Emergence of terpene chemical communication in insects: Evolutionary recruitment of isoprenoid metabolism

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dc.contributor.authorRebholz, Zarleyen
dc.contributor.authorShewade, Leenaen
dc.contributor.authorKaler, Kylieen
dc.contributor.authorLarose, Haileyen
dc.contributor.authorSchubot, Florianen
dc.contributor.authorTholl, Dorotheaen
dc.contributor.authorMorozov, Alexandre V.en
dc.contributor.authorO'Maille, Paul E.en
dc.date.accessioned2023-08-03T14:39:25Zen
dc.date.available2023-08-03T14:39:25Zen
dc.date.issued2023-05en
dc.description.abstractInsects have evolved a chemical communication system using terpenoids, a structurally diverse class of specialized metabolites, previously thought to be exclusively produced by plants and microbes. Gene discovery, bioinformatics, and biochemical characterization of multiple insect terpene synthases (TPSs) revealed that isopentenyl diphosphate synthases (IDS), enzymes from primary isoprenoid metabolism, are their likely evolutionary progenitors. However, the mutations underlying the emergence of the TPS function remain a mystery. To address this gap, we present the first structural and mechanistic model for the evolutionary emergence of TPS function in insects. Through identifying key mechanistic differences between IDS and TPS enzymes, we hypothesize that the loss of isopentenyl diphosphate (IPP) binding motifs strongly correlates with the gain of the TPS function. Based on this premise, we have elaborated the first explicit structural definition of isopentenyl diphosphate-binding motifs (IBMs) and used the IBM definitions to examine previously characterized insect IDSs and TPSs and to predict the functions of as yet uncharacterized insect IDSs. Consistent with our hypothesis, we observed a clear pattern of disruptive substitutions to IBMs in characterized insect TPSs. In contrast, insect IDSs maintain essential consensus residues for binding IPP. Extending our analysis, we constructed the most comprehensive phylogeny of insect IDS sequences (430 full length sequences from eight insect orders) and used IBMs to predict the function of TPSs. Based on our analysis, we infer multiple, independent TPS emergence events across the class of insects, paving the way for future gene discovery efforts.en
dc.description.notesACKNOWLEDGMENTS This work was supported by National Science Foundation awards MCB1920914 to Alexandre V. Morozov, MCB1920922 to Paul E. O'Maille, and MCB1920925 to Dorothea Tholl.en
dc.description.sponsorshipNational Science Foundation [MCB1920914, MCB1920922, MCB1920925]en
dc.description.versionPublished versionen
dc.format.mimetypeapplication/pdfen
dc.identifier.doihttps://doi.org/10.1002/pro.4634en
dc.identifier.eissn1469-896Xen
dc.identifier.issn0961-8368en
dc.identifier.issue5en
dc.identifier.othere4634en
dc.identifier.pmid36974623en
dc.identifier.urihttp://hdl.handle.net/10919/115977en
dc.identifier.volume32en
dc.language.isoenen
dc.publisherWileyen
dc.rightsCreative Commons Attribution-NonCommercial 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by-nc/4.0/en
dc.subjectevolutionen
dc.subjectinsectsen
dc.subjectisoprenoiden
dc.subjectisopentenyl diphosphate synthaseen
dc.subjectmechanismen
dc.subjectmotifsen
dc.subjectphylogenyen
dc.subjectstructureen
dc.subjectterpeneen
dc.subjectTerpene synthaseen
dc.titleEmergence of terpene chemical communication in insects: Evolutionary recruitment of isoprenoid metabolismen
dc.title.serialProtein Scienceen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten

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