Evolution of isoprenyl diphosphate synthase-like terpene synthases in fungi
Identifieur interne : 000236 ( Pmc/Curation ); précédent : 000235; suivant : 000237Evolution 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
Url:
DOI: 10.1038/s41598-020-71219-z
PubMed: 32913319
PubMed Central: 7484799
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<author><name sortKey="Chen, Feng" sort="Chen, Feng" uniqKey="Chen F" first="Feng" last="Chen">Feng Chen</name>
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<front><div type="abstract" xml:lang="en"><p id="Par1">Terpene synthases (TPSs) and <italic>trans</italic>
-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 <italic>Melampsora</italic>
. Among the GGDPS family of the two <italic>Melampsora</italic>
species experimentally characterized, one enzyme was verified to be <italic>bona fide</italic>
GGDPS and all others were demonstrated to function as TPSs. <italic>Melampsora</italic>
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 <italic>ILTPSs</italic>
from a <italic>GGDPS</italic>
progenitor in fungi, after the split of <italic>Melampsora</italic>
from other genera within the class of Pucciniomycetes. For the poplar leaf rust fungus <italic>Melampsora larici-populina</italic>
, the transcripts of its <italic>ILTPS</italic>
genes were detected in infected poplar leaves, suggesting possible involvement of these recently evolved <italic>ILTPS</italic>
genes in the infection process. This study reveals the recurrent evolution of <italic>TPSs</italic>
from <italic>IDSs</italic>
since their ancient occurrence and points to the possibility of a wide distribution of <italic>ILTPS</italic>
genes in three domains of life.</p>
</div>
</front>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Sci Rep</journal-id>
<journal-id journal-id-type="iso-abbrev">Sci Rep</journal-id>
<journal-title-group><journal-title>Scientific Reports</journal-title>
</journal-title-group>
<issn pub-type="epub">2045-2322</issn>
<publisher><publisher-name>Nature Publishing Group UK</publisher-name>
<publisher-loc>London</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32913319</article-id>
<article-id pub-id-type="pmc">7484799</article-id>
<article-id pub-id-type="publisher-id">71219</article-id>
<article-id pub-id-type="doi">10.1038/s41598-020-71219-z</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Evolution of isoprenyl diphosphate synthase-like terpene synthases in fungi</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Wei</surname>
<given-names>Guo</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Eberl</surname>
<given-names>Franziska</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Chen</surname>
<given-names>Xinlu</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Zhang</surname>
<given-names>Chi</given-names>
</name>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Unsicker</surname>
<given-names>Sybille B.</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Köllner</surname>
<given-names>Tobias G.</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Gershenzon</surname>
<given-names>Jonathan</given-names>
</name>
<xref ref-type="aff" rid="Aff2">2</xref>
</contrib>
<contrib contrib-type="author" corresp="yes"><name><surname>Chen</surname>
<given-names>Feng</given-names>
</name>
<address><email>fengc@utk.edu</email>
</address>
<xref ref-type="aff" rid="Aff1">1</xref>
</contrib>
<aff id="Aff1"><label>1</label>
<institution-wrap><institution-id institution-id-type="GRID">grid.411461.7</institution-id>
<institution-id institution-id-type="ISNI">0000 0001 2315 1184</institution-id>
<institution>Department of Plant Sciences,</institution>
<institution>University of Tennessee,</institution>
</institution-wrap>
Knoxville, TN 37996 USA</aff>
<aff id="Aff2"><label>2</label>
<institution-wrap><institution-id institution-id-type="GRID">grid.418160.a</institution-id>
<institution-id institution-id-type="ISNI">0000 0004 0491 7131</institution-id>
<institution>Department of Biochemistry,</institution>
<institution>Max Planck Institute for Chemical Ecology,</institution>
</institution-wrap>
Hans-Knöll Str. 8, 07745 Jena, Germany</aff>
</contrib-group>
<pub-date pub-type="epub"><day>10</day>
<month>9</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="pmc-release"><day>10</day>
<month>9</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="collection"><year>2020</year>
</pub-date>
<volume>10</volume>
<elocation-id>14944</elocation-id>
<history><date date-type="received"><day>30</day>
<month>4</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>27</day>
<month>7</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© The Author(s) 2020</copyright-statement>
<license license-type="OpenAccess"><license-p><bold>Open Access</bold>
This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
.</license-p>
</license>
</permissions>
<abstract id="Abs1"><p id="Par1">Terpene synthases (TPSs) and <italic>trans</italic>
-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 <italic>Melampsora</italic>
. Among the GGDPS family of the two <italic>Melampsora</italic>
species experimentally characterized, one enzyme was verified to be <italic>bona fide</italic>
GGDPS and all others were demonstrated to function as TPSs. <italic>Melampsora</italic>
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 <italic>ILTPSs</italic>
from a <italic>GGDPS</italic>
progenitor in fungi, after the split of <italic>Melampsora</italic>
from other genera within the class of Pucciniomycetes. For the poplar leaf rust fungus <italic>Melampsora larici-populina</italic>
, the transcripts of its <italic>ILTPS</italic>
genes were detected in infected poplar leaves, suggesting possible involvement of these recently evolved <italic>ILTPS</italic>
genes in the infection process. This study reveals the recurrent evolution of <italic>TPSs</italic>
from <italic>IDSs</italic>
since their ancient occurrence and points to the possibility of a wide distribution of <italic>ILTPS</italic>
genes in three domains of life.</p>
</abstract>
<kwd-group kwd-group-type="npg-subject"><title>Subject terms</title>
<kwd>Biochemistry</kwd>
<kwd>Molecular biology</kwd>
</kwd-group>
<custom-meta-group><custom-meta><meta-name>issue-copyright-statement</meta-name>
<meta-value>© The Author(s) 2020</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
</front>
</pmc>
</record>
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