Evolution of isoprenyl diphosphate synthase-like terpene synthases in fungi.
Identifieur interne : 000414 ( Main/Exploration ); précédent : 000413; suivant : 000415Evolution of isoprenyl diphosphate synthase-like terpene synthases in fungi.
Auteurs : Guo Wei [États-Unis] ; Franziska Eberl [Allemagne] ; Xinlu Chen [États-Unis] ; Chi Zhang [États-Unis] ; Sybille B. Unsicker [Allemagne] ; Tobias G. Köllner [Allemagne] ; Jonathan Gershenzon [Allemagne] ; Feng Chen [États-Unis]Source :
- Scientific reports [ 2045-2322 ] ; 2020.
Abstract
Terpene synthases (TPSs) and trans-isoprenyl diphosphate synthases (IDSs) are among the core enzymes for creating the enormous diversity of terpenoids. Despite having no sequence homology, TPSs and IDSs share a conserved "α terpenoid synthase fold" and a trinuclear metal cluster for catalysis, implying a common ancestry with TPSs hypothesized to evolve from IDSs anciently. Here we report on the identification and functional characterization of novel IDS-like TPSs (ILTPSs) in fungi that evolved from IDS relatively recently, indicating recurrent evolution of TPSs from IDSs. Through large-scale bioinformatic analyses of fungal IDSs, putative ILTPSs that belong to the geranylgeranyl diphosphate synthase (GGDPS) family of IDSs were identified in three species of Melampsora. Among the GGDPS family of the two Melampsora species experimentally characterized, one enzyme was verified to be bona fide GGDPS and all others were demonstrated to function as TPSs. Melampsora ILTPSs displayed kinetic parameters similar to those of classic TPSs. Key residues underlying the determination of GGDPS versus ILTPS activity and functional divergence of ILTPSs were identified. Phylogenetic analysis implies a recent origination of these ILTPSs from a GGDPS progenitor in fungi, after the split of Melampsora from other genera within the class of Pucciniomycetes. For the poplar leaf rust fungus Melampsora larici-populina, the transcripts of its ILTPS genes were detected in infected poplar leaves, suggesting possible involvement of these recently evolved ILTPS genes in the infection process. This study reveals the recurrent evolution of TPSs from IDSs since their ancient occurrence and points to the possibility of a wide distribution of ILTPS genes in three domains of life.
DOI: 10.1038/s41598-020-71219-z
PubMed: 32913319
PubMed Central: PMC7484799
Affiliations:
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Unsicker</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></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:affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></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:affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena</wicri:regionArea><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>07745, Jena</wicri:noRegion><wicri:noRegion>Jena</wicri:noRegion></affiliation></author><author><name sortKey="Chen, Feng" sort="Chen, Feng" uniqKey="Chen F" first="Feng" last="Chen">Feng Chen</name><affiliation wicri:level="1"><nlm:affiliation>Department of Plant Sciences, University of Tennessee, Knoxville, TN, 37996, USA. fengc@utk.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Sciences, University of Tennessee, Knoxville, TN, 37996</wicri:regionArea><wicri:noRegion>37996</wicri:noRegion></affiliation></author></analytic><series><title level="j">Scientific reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Terpene synthases (TPSs) and trans-isoprenyl diphosphate synthases (IDSs) are among the core enzymes for creating the enormous diversity of terpenoids. Despite having no sequence homology, TPSs and IDSs share a conserved "α terpenoid synthase fold" and a trinuclear metal cluster for catalysis, implying a common ancestry with TPSs hypothesized to evolve from IDSs anciently. Here we report on the identification and functional characterization of novel IDS-like TPSs (ILTPSs) in fungi that evolved from IDS relatively recently, indicating recurrent evolution of TPSs from IDSs. Through large-scale bioinformatic analyses of fungal IDSs, putative ILTPSs that belong to the geranylgeranyl diphosphate synthase (GGDPS) family of IDSs were identified in three species of Melampsora. Among the GGDPS family of the two Melampsora species experimentally characterized, one enzyme was verified to be bona fide GGDPS and all others were demonstrated to function as TPSs. Melampsora ILTPSs displayed kinetic parameters similar to those of classic TPSs. Key residues underlying the determination of GGDPS versus ILTPS activity and functional divergence of ILTPSs were identified. Phylogenetic analysis implies a recent origination of these ILTPSs from a GGDPS progenitor in fungi, after the split of Melampsora from other genera within the class of Pucciniomycetes. For the poplar leaf rust fungus Melampsora larici-populina, the transcripts of its ILTPS genes were detected in infected poplar leaves, suggesting possible involvement of these recently evolved ILTPS genes in the infection process. This study reveals the recurrent evolution of TPSs from IDSs since their ancient occurrence and points to the possibility of a wide distribution of ILTPS genes in three domains of life.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32913319</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>27</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2045-2322</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>09</Month><Day>10</Day></PubDate></JournalIssue><Title>Scientific reports</Title><ISOAbbreviation>Sci Rep</ISOAbbreviation></Journal><ArticleTitle>Evolution of isoprenyl diphosphate synthase-like terpene synthases in fungi.</ArticleTitle><Pagination><MedlinePgn>14944</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41598-020-71219-z</ELocationID><Abstract><AbstractText>Terpene synthases (TPSs) and trans-isoprenyl diphosphate synthases (IDSs) are among the core enzymes for creating the enormous diversity of terpenoids. Despite having no sequence homology, TPSs and IDSs share a conserved "α terpenoid synthase fold" and a trinuclear metal cluster for catalysis, implying a common ancestry with TPSs hypothesized to evolve from IDSs anciently. Here we report on the identification and functional characterization of novel IDS-like TPSs (ILTPSs) in fungi that evolved from IDS relatively recently, indicating recurrent evolution of TPSs from IDSs. Through large-scale bioinformatic analyses of fungal IDSs, putative ILTPSs that belong to the geranylgeranyl diphosphate synthase (GGDPS) family of IDSs were identified in three species of Melampsora. Among the GGDPS family of the two Melampsora species experimentally characterized, one enzyme was verified to be bona fide GGDPS and all others were demonstrated to function as TPSs. Melampsora ILTPSs displayed kinetic parameters similar to those of classic TPSs. Key residues underlying the determination of GGDPS versus ILTPS activity and functional divergence of ILTPSs were identified. Phylogenetic analysis implies a recent origination of these ILTPSs from a GGDPS progenitor in fungi, after the split of Melampsora from other genera within the class of Pucciniomycetes. For the poplar leaf rust fungus Melampsora larici-populina, the transcripts of its ILTPS genes were detected in infected poplar leaves, suggesting possible involvement of these recently evolved ILTPS genes in the infection process. This study reveals the recurrent evolution of TPSs from IDSs since their ancient occurrence and points to the possibility of a wide distribution of ILTPS genes in three domains of life.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Wei</LastName><ForeName>Guo</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of Tennessee, Knoxville, TN, 37996, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Eberl</LastName><ForeName>Franziska</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Xinlu</ForeName><Initials>X</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of Tennessee, Knoxville, TN, 37996, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zhang</LastName><ForeName>Chi</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of Tennessee, Knoxville, TN, 37996, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Unsicker</LastName><ForeName>Sybille B</ForeName><Initials>SB</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Köllner</LastName><ForeName>Tobias G</ForeName><Initials>TG</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gershenzon</LastName><ForeName>Jonathan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, Max Planck Institute for Chemical Ecology, Hans-Knöll Str. 8, 07745, Jena, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chen</LastName><ForeName>Feng</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of Tennessee, Knoxville, TN, 37996, USA. fengc@utk.edu.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>10</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Sci Rep</MedlineTA><NlmUniqueID>101563288</NlmUniqueID><ISSNLinking>2045-2322</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate 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name="États-Unis"><noRegion><name sortKey="Wei, Guo" sort="Wei, Guo" uniqKey="Wei G" first="Guo" last="Wei">Guo Wei</name></noRegion><name sortKey="Chen, Feng" sort="Chen, Feng" uniqKey="Chen F" first="Feng" last="Chen">Feng Chen</name><name sortKey="Chen, Xinlu" sort="Chen, Xinlu" uniqKey="Chen X" first="Xinlu" last="Chen">Xinlu Chen</name><name sortKey="Zhang, Chi" sort="Zhang, Chi" uniqKey="Zhang C" first="Chi" last="Zhang">Chi Zhang</name></country><country name="Allemagne"><noRegion><name sortKey="Eberl, Franziska" sort="Eberl, Franziska" uniqKey="Eberl F" first="Franziska" last="Eberl">Franziska Eberl</name></noRegion><name sortKey="Gershenzon, Jonathan" sort="Gershenzon, Jonathan" uniqKey="Gershenzon J" first="Jonathan" last="Gershenzon">Jonathan Gershenzon</name><name sortKey="Kollner, Tobias G" sort="Kollner, Tobias G" uniqKey="Kollner T" first="Tobias G" last="Köllner">Tobias G. Köllner</name><name sortKey="Unsicker, Sybille B" sort="Unsicker, Sybille B" uniqKey="Unsicker S" first="Sybille B" last="Unsicker">Sybille B. Unsicker</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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