csp", "binding", "pockets", "ligand"], "article_id"=>707668, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063688.g002", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differences_in_the_size_of_the_CSP_binding_pockets_can_reflect_ligand_differences_/707668", "title"=>"Differences in the size of the CSP binding pockets can reflect ligand differences.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-28 02:07:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/1068763"], "description"=>"<p>CSP1 and CSP5 have a strictly conserved charge-profile, whereas CSP3, CSP6 and CSP7 show great charge heterogeneity between the ant species. The amino acid (aa) residues with >20% solvent accessible area in the CSP homology models were considered surface residues. The number of positively and negatively charged amino acid residues on the surface of the CSP structure chosen for modeling is shown (represents a single species). The last column shows the number of residues with charge changes in the solvent-exposed residues in all the seven species of ants basing on a sequence alignment.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "orthologous", "ant", "csps"], "article_id"=>707673, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063688.t001", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Surface_charge_variation_in_orthologous_ant_CSPs_between_the_seven_ant_species_/707673", "title"=>"Surface charge variation in orthologous ant CSPs between the seven ant species.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-28 02:07:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/1068761"], "description"=>"<p>The residue numbering is according to AcepCSP8. The average solvent accessible area (with standard deviation) was calculated for the seven modeled ant-specific CSPs, and is indicated for each positively selected residue. Binding residues correspond to the residues at 5 Å distance from the ligands in MbraCSPA6 structure. The amino acid variation for each positively selected residue is shown in the last column, where all the ant-specific proteins of the seven species were taken into account. All solvent accessible positively selected amino acid residues show charge variation that can potentially modify the proteins’ electrochemical surface interactions.</p><p><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0063688#pone.0063688.s003\" target=\"_blank\">Dataset S2</a> Alignment used in homology modeling and phylogeny reconstruction.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "amino", "residues"], "article_id"=>707671, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063688.t003", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Chemical_characteristics_of_the_ten_amino_acid_residues_under_positive_selection_/707671", "title"=>"Chemical characteristics of the ten amino acid residues under positive selection.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-28 02:07:51"}
  • {"files"=>["https://ndownloader.figshare.com/files/1068762"], "description"=>"<p>Twentynine non-cysteine binding-residues were divided based on their size into small (S,T,C,G,P,A, V) intermediate (H,D,E,N,Q,I,L,M) and large (R, K, F, Y,W) for each CSP in the seven ant species. The binding-residues located in helix-6 were left out due to the lack of helix-6 in CSP5.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "binding"], "article_id"=>707672, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063688.t002", "stats"=>{"downloads"=>1, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Size_distribution_of_the_binding_pocket_residues_/707672", "title"=>"Size distribution of the binding pocket residues.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-05-28 02:07:52"}
  • {"files"=>["https://ndownloader.figshare.com/files/1068760"], "description"=>"<p>Maximum likelihood tree constructed from representative arthropod CSP protein sequences. Species are referred to in three letter codes. Confidence values (1000 bootstraps) are indicated. Different CSP groups are highlighted in different colors. Typical CSPs are highlighted in green and CSPs with smaller binding pocket in purple. All 5-helical CSPs in arthropods form a single clade which is highlighted in grey. The ant-specific expansion is highlighted in yellow.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "csp"], "article_id"=>707670, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063688.g004", "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Arthropod_CSP_phylogeny_/707670", "title"=>"Arthropod CSP phylogeny.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-28 02:07:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/1068756"], "description"=>"<p>All ants share seven orthologous CSPs (CSP1-7; the uppermost row of models), of which CSP7 or a protein similar to that has given rise to the ant-specific expansions (representative proteins on the middle row). The largest currently known ant-expansion is found in <i>S. invicta</i> (the lowest row). In the orthologs, CSP1-4 can be grouped together based on their evenly speckled surface charges and similarities in their binding pocket (“Typical CSPs”; green). CSP5 (grey) is conserved across arthropods, and is one of the oldest CSPs. It differs from the other orthologs by having five instead of six helices, a reduced charge on the surface and by changes to its binding pocket. CSP6 and CSP7 are grouped together (purple) due to mutations in their binding pocket that are likely to reduce the size of the pocket cavity. Examples of the ant-specific CSP expansion are shown; <i>Atta cephalotes</i> CSP8, <i>Pogonomyrmex barbatus</i> CSP10, <i>Camponotus floridanus</i> CSP11, <i>Acromyrmex echinatior</i> CSP14 and <i>Solenopsis invicta</i> CSP17. In the models, negatively charged amino acids (E, D) are shown in red and positively charged amino acids (K, R) in blue. C-termini are marked by an arrow. The <i>S. invicta</i> expansion proteins, together with CSP5, are one helix shorter than the other CSPs in their C-terminus, which is depicted by the altered location of the arrow in these models.</p>", "links"=>[], "tags"=>["Biochemistry", "proteins", "protein structure", "Computational biology", "Macromolecular structure analysis", "Sequence analysis", "Evolutionary biology", "Evolutionary processes", "adaptation", "natural selection", "Comparative genomics", "Evolutionary genetics", "ant", "csps", "phylogeny"], "article_id"=>707667, "categories"=>["Biological Sciences"], "users"=>["Jonna Kulmuni", "Heli Havukainen"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0063688.g001", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Groups_of_ant_CSPs_based_on_their_phylogeny_and_structural_models_/707667", "title"=>"Groups of ant CSPs based on their phylogeny and structural models.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-05-28 02:07:47"}

PMC Usage Stats | Further Information

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Organisms", "average_usage"=>[281, 484, 611, 728, 835, 934, 1030, 1123, 1214, 1299, 1383, 1464]}, {"subject_area"=>"/Biology and life sciences/Zoology", "average_usage"=>[294, 473, 591, 693, 788, 883, 972, 1054, 1140, 1222, 1299, 1381, 1446]}, {"subject_area"=>"/Computer and information sciences/Data management", "average_usage"=>[301, 521, 654, 776, 898, 1028, 1133, 1258, 1373, 1457, 1542, 1648, 1738]}]}
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