Adaptive Evolution of the Venom-Targeted vWF Protein in Opossums that Eat Pitvipers
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{"title"=>"Adaptive evolution of the Venom-targeted vWF protein in opossums that Eat Pitvipers", "type"=>"journal", "authors"=>[{"first_name"=>"Sharon A.", "last_name"=>"Jansa", "scopus_author_id"=>"6602461706"}, {"first_name"=>"Robert S.", "last_name"=>"Voss", "scopus_author_id"=>"7101728261"}], "year"=>2011, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "scopus"=>"2-s2.0-79959451069", "sgr"=>"79959451069", "pui"=>"361997144", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"21731638", "doi"=>"10.1371/journal.pone.0020997"}, "id"=>"e4a9f78d-0fd5-3158-91f9-4c9c22818aca", "abstract"=>"The rapid evolution of venom toxin genes is often explained as the result of a biochemical arms race between venomous animals and their prey. However, it is not clear that an arms race analogy is appropriate in this context because there is no published evidence for rapid evolution in genes that might confer toxin resistance among routinely envenomed species. Here we report such evidence from an unusual predator-prey relationship between opossums (Marsupialia: Didelphidae) and pitvipers (Serpentes: Crotalinae). In particular, we found high ratios of replacement to silent substitutions in the gene encoding von Willebrand Factor (vWF), a venom-targeted hemostatic blood protein, in a clade of opossums known to eat pitvipers and to be resistant to their hemorrhagic venom. Observed amino-acid substitutions in venom-resistant opossums include changes in net charge and hydrophobicity that are hypothesized to weaken the bond between vWF and one of its toxic snake-venom ligands, the C-type lectin-like protein botrocetin. Our results provide the first example of rapid adaptive evolution in any venom-targeted molecule, and they support the notion that an evolutionary arms race might be driving the rapid evolution of snake venoms. However, in the arms race implied by our results, venomous snakes are prey, and their venom has a correspondingly defensive function in addition to its usual trophic role.", "link"=>"http://www.mendeley.com/research/adaptive-evolution-venomtargeted-vwf-protein-opossums-eat-pitvipers", "reader_count"=>89, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>16, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>5, "Other"=>4, "Student > Master"=>8, "Student > Bachelor"=>11, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>6, "Researcher"=>16, "Student > Doctoral Student"=>8, "Student > Ph. D. Student"=>25, "Student > Postgraduate"=>5, "Other"=>4, "Student > Master"=>8, "Student > Bachelor"=>11, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>5, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>67, "Medicine and Dentistry"=>3, "Neuroscience"=>1, "Pharmacology, Toxicology and Pharmaceutical Science"=>1, "Physics and Astronomy"=>1, "Earth and Planetary Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Neuroscience"=>{"Neuroscience"=>1}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>67}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>5}, "Environmental Science"=>{"Environmental Science"=>2}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Canada"=>2, "United States"=>7, "Philippines"=>1, "Sudan"=>1, "Brazil"=>1, "United Kingdom"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/763329"], "description"=>"<p>Parameter estimates for branch-site tests (H<sub>0</sub>: <sub>2</sub> = 1; H<sub>A</sub>: <sub>2</sub>>1) applied to vWF sequences with either the clade Didelphini ( = −5436.01;  = −5422.79) or Didelphini excluding <i>Chironectes</i> ( = −5440.51;  = −5431.74; parameter values in parentheses) designated as foreground lineages.</p>1<p>Site classes 0 and 1 comprise sites under purifying selection (0<<sub>0</sub><1) and neutral sites (<sub>1</sub> = 1), respectively in both foreground and background lineages. Site class 2 allows a proportion of positively selected sites in the foreground lineages, where 2a includes sites under purifying selection (0<<sub>0</sub><1) in the background lineages, 2b includes neutral sites in the background lineages. Both 2a and 2b allow a proportion of sites in the foreground lineages to be under positive selection (<sub>2</sub>>1).</p>", "links"=>[], "tags"=>["branch-site"], "article_id"=>433714, "categories"=>["Biochemistry", "Hematology", "Evolutionary Biology"], "users"=>["Sharon A. Jansa", "Robert S. Voss"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020997.t001", "stats"=>{"downloads"=>5, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_branch_site_tests_for_selection_on_vWF_/433714", "title"=>"Results of branch-site tests for selection on vWF.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 17:21:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/763362"], "description"=>"<p>Sites in vWF that were identified as being under positive selection (>1) with posterior probability >0.50 in Bayes-Emipircal-Bayes analyses with Didelphini (either excluding or including <i>Chironectes</i>) assigned as foreground lineages.</p>1<p>Numbered according to the mature vWF peptide in <i>Mus</i>.</p>2<p>Sites inferred to be under positive selection with <i>P</i>≥0.95 are shown in bold.</p>3<p>Positively selected sites corresponding to those involved in botrocetin binding in <i>Mus</i> are indicated. An additional five sites (Arg629, Arg632, Lys660, Gln661, Lys667) bind botrocetin in <i>Mus</i> but are not inferred to be positively selected in any of our analyses of opossum vWF sequences.</p>", "links"=>[], "tags"=>["bayes-empirical-bayes", "analyses", "positively"], "article_id"=>433734, "categories"=>["Biochemistry", "Hematology", "Evolutionary Biology"], "users"=>["Sharon A. Jansa", "Robert S. Voss"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020997.t002", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Results_of_Bayes_Empirical_Bayes_analyses_identifying_positively_selected_sites_/433734", "title"=>"Results of Bayes-Empirical-Bayes analyses identifying positively selected sites.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2013-02-20 17:21:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/763130"], "description"=>"<p>A. The structure of the mouse vWF A1 domain complexed with botrocetin (Protein Data Bank file 1U0O <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020997#pone.0020997-Fukuda2\" target=\"_blank\">[47]</a>; image realized using Geneious v.5.0.3 <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020997#pone.0020997-Drummond1\" target=\"_blank\">[78]</a>). The two chains of botrocetin are shown as a dark grey trace model. The vWF A1 domain is shown as a light grey spacefill model, with residues that are involved in botrocetin binding shown in color (yellow, red, or blue). Amino acid residues identified as being under positive selection in the lineage of venom-resistant opossums (Didelphini) are shown in red (<i>P</i>≥0.95) or yellow (0.5<<i>P</i><0.95). Residues that are colored blue are involved in botrocetin binding but are not inferred to be under positive selection in opossums. <b>B</b>. Box plots of the absolute value of change in amino acid charge (top) and hydrophobicity (bottom) between venom-resistant and non-resistant taxa for sites of the vWF-A1 domain that bind botrocetin and those that do not. <b>C</b>. A site-by-site sliding window analysis along the vWF-A1 domain showing the average change in charge (solid line) and hydrophobicity (dashed line) between resistant and non-resistant taxa. Botrocetin-binding sites are indicated with pale grey bars, sites that bind platelet glycoprotein Ibα are dark grey, and sites that are under positive selection in venom-resistant opossums are indicated with red asterisks.</p>", "links"=>[], "tags"=>["analyses", "vwf-a1"], "article_id"=>433510, "categories"=>["Biochemistry", "Hematology", "Evolutionary Biology"], "users"=>["Sharon A. Jansa", "Robert S. Voss"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020997.g003", "stats"=>{"downloads"=>2, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structure_and_functional_analyses_of_the_vWF_A1_domain_/433510", "title"=>"Structure and functional analyses of the vWF-A1 domain.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 17:20:08"}
  • {"files"=>["https://ndownloader.figshare.com/files/763031"], "description"=>"<p>Schematic showing the structure of the mature vWF protein and its constituent domains (A, B, C, D, and CK; modified from <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020997#pone.0020997-Sadler1\" target=\"_blank\">[39]</a>). Amino-acid residues are numbered 1–2050 corresponding to the human vWF sequence, with the A1 domain spanning residues 478–728. The region sequenced from opossums for this study includes part of the A1 and A2 domains and spans residues 524–843 (indicated with a grey box). The botrocetin-binding region (indicated with a black box) is located in the A1 domain and spans residues 623–671. Aligned amino-acid sequences of this region are shown for five placental taxa (<i>Homo</i>, <i>Mus</i>, <i>Canis</i>, <i>Talpa</i>, and <i>Dugong</i>) as well as members of the opossum tribe Didelphini (including species of <i>Didelphis</i>, <i>Philander</i>, <i>Lutreolina</i>, and <i>Chironectes</i>) and its sister taxon Metachirini (<i>Metachirus nudicaudatus</i>). Amino acids that are identical to vWF sequence from <i>Homo</i> are shaded in grey. The 12 amino-acid residues (positions 628, 629, 632, 635, 636, 639, 643, 660, 661, 664, 667, and 668) identified as critical for botrocetin binding in <i>Mus </i><a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020997#pone.0020997-Fukuda2\" target=\"_blank\">[47]</a> are indicated with red dots below the sequences.</p>", "links"=>[], "tags"=>["vwf", "botrocetin-binding"], "article_id"=>433403, "categories"=>["Biochemistry", "Hematology", "Evolutionary Biology"], "users"=>["Sharon A. Jansa", "Robert S. Voss"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020997.g002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Structure_of_vWF_showing_botrocetin_binding_sites_/433403", "title"=>"Structure of vWF showing botrocetin-binding sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 17:19:35"}
  • {"files"=>["https://ndownloader.figshare.com/files/763235"], "description"=>"<p>Plots of the absolute value of the average change in amino-acid charge (<b>a</b>) and hydrophobicity (<b>d</b>) between resistant and non-resistant taxa as a function of distance from a known botrocetin-binding site. Solid dots correspond to values at known botrocetin-binding sites; open circles indicate other sites in the A1 domain. For both physicochemical properties (charge, hydrophobicity), the magnitude of change is negatively correlated with distance from a known botrocetin-binding site. To test the significance of this correlation, we analyzed 1000 replicate datasets in which magnitude of change in each physicochemical property was randomized across the sequence. Histograms show the distribution of slope values for the best-fit regression lines through scatterplots of change in charge (<b>b</b>, <b>c</b>) or change in hydrophobicity (<b>e</b>, <b>f</b>) as a function of these randomly permuted distances. Permutations were performed with (<b>b</b>, <b>e</b>) and without (<b>c</b>, <b>f</b>) botrocetin-binding sites included. Dashed lines indicate the limits of the 95% confidence interval; solid lines correspond to the slope of the best-fit regression line based on the unpermuted data.</p>", "links"=>[], "tags"=>["amino-acid", "properties", "botrocetin-binding"], "article_id"=>433612, "categories"=>["Biochemistry", "Hematology", "Evolutionary Biology"], "users"=>["Sharon A. Jansa", "Robert S. Voss"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020997.g004", "stats"=>{"downloads"=>2, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Change_in_amino_acid_properties_as_a_function_of_distance_from_botrocetin_binding_sites_/433612", "title"=>"Change in amino-acid properties as a function of distance from botrocetin-binding sites.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 17:20:43"}
  • {"files"=>["https://ndownloader.figshare.com/files/762873"], "description"=>"<p><b>A</b>. The phylogeny of didelphids resulting from a mixed-model Bayesian analysis of a combined-data matrix comprising DNA sequences from five nuclear protein-coding genes and morphological data <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020997#pone.0020997-Voss1\" target=\"_blank\">[28]</a>. Nodes that received Bayesian posterior probability values ≥0.95 in this analysis are indicated with black circles. <b>B</b>. The topology from <b>A</b> excluding <i>Lestodelphys</i> and <i>Caluromysiops</i>, (for which no vWF sequences are available). Branch lengths are shown as the estimated number of amino acid substitutions in vWF, assuming the JTT model of amino acid substitution as implemented in PAML <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0020997#pone.0020997-Yang3\" target=\"_blank\">[74]</a>. Taxa that are known to eat pitvipers are indicated in bold; those that are known to exhibit resistance to pitviper venom are indicated with an asterisk. <i>Metachirus</i> (indicated with a dagger) has been challenged with pitviper venom but does not exhibit resistance. Branches that were included in the foreground for branch-site tests are shown with solid heavy lines. Venom resistance of <i>Chironectes</i> is unknown; therefore, this taxon was included in one set of branch-site tests and excluded from the other (indicated with a dashed heavy line). For the purpose of this analysis, <i>Didelphis marsupialis</i> includes its dubiously distinct sister taxon <i>D. aurita</i>.</p>", "links"=>[], "tags"=>["trees"], "article_id"=>433247, "categories"=>["Biochemistry", "Hematology", "Evolutionary Biology"], "users"=>["Sharon A. Jansa", "Robert S. Voss"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0020997.g001", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Phylogenetic_trees_of_opossums_/433247", "title"=>"Phylogenetic trees of opossums.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-02-20 17:18:40"}

PMC Usage Stats | Further Information

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Relative Metric

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