Novel family of terpene synthases evolved from trans-isoprenyl diphosphate synthases in a flea beetle
Identifieur interne : 000083 ( Pmc/Checkpoint ); précédent : 000082; suivant : 000084Novel family of terpene synthases evolved from trans-isoprenyl diphosphate synthases in a flea beetle
Auteurs : Franziska Beran [Allemagne] ; Peter Rahfeld [Allemagne] ; Katrin Luck [Allemagne] ; Raimund Nagel [Allemagne] ; Heiko Vogel [Allemagne] ; Natalie Wielsch [Allemagne] ; Sandra Irmisch [Allemagne] ; Srinivasan Ramasamy [Taïwan] ; Jonathan Gershenzon [Allemagne] ; David G. Heckel [Allemagne] ; Tobias G. Köllner [Allemagne]Source :
- Proceedings of the National Academy of Sciences of the United States of America [ 0027-8424 ] ; 2016.
Abstract
Whether insect sesquiterpenes are synthesized de novo, derived from plant precursors, or produced by symbionts is often unknown. We identified an evolutionarily novel terpene synthase gene family in the striped flea beetle, a notorious pest of
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DOI: 10.1073/pnas.1523468113
PubMed: 26936952
PubMed Central: 4801258
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Novel family of terpene synthases evolved from <italic>trans</italic>-isoprenyl diphosphate synthases in a flea beetle</title><author><name sortKey="Beran, Franziska" sort="Beran, Franziska" uniqKey="Beran F" first="Franziska" last="Beran">Franziska Beran</name><affiliation wicri:level="1"><nlm:aff id="aff1">Research Group Sequestration and Detoxification in Insects,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Rahfeld, Peter" sort="Rahfeld, Peter" uniqKey="Rahfeld P" first="Peter" last="Rahfeld">Peter Rahfeld</name><affiliation wicri:level="1"><nlm:aff id="aff2">Department of Bioorganic Chemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Luck, Katrin" sort="Luck, Katrin" uniqKey="Luck K" first="Katrin" last="Luck">Katrin Luck</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Nagel, Raimund" sort="Nagel, Raimund" uniqKey="Nagel R" first="Raimund" last="Nagel">Raimund Nagel</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Vogel, Heiko" sort="Vogel, Heiko" uniqKey="Vogel H" first="Heiko" last="Vogel">Heiko Vogel</name><affiliation wicri:level="1"><nlm:aff id="aff4">Department of Entomology,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wielsch, Natalie" sort="Wielsch, Natalie" uniqKey="Wielsch N" first="Natalie" last="Wielsch">Natalie Wielsch</name><affiliation wicri:level="1"><nlm:aff id="aff5">Department of Mass Spectrometry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Irmisch, Sandra" sort="Irmisch, Sandra" uniqKey="Irmisch S" first="Sandra" last="Irmisch">Sandra Irmisch</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Ramasamy, Srinivasan" sort="Ramasamy, Srinivasan" uniqKey="Ramasamy S" first="Srinivasan" last="Ramasamy">Srinivasan Ramasamy</name><affiliation wicri:level="1"><nlm:aff id="aff6">Entomology,<institution>AVRDC–The World Vegetable Center</institution>, Shanhua, Tainan 74151,<country>Taiwan</country></nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Gershenzon, Jonathan" sort="Gershenzon, Jonathan" uniqKey="Gershenzon J" first="Jonathan" last="Gershenzon">Jonathan Gershenzon</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Heckel, David G" sort="Heckel, David G" uniqKey="Heckel D" first="David G." last="Heckel">David G. Heckel</name><affiliation wicri:level="1"><nlm:aff id="aff4">Department of Entomology,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kollner, Tobias G" sort="Kollner, Tobias G" uniqKey="Kollner T" first="Tobias G." last="Köllner">Tobias G. Köllner</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26936952</idno><idno type="pmc">4801258</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4801258</idno><idno type="RBID">PMC:4801258</idno><idno type="doi">10.1073/pnas.1523468113</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000270</idno><idno type="wicri:Area/Pmc/Curation">000269</idno><idno type="wicri:Area/Pmc/Checkpoint">000083</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Novel family of terpene synthases evolved from <italic>trans</italic>-isoprenyl diphosphate synthases in a flea beetle</title><author><name sortKey="Beran, Franziska" sort="Beran, Franziska" uniqKey="Beran F" first="Franziska" last="Beran">Franziska Beran</name><affiliation wicri:level="1"><nlm:aff id="aff1">Research Group Sequestration and Detoxification in Insects,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Rahfeld, Peter" sort="Rahfeld, Peter" uniqKey="Rahfeld P" first="Peter" last="Rahfeld">Peter Rahfeld</name><affiliation wicri:level="1"><nlm:aff id="aff2">Department of Bioorganic Chemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Luck, Katrin" sort="Luck, Katrin" uniqKey="Luck K" first="Katrin" last="Luck">Katrin Luck</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Nagel, Raimund" sort="Nagel, Raimund" uniqKey="Nagel R" first="Raimund" last="Nagel">Raimund Nagel</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Vogel, Heiko" sort="Vogel, Heiko" uniqKey="Vogel H" first="Heiko" last="Vogel">Heiko Vogel</name><affiliation wicri:level="1"><nlm:aff id="aff4">Department of Entomology,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Wielsch, Natalie" sort="Wielsch, Natalie" uniqKey="Wielsch N" first="Natalie" last="Wielsch">Natalie Wielsch</name><affiliation wicri:level="1"><nlm:aff id="aff5">Department of Mass Spectrometry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Irmisch, Sandra" sort="Irmisch, Sandra" uniqKey="Irmisch S" first="Sandra" last="Irmisch">Sandra Irmisch</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Ramasamy, Srinivasan" sort="Ramasamy, Srinivasan" uniqKey="Ramasamy S" first="Srinivasan" last="Ramasamy">Srinivasan Ramasamy</name><affiliation wicri:level="1"><nlm:aff id="aff6">Entomology,<institution>AVRDC–The World Vegetable Center</institution>, Shanhua, Tainan 74151,<country>Taiwan</country></nlm:aff><country xml:lang="fr">Taïwan</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Gershenzon, Jonathan" sort="Gershenzon, Jonathan" uniqKey="Gershenzon J" first="Jonathan" last="Gershenzon">Jonathan Gershenzon</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Heckel, David G" sort="Heckel, David G" uniqKey="Heckel D" first="David G." last="Heckel">David G. Heckel</name><affiliation wicri:level="1"><nlm:aff id="aff4">Department of Entomology,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author><author><name sortKey="Kollner, Tobias G" sort="Kollner, Tobias G" uniqKey="Kollner T" first="Tobias G." last="Köllner">Tobias G. Köllner</name><affiliation wicri:level="1"><nlm:aff id="aff3">Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea># see nlm:aff country strict</wicri:regionArea></affiliation></author></analytic><series><title level="j">Proceedings of the National Academy of Sciences of the United States of America</title><idno type="ISSN">0027-8424</idno><idno type="eISSN">1091-6490</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Significance</title><p>Whether insect sesquiterpenes are synthesized de novo, derived from plant precursors, or produced by symbionts is often unknown. We identified an evolutionarily novel terpene synthase gene family in the striped flea beetle, a notorious pest of <italic>Brassica</italic> crops in North America and Asia, and one of these genes was shown to be directly involved in the biosynthesis of the male-specific sesquiterpene aggregation pheromone. Phylogenetic and gene structure analyses indicate that an expansion of the <italic>trans</italic>-isoprenyl diphosphate synthase gene family in the ancestor of the subfamily Galerucinae enabled functional diversification toward this terpene synthase gene family. These insights into how flea beetles synthesize their aggregation pheromones may lead to new approaches for pest management.</p></div></front></TEI><pmc article-type="research-article"><pmc-comment>The publisher of this article does not allow downloading of the full text in XML form.</pmc-comment>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Proc Natl Acad Sci U S A</journal-id><journal-id journal-id-type="iso-abbrev">Proc. Natl. Acad. Sci. U.S.A</journal-id><journal-id journal-id-type="hwp">pnas</journal-id><journal-id journal-id-type="pmc">pnas</journal-id><journal-id journal-id-type="publisher-id">PNAS</journal-id><journal-title-group><journal-title>Proceedings of the National Academy of Sciences of the United States of America</journal-title></journal-title-group><issn pub-type="ppub">0027-8424</issn><issn pub-type="epub">1091-6490</issn><publisher><publisher-name>National Academy of Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26936952</article-id><article-id pub-id-type="pmc">4801258</article-id><article-id pub-id-type="publisher-id">201523468</article-id><article-id pub-id-type="doi">10.1073/pnas.1523468113</article-id><article-categories><subj-group subj-group-type="heading"><subject>Biological Sciences</subject><subj-group><subject>Biochemistry</subject></subj-group></subj-group></article-categories><title-group><article-title>Novel family of terpene synthases evolved from <italic>trans</italic>-isoprenyl diphosphate synthases in a flea beetle</article-title><alt-title alt-title-type="short">Novel family of terpene synthases in a flea beetle</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Beran</surname><given-names>Franziska</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Rahfeld</surname><given-names>Peter</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref><xref ref-type="author-notes" rid="fn1"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Luck</surname><given-names>Katrin</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Nagel</surname><given-names>Raimund</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref><xref ref-type="author-notes" rid="fn2"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Vogel</surname><given-names>Heiko</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Wielsch</surname><given-names>Natalie</given-names></name><xref ref-type="aff" rid="aff5"><sup>e</sup></xref></contrib><contrib contrib-type="author"><name><surname>Irmisch</surname><given-names>Sandra</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref><xref ref-type="author-notes" rid="fn3"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ramasamy</surname><given-names>Srinivasan</given-names></name><xref ref-type="aff" rid="aff6"><sup>f</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gershenzon</surname><given-names>Jonathan</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Heckel</surname><given-names>David G.</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref></contrib><contrib contrib-type="author"><name><surname>Köllner</surname><given-names>Tobias G.</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><aff id="aff1"><sup>a</sup>Research Group Sequestration and Detoxification in Insects,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</aff><aff id="aff2"><sup>b</sup>Department of Bioorganic Chemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</aff><aff id="aff3"><sup>c</sup>Department of Biochemistry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</aff><aff id="aff4"><sup>d</sup>Department of Entomology,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</aff><aff id="aff5"><sup>e</sup>Department of Mass Spectrometry,<institution>Max Planck Institute for Chemical Ecology</institution>, 07745 Jena,<country>Germany</country>;</aff><aff id="aff6"><sup>f</sup>Entomology,<institution>AVRDC–The World Vegetable Center</institution>, Shanhua, Tainan 74151,<country>Taiwan</country></aff></contrib-group><author-notes><corresp id="cor1"><sup>1</sup>To whom correspondence should be addressed. Email: <email>fberan@ice.mpg.de</email>.</corresp><fn fn-type="edited-by"><p>Edited by Jerrold Meinwald, Cornell University, Ithaca, NY, and approved February 5, 2016 (received for review November 27, 2015)</p></fn><fn fn-type="con"><p>Author contributions: F.B., P.R., R.N., S.I., J.G., D.G.H., and T.G.K. designed research; F.B., P.R., K.L., R.N., H.V., N.W., and T.G.K. performed research; S.R. contributed new reagents/analytic tools; F.B., P.R., R.N., H.V., N.W., and T.G.K. analyzed data; and F.B. and T.G.K. wrote the paper.</p></fn><fn fn-type="present-address" id="fn1"><p><sup>2</sup>Present address: Department of Chemistry, The University of British Columbia, Vancouver, BC V6T 1Z1, Canada.</p></fn><fn fn-type="present-address" id="fn2"><p><sup>3</sup>Present address: Department of Biochemistry, Biophysics and Molecular Biology, Iowa State University, Ames, IA 50011.</p></fn><fn fn-type="present-address" id="fn3"><p><sup>4</sup>Present address: Michael Smith Laboratories, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada.</p></fn></author-notes><pub-date pub-type="ppub"><day>15</day><month>3</month><year>2016</year></pub-date><pub-date pub-type="epub"><day>02</day><month>3</month><year>2016</year></pub-date><volume>113</volume><issue>11</issue><fpage>2922</fpage><lpage>2927</lpage><self-uri xlink:title="pdf" xlink:href="pnas.201523468.pdf"></self-uri><abstract abstract-type="executive-summary"><title>Significance</title><p>Whether insect sesquiterpenes are synthesized de novo, derived from plant precursors, or produced by symbionts is often unknown. We identified an evolutionarily novel terpene synthase gene family in the striped flea beetle, a notorious pest of <italic>Brassica</italic> crops in North America and Asia, and one of these genes was shown to be directly involved in the biosynthesis of the male-specific sesquiterpene aggregation pheromone. Phylogenetic and gene structure analyses indicate that an expansion of the <italic>trans</italic>-isoprenyl diphosphate synthase gene family in the ancestor of the subfamily Galerucinae enabled functional diversification toward this terpene synthase gene family. These insights into how flea beetles synthesize their aggregation pheromones may lead to new approaches for pest management.</p></abstract><abstract><p>Sesquiterpenes play important roles in insect communication, for example as pheromones. However, no sesquiterpene synthases, the enzymes involved in construction of the basic carbon skeleton, have been identified in insects to date. We investigated the biosynthesis of the sesquiterpene (6<italic>R</italic>,7<italic>S</italic>)-himachala-9,11-diene in the crucifer flea beetle <italic>Phyllotreta striolata</italic>, a compound previously identified as a male-produced aggregation pheromone in several <italic>Phyllotreta</italic> species. A (6<italic>R</italic>,7<italic>S</italic>)-himachala-9,11-diene–producing sesquiterpene synthase activity was detected in crude beetle protein extracts, but only when (<italic>Z</italic>,<italic>E</italic>)-farnesyl diphosphate [(<italic>Z</italic>,<italic>E</italic>)-FPP] was offered as a substrate. No sequences resembling sesquiterpene synthases from plants, fungi, or bacteria were found in the <italic>P. striolata</italic> transcriptome, but we identified nine divergent putative <italic>trans</italic>-isoprenyl diphosphate synthase (<italic>trans</italic>-IDS) transcripts. Four of these putative <italic>trans</italic>-IDSs exhibited terpene synthase (TPS) activity when heterologously expressed. Recombinant <italic>Ps</italic>TPS1 converted (<italic>Z</italic>,<italic>E</italic>)-FPP to (6<italic>R</italic>,7<italic>S</italic>)-himachala-9,11-diene and other sesquiterpenes observed in beetle extracts. RNAi-mediated knockdown of <italic>Ps</italic>TPS1 mRNA in <italic>P. striolata</italic> males led to reduced emission of aggregation pheromone, confirming a significant role of <italic>Ps</italic>TPS1 in pheromone biosynthesis. Two expressed enzymes showed genuine IDS activity, with <italic>Ps</italic>IDS1 synthesizing (<italic>E</italic>,<italic>E</italic>)-FPP, whereas <italic>Ps</italic>IDS3 produced neryl diphosphate, (<italic>Z</italic>,<italic>Z</italic>)-FPP, and (<italic>Z</italic>,<italic>E</italic>)-FPP. In a phylogenetic analysis, the <italic>Ps</italic>TPS enzymes and <italic>Ps</italic>IDS3 were clearly separated from a clade of known coleopteran <italic>trans</italic>-IDS enzymes including <italic>Ps</italic>IDS1 and <italic>Ps</italic>IDS2. However, the exon–intron structures of <italic>IDS</italic> and <italic>TPS</italic> genes in <italic>P. striolata</italic> are conserved, suggesting that this TPS gene family evolved from <italic>trans-IDS</italic> ancestors.</p></abstract><kwd-group><kwd>isoprenyl diphosphate synthase</kwd><kwd>sesquiterpene synthase</kwd><kwd>(6<italic>R</italic>,7<italic>S</italic>)-himachala-9,11-diene</kwd><kwd>aggregation pheromone</kwd><kwd>flea beetle</kwd></kwd-group><counts><page-count count="6"></page-count></counts></article-meta></front></pmc><affiliations><list><country><li>Allemagne</li><li>Taïwan</li></country></list><tree><country name="Allemagne"><noRegion><name sortKey="Beran, Franziska" sort="Beran, Franziska" uniqKey="Beran F" first="Franziska" last="Beran">Franziska Beran</name></noRegion><name sortKey="Gershenzon, Jonathan" sort="Gershenzon, Jonathan" uniqKey="Gershenzon J" first="Jonathan" last="Gershenzon">Jonathan Gershenzon</name><name sortKey="Heckel, David G" sort="Heckel, David G" uniqKey="Heckel D" first="David G." last="Heckel">David G. Heckel</name><name sortKey="Irmisch, Sandra" sort="Irmisch, Sandra" uniqKey="Irmisch S" first="Sandra" last="Irmisch">Sandra Irmisch</name><name sortKey="Kollner, Tobias G" sort="Kollner, Tobias G" uniqKey="Kollner T" first="Tobias G." last="Köllner">Tobias G. Köllner</name><name sortKey="Luck, Katrin" sort="Luck, Katrin" uniqKey="Luck K" first="Katrin" last="Luck">Katrin Luck</name><name sortKey="Nagel, Raimund" sort="Nagel, Raimund" uniqKey="Nagel R" first="Raimund" last="Nagel">Raimund Nagel</name><name sortKey="Rahfeld, Peter" sort="Rahfeld, Peter" uniqKey="Rahfeld P" first="Peter" last="Rahfeld">Peter Rahfeld</name><name sortKey="Vogel, Heiko" sort="Vogel, Heiko" uniqKey="Vogel H" first="Heiko" last="Vogel">Heiko Vogel</name><name sortKey="Wielsch, Natalie" sort="Wielsch, Natalie" uniqKey="Wielsch N" first="Natalie" last="Wielsch">Natalie Wielsch</name></country><country name="Taïwan"><noRegion><name sortKey="Ramasamy, Srinivasan" sort="Ramasamy, Srinivasan" uniqKey="Ramasamy S" first="Srinivasan" last="Ramasamy">Srinivasan Ramasamy</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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|étape= Checkpoint
|type= RBID
|clé= PMC:4801258
|texte= Novel family of terpene synthases evolved from trans-isoprenyl diphosphate synthases in a flea beetle
}}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Checkpoint/RBID.i -Sk "pubmed:26936952" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Checkpoint/biblio.hfd \
| NlmPubMed2Wicri -a OrangerV1
| This area was generated with Dilib version V0.6.25. |  |