Sex Pheromone Evolution Is Associated with Differential Regulation of the Same Desaturase Gene in Two Genera of Leafroller Moths
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{"title"=>"Sex pheromone evolution is associated with differential regulation of the same desaturase gene in two genera of leafroller moths", "type"=>"journal", "authors"=>[{"first_name"=>"Jérôme", "last_name"=>"Albre", "scopus_author_id"=>"6506339640"}, {"first_name"=>"Marjorie A.", "last_name"=>"Liénard", "scopus_author_id"=>"13608875500"}, {"first_name"=>"Tamara M.", "last_name"=>"Sirey", "scopus_author_id"=>"6508218985"}, {"first_name"=>"Silvia", "last_name"=>"Schmidt", "scopus_author_id"=>"57198523436"}, {"first_name"=>"Leah K.", "last_name"=>"Tooman", "scopus_author_id"=>"47161726200"}, {"first_name"=>"Colm", "last_name"=>"Carraher", "scopus_author_id"=>"24398444800"}, {"first_name"=>"David R.", "last_name"=>"Greenwood", "scopus_author_id"=>"35233357400"}, {"first_name"=>"Christer", "last_name"=>"Löfstedt", "scopus_author_id"=>"7003385545"}, {"first_name"=>"Richard D.", "last_name"=>"Newcomb", "scopus_author_id"=>"7103019398"}], "year"=>2012, "source"=>"PLoS Genetics", "identifiers"=>{"pui"=>"364329937", "sgr"=>"84857495692", "issn"=>"15537390", "pmid"=>"22291612", "scopus"=>"2-s2.0-84857495692", "doi"=>"10.1371/journal.pgen.1002489", "isbn"=>"1553-7404"}, "id"=>"3e07ece3-1038-313a-95c5-f2f279cd01e5", "abstract"=>"Chemical signals are prevalent in sexual communication systems. Mate recognition has been extensively studied within the Lepidoptera, where the production and recognition of species-specific sex pheromone signals are typically the defining character. While the specific blend of compounds that makes up the sex pheromones of many species has been characterized, the molecular mechanisms underpinning the evolution of pheromone-based mate recognition systems remain largely unknown. We have focused on two sets of sibling species within the leafroller moth genera Ctenopseustis and Planotortrix that have rapidly evolved the use of distinct sex pheromone blends. The compounds within these blends differ almost exclusively in the relative position of double bonds that are introduced by desaturase enzymes. Of the six desaturase orthologs isolated from all four species, functional analyses in yeast and gene expression in pheromone glands implicate three in pheromone biosynthesis, two Δ9-desaturases, and a Δ10-desaturase, while the remaining three desaturases include a Δ6-desaturase, a terminal desaturase, and a non-functional desaturase. Comparative quantitative real-time PCR reveals that the Δ10-desaturase is differentially expressed in the pheromone glands of the two sets of sibling species, consistent with differences in the pheromone blend in both species pairs. In the pheromone glands of species that utilize (Z)-8-tetradecenyl acetate as sex pheromone component (Ctenopseustis obliquana and Planotortrix octo), the expression levels of the Δ10-desaturase are significantly higher than in the pheromone glands of their respective sibling species (C. herana and P. excessana). Our results demonstrate that interspecific sex pheromone differences are associated with differential regulation of the same desaturase gene in two genera of moths. We suggest that differential gene regulation among members of a multigene family may be an important mechanism of molecular innovation in sex pheromone evolution and speciation.", "link"=>"http://www.mendeley.com/research/sex-pheromone-evolution-associated-differential-regulation-same-desaturase-gene-two-genera-leafrolle", "reader_count"=>37, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>4, "Researcher"=>7, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>3, "Student > Doctoral Student"=>4, "Researcher"=>7, "Student > Ph. D. Student"=>11, "Student > Postgraduate"=>2, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>2, "Lecturer"=>1, "Professor"=>3}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Environmental Science"=>1, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>30, "Chemistry"=>2}, "reader_count_by_subdiscipline"=>{"Chemistry"=>{"Chemistry"=>2}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>30}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>1}, "Environmental Science"=>{"Environmental Science"=>1}}, "reader_count_by_country"=>{"Netherlands"=>1, "Hungary"=>1, "United States"=>1, "Japan"=>1, "Germany"=>1}, "group_count"=>1}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/350643", "https://ndownloader.figshare.com/files/350709", "https://ndownloader.figshare.com/files/350751", "https://ndownloader.figshare.com/files/350794", "https://ndownloader.figshare.com/files/350823", "https://ndownloader.figshare.com/files/350854", "https://ndownloader.figshare.com/files/350887", "https://ndownloader.figshare.com/files/350927", "https://ndownloader.figshare.com/files/350971"], "description"=>"<div><p>Chemical signals are prevalent in sexual communication systems. Mate recognition has been extensively studied within the Lepidoptera, where the production and recognition of species-specific sex pheromone signals are typically the defining character. While the specific blend of compounds that makes up the sex pheromones of many species has been characterized, the molecular mechanisms underpinning the evolution of pheromone-based mate recognition systems remain largely unknown. We have focused on two sets of sibling species within the leafroller moth genera <em>Ctenopseustis</em> and <em>Planotortrix</em> that have rapidly evolved the use of distinct sex pheromone blends. The compounds within these blends differ almost exclusively in the relative position of double bonds that are introduced by desaturase enzymes. Of the six desaturase orthologs isolated from all four species, functional analyses in yeast and gene expression in pheromone glands implicate three in pheromone biosynthesis, two Δ9-desaturases, and a Δ10-desaturase, while the remaining three desaturases include a Δ6-desaturase, a terminal desaturase, and a non-functional desaturase. Comparative quantitative real-time PCR reveals that the Δ10-desaturase is differentially expressed in the pheromone glands of the two sets of sibling species, consistent with differences in the pheromone blend in both species pairs. In the pheromone glands of species that utilize (<em>Z</em>)-8-tetradecenyl acetate as sex pheromone component (<em>Ctenopseustis obliquana</em> and <em>Planotortrix octo</em>), the expression levels of the Δ10-desaturase are significantly higher than in the pheromone glands of their respective sibling species (<em>C. herana</em> and <em>P. excessana</em>). Our results demonstrate that interspecific sex pheromone differences are associated with differential regulation of the same desaturase gene in two genera of moths. We suggest that differential gene regulation among members of a multigene family may be an important mechanism of molecular innovation in sex pheromone evolution and speciation.</p> </div>", "links"=>[], "tags"=>["pheromone", "differential", "desaturase", "genera", "leafroller", "moths"], "article_id"=>129310, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>[nil, nil, nil, nil, nil, nil, nil, nil, nil], "stats"=>{"downloads"=>83, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Sex_Pheromone_Evolution_Is_Associated_with_Differential_Regulation_of_the_Same_Desaturase_Gene_in_Two_Genera_of_Leafroller_Moths/129310", "title"=>"Sex Pheromone Evolution Is Associated with Differential Regulation of the Same Desaturase Gene in Two Genera of Leafroller Moths", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-01-26 02:35:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/688255"], "description"=>"<p>The phylogeny was constructed from protein sequences using PHYML implemented within Geneious using JTT distances. Complete amino acid sequence information was obtained from GenBank, along with desaturases predicted from the genomic sequence of <i>Bombyx mori</i> from the Silkmoth database. Sequences are abbreviated as following: Ape, <i>Antherea pernyi</i>; Ase, <i>Ascotis selenaria</i>; Ave, <i>Argyrotaenia velutinana</i>; Bmo, <i>Bombyx mori</i>; Cpa, <i>Choristoneura parallela</i>; Cro, <i>Choristoneura rosaceana</i>; Che, <i>Ctenopseustis herana</i>; Cob, <i>Ctenopseustis obliquana</i>; Cpo, <i>Cydia pomonella</i>; Epo, <i>Epiphyas postvittana</i>; Has, <i>Helicoverpa assulta</i>; Hze, <i>Helicoverpa zea</i>; Lca, <i>Lampronia capitella</i>; Mbr, <i>Mamestra brassicae</i>; Mse, <i>Manduca sexta</i>; Pex, <i>Planotortrix excessana</i>; Poc, <i>Planotortrix octo</i>; Pno, <i>Planotortrix notophaea</i>; Onu, <i>Ostrinia nubilalis</i>; Ofu, <i>Ostrinia furnacalis</i>; Osc, <i>Ostrinia scapulalis</i>: Obr, <i>Operophtera brumata</i>; Sli, <i>Spodoptera littoralis</i>; Tni, <i>Trichoplusia ni</i>; Tpi, <i>Thaumetopoea pityocampa</i>; Ypa: <i>Yponomeuta padellus</i>. After the abbreviated species name are the desaturase activity if known with NF  =  non-functional in pheromone biosynthesis; TerDesat  =  terminal desaturase activity; Z or E, geometry of the double bond. The GenBank accession numbers are given in brackets for previously described desaturases. Bootstrap values in percentages from 1000 bootstrap replicates supporting the three major clades (Δ9-desaturase 16C&gt;18C, Δ9-desaturase 18C&gt;16C, and Δ11-desaturase) and the groups containing the <i>Ctenopseustis</i> and <i>Planotortrix</i> desaturases, indicated by the red outline boxes, are given above the relevant branches.</p>", "links"=>[], "tags"=>["86", "lepidopteran", "desaturases", "encoded"], "article_id"=>358732, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.g002", "stats"=>{"downloads"=>1, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Phylogeny_of_86_lepidopteran_desaturases_including_those_encoded_by_i_desat1_6_i_from_i_Ctenopseustis_i_and_i_Planotortrix_i_/358732", "title"=>"Phylogeny of 86 lepidopteran desaturases including those encoded by <i>desat1-6</i> from <i>Ctenopseustis</i> and <i>Planotortrix</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:25:32"}
  • {"files"=>["https://ndownloader.figshare.com/files/688590"], "description"=>"<p>In panel (A) the normalised expression levels in the pheromone gland [PG] of <i>C. herana</i> (Che; light brown; n = 20) and <i>C. obliquana</i> (Cob; dark brown; n = 21) was compared with those in the abdomen [Ab] of <i>C. herana</i> (n = 20) and <i>C. obliquana</i> (n = 21), while in panel (B) the normalised expression levels in the pheromone gland of <i>P. excessana</i> (Pex; light green; n = 39) and <i>P. octo</i> (Poc; dark green; n = 24) are compared with those in the abdomen of <i>P. excessana</i> (n = 39) and <i>P. octo</i> (n = 25). Bars are the mean normalized gene expression, with error bars representing SEMs. Different small case letters indicate significant differences between tissues and/or species at the 95% level using the Bonferroni correction for each desaturase gene.</p>", "links"=>[], "tags"=>["pheromone", "gland", "abdomen", "virgin", "females", "housekeeper"], "article_id"=>359066, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.g005", "stats"=>{"downloads"=>1, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Gene_expression_of_i_desat1_i_i_desat5_i_and_i_desat6_i_in_the_pheromone_gland_and_abdomen_of_virgin_females_in_i_Ctenopseustis_obliquana_i_i_C_herana_i_i_P_excessana_i_and_i_P_octo_i_relative_to_housekeeper_genes_/359066", "title"=>"Gene expression of <i>desat1</i>, <i>desat5</i>, and <i>desat6</i> in the pheromone gland and abdomen of virgin females in <i>Ctenopseustis obliquana</i>, <i>C. herana</i>, <i>P. excessana</i>, and <i>P. octo</i> relative to housekeeper genes.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:31:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/688658"], "description"=>"a<p>number of sequences.</p>b<p>number of codons.</p>c<p>tree length.</p>d<p>transition/transversion ratio.</p>e<p>ω under M0.</p>f<p>ω under M3.</p>", "links"=>[], "tags"=>["desaturases"], "article_id"=>359144, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.t001", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Summary_statistics_for_desaturases_from_i_Ctenopseustis_i_and_i_Planotortrix_i_species_/359144", "title"=>"Summary statistics for desaturases from <i>Ctenopseustis</i> and <i>Planotortrix</i> species.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-01-26 02:32:24"}
  • {"files"=>["https://ndownloader.figshare.com/files/688091"], "description"=>"<p><i>Desat1</i>, <i>desat5</i> and <i>desat6</i> correspond to the desaturase genes encoding a Δ9 desaturase with a preference for 16&gt;18 carbon fatty acids, a Δ10-desaturase and a Δ9-desaturase with a preference for 18&gt;16 carbon fatty acids, respectively. <i>Desat?</i> refers to a yet to be identified Δ5-desaturase. Chain shortening by β-oxidation is indicated by ‘−2C’. The minor products of the two Δ9-desaturases in <i>P. excessana</i> (<i>desat1</i> and <i>desat6</i>) are indicated in brackets. We also note that Z10-14:OAc is a very minor (2%) component of the pheromone blend of <i>P. octo</i> (not shown).</p>", "links"=>[], "tags"=>["outlining", "biosynthetic", "routes", "pheromone", "components"], "article_id"=>358574, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Schematic_outlining_the_likely_biosynthetic_routes_of_the_sex_pheromone_components_of_i_C_obliquana_i_i_C_herana_i_i_P_octo_i_and_i_P_excessana_i_/358574", "title"=>"Schematic outlining the likely biosynthetic routes of the sex pheromone components of <i>C. obliquana</i>, <i>C. herana</i>, <i>P. octo</i>, and <i>P. excessana</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:22:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/688700"], "description"=>"a<p>Twice the difference of log likelihood between the two models (χ<sup>2</sup>)  =  probability that two models should differ in log likelihood, as much as that observed, given the degree of freedom. Degrees of freedom are equal to the difference in the number of parameters between models; M0 v. M3  =  4, M7 v. M8  = 2, M8a v. M8  = 2, M8a v. M8  = 1. M8a v. M8 comparison significance is determined by a <i>P</i>-value for the 50∶50 mixture of distributions.</p>", "links"=>[], "tags"=>["nested", "site-specific"], "article_id"=>359185, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.t002", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Likelihood_ratio_tests_between_nested_site_specific_models_sup_a_sup_/359185", "title"=>"Likelihood ratio tests between nested site-specific models.<sup>a</sup>", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-01-26 02:33:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/688504"], "description"=>"<p>GC-MS analysis of methanolysed total lipid extracts from <i>ole1 S. cerevisiae</i> yeast transformed with YEpOLEX-Cob-desat6. (A) Total ion current (TIC) chromatogram of fatty acid methyl esters of yeast expressing the Cob-desat6 gene. (B) DMDS derivatives of methanolyzed YEpOLEX-Cob-desat6 yeast extracts. The chromatogram traces represent the ion current obtained by selection of the characteristic ion of Δ9-adducts at <i>m/z</i> 217.</p>", "links"=>[], "tags"=>["Evolutionary biology"], "article_id"=>358990, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.g004", "stats"=>{"downloads"=>1, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/GC_MS_analysis_/358990", "title"=>"GC-MS analysis.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:29:50"}
  • {"files"=>["https://ndownloader.figshare.com/files/688728"], "description"=>"<p>Putative positively selected sites and posterior probabilities under M8.</p>", "links"=>[], "tags"=>["positively", "sites", "posterior", "probabilities"], "article_id"=>359214, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.t003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Putative_positively_selected_sites_and_posterior_probabilities_under_M8_/359214", "title"=>"Putative positively selected sites and posterior probabilities under M8.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2012-01-26 02:33:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/688389"], "description"=>"<p>GC-MS analyses of DMDS derivatives from methanolysed Cu<sup>2+</sup>-induced <i>ole1 elo1 S. cerevisiae</i> yeast supplemented with Z9-18:Me and transformed with (A and C) control pYEX-CHT vector, (B) pYEX-CHT-Pex-desat3 and (D) pYEX-CHT-Che-desat4. The chromatogram traces represent the ion currents obtained by selection of the characteristic ion of terminal and Δ6-DMDS adducts at <i>m/z</i> 61 (A and B) and <i>m/z</i> 175 (C and D), respectively. (E) and (F) represent the mass spectra for terminal C16 DMDS adducts (Δ15-16) (<i>m/z</i> 362 [M<sup>+</sup>], 61, 301 (A<sup>+</sup>) and 269 (A<sup>+</sup>-32)) and Δ6-16 DMDS adducts (<i>m/z</i> 362 [M<sup>+</sup>], 187, 175 (A+) and 143 (A<sup>+</sup>-32), respectively. The mass spectra for other DMDS adducts present in the extracts are not shown and displayed a spectrum with the characteristic ions at <i>m/z</i> 334 [M<sup>+</sup>], 61 and 273 for Δ13-14, at <i>m/z</i> 390 [M<sup>+</sup>], 61 and 329 for Δ17-18 and at <i>m/z</i> 334 [M<sup>+</sup>], 175 and 159 for Δ6-14, respectively.</p>", "links"=>[], "tags"=>["Evolutionary biology"], "article_id"=>358873, "categories"=>["Evolutionary Biology"], "users"=>["Jérôme Albre", "Marjorie A. Liénard", "Tamara M. Sirey", "Silvia Schmidt", "Leah K. Tooman", "Colm Carraher", "David R. Greenwood", "Christer Löfstedt", "Richard D. Newcomb"], "doi"=>"https://dx.doi.org/10.1371/journal.pgen.1002489.g003", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/GC_MS_analyses_/358873", "title"=>"GC-MS analyses.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-26 02:27:53"}

PMC Usage Stats | Further Information

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Relative Metric

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