Evolution of a secondary metabolic pathway from primary metabolism: shikimate and quinate biosynthesis in plants.
Identifieur interne : 000F12 ( Main/Exploration ); précédent : 000F11; suivant : 000F13Evolution of a secondary metabolic pathway from primary metabolism: shikimate and quinate biosynthesis in plants.
Auteurs : Yuriko Carrington [Canada] ; Jia Guo [Canada] ; Cuong H. Le [Canada] ; Alexander Fillo [Canada] ; Junsu Kwon [Canada] ; Lan T. Tran [Canada] ; Jürgen Ehlting [Canada]Source :
- The Plant journal : for cell and molecular biology [ 1365-313X ] ; 2018.
Abstract
The shikimate pathway synthesizes aromatic amino acids essential for protein biosynthesis. Shikimate dehydrogenase (SDH) is a central enzyme of this primary metabolic pathway, producing shikimate. The structurally similar quinate is a secondary metabolite synthesized by quinate dehydrogenase (QDH). SDH and QDH belong to the same gene family, which diverged into two phylogenetic clades after a defining gene duplication just prior to the angiosperm/gymnosperm split. Non-seed plants that diverged before this duplication harbour only a single gene of this family. Extant representatives from the chlorophytes (Chlamydomonas reinhardtii), bryophytes (Physcomitrella patens) and lycophytes (Selaginella moellendorfii) encoded almost exclusively SDH activity in vitro. A reconstructed ancestral sequence representing the node just prior to the gene duplication also encoded SDH activity. Quinate dehydrogenase activity was gained only in seed plants following gene duplication. Quinate dehydrogenases of gymnosperms, represented here by Pinus taeda, may be reminiscent of an evolutionary intermediate since they encode equal SDH and QDH activities. The second copy in P. taeda maintained specificity for shikimate similar to the activity found in the angiosperm SDH sister clade. The codon for a tyrosine residue within the active site displayed a signature of positive selection at the node defining the QDH clade, where it changed to a glycine. Replacing the tyrosine with a glycine in a highly shikimate-specific angiosperm SDH was sufficient to gain some QDH function. Thus, very few mutations were necessary to facilitate the evolution of QDH genes.
DOI: 10.1111/tpj.13990
PubMed: 29894016
Affiliations:
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Le</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biochemistry and Microbiology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Biochemistry and Microbiology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2</wicri:regionArea><wicri:noRegion>V8W 2Y2</wicri:noRegion></affiliation></author><author><name sortKey="Fillo, Alexander" sort="Fillo, Alexander" uniqKey="Fillo A" first="Alexander" last="Fillo">Alexander Fillo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2</wicri:regionArea><wicri:noRegion>V8W 2Y2</wicri:noRegion></affiliation></author><author><name sortKey="Kwon, Junsu" sort="Kwon, Junsu" uniqKey="Kwon J" first="Junsu" last="Kwon">Junsu Kwon</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2</wicri:regionArea><wicri:noRegion>V8W 2Y2</wicri:noRegion></affiliation></author><author><name sortKey="Tran, Lan T" sort="Tran, Lan T" uniqKey="Tran L" first="Lan T" last="Tran">Lan T. Tran</name><affiliation wicri:level="4"><nlm:affiliation>Department of Botany, University of British Columbia, Vancouver, BC, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Botany, University of British Columbia, Vancouver, BC</wicri:regionArea><orgName type="university">Université de la Colombie-Britannique</orgName><placeName><settlement type="city">Vancouver</settlement><region type="state">Colombie-Britannique </region></placeName></affiliation></author><author><name sortKey="Ehlting, Jurgen" sort="Ehlting, Jurgen" uniqKey="Ehlting J" first="Jürgen" last="Ehlting">Jürgen Ehlting</name><affiliation wicri:level="1"><nlm:affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</nlm:affiliation><country xml:lang="fr">Canada</country><wicri:regionArea>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2</wicri:regionArea><wicri:noRegion>V8W 2Y2</wicri:noRegion></affiliation></author></analytic><series><title level="j">The Plant journal : for cell and molecular biology</title><idno type="eISSN">1365-313X</idno><imprint><date when="2018" type="published">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">The shikimate pathway synthesizes aromatic amino acids essential for protein biosynthesis. Shikimate dehydrogenase (SDH) is a central enzyme of this primary metabolic pathway, producing shikimate. The structurally similar quinate is a secondary metabolite synthesized by quinate dehydrogenase (QDH). SDH and QDH belong to the same gene family, which diverged into two phylogenetic clades after a defining gene duplication just prior to the angiosperm/gymnosperm split. Non-seed plants that diverged before this duplication harbour only a single gene of this family. Extant representatives from the chlorophytes (Chlamydomonas reinhardtii), bryophytes (Physcomitrella patens) and lycophytes (Selaginella moellendorfii) encoded almost exclusively SDH activity in vitro. A reconstructed ancestral sequence representing the node just prior to the gene duplication also encoded SDH activity. Quinate dehydrogenase activity was gained only in seed plants following gene duplication. Quinate dehydrogenases of gymnosperms, represented here by Pinus taeda, may be reminiscent of an evolutionary intermediate since they encode equal SDH and QDH activities. The second copy in P. taeda maintained specificity for shikimate similar to the activity found in the angiosperm SDH sister clade. The codon for a tyrosine residue within the active site displayed a signature of positive selection at the node defining the QDH clade, where it changed to a glycine. Replacing the tyrosine with a glycine in a highly shikimate-specific angiosperm SDH was sufficient to gain some QDH function. Thus, very few mutations were necessary to facilitate the evolution of QDH genes.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">29894016</PMID><DateRevised><Year>2019</Year><Month>11</Month><Day>20</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1365-313X</ISSN><JournalIssue CitedMedium="Internet"><PubDate><Year>2018</Year><Month>Jun</Month><Day>12</Day></PubDate></JournalIssue><Title>The Plant journal : for cell and molecular biology</Title><ISOAbbreviation>Plant J</ISOAbbreviation></Journal><ArticleTitle>Evolution of a secondary metabolic pathway from primary metabolism: shikimate and quinate biosynthesis in plants.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1111/tpj.13990</ELocationID><Abstract><AbstractText>The shikimate pathway synthesizes aromatic amino acids essential for protein biosynthesis. Shikimate dehydrogenase (SDH) is a central enzyme of this primary metabolic pathway, producing shikimate. The structurally similar quinate is a secondary metabolite synthesized by quinate dehydrogenase (QDH). SDH and QDH belong to the same gene family, which diverged into two phylogenetic clades after a defining gene duplication just prior to the angiosperm/gymnosperm split. Non-seed plants that diverged before this duplication harbour only a single gene of this family. Extant representatives from the chlorophytes (Chlamydomonas reinhardtii), bryophytes (Physcomitrella patens) and lycophytes (Selaginella moellendorfii) encoded almost exclusively SDH activity in vitro. A reconstructed ancestral sequence representing the node just prior to the gene duplication also encoded SDH activity. Quinate dehydrogenase activity was gained only in seed plants following gene duplication. Quinate dehydrogenases of gymnosperms, represented here by Pinus taeda, may be reminiscent of an evolutionary intermediate since they encode equal SDH and QDH activities. The second copy in P. taeda maintained specificity for shikimate similar to the activity found in the angiosperm SDH sister clade. The codon for a tyrosine residue within the active site displayed a signature of positive selection at the node defining the QDH clade, where it changed to a glycine. Replacing the tyrosine with a glycine in a highly shikimate-specific angiosperm SDH was sufficient to gain some QDH function. Thus, very few mutations were necessary to facilitate the evolution of QDH genes.</AbstractText><CopyrightInformation>© 2018 The Authors The Plant Journal © 2018 John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Carrington</LastName><ForeName>Yuriko</ForeName><Initials>Y</Initials><AffiliationInfo><Affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Guo</LastName><ForeName>Jia</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Le</LastName><ForeName>Cuong H</ForeName><Initials>CH</Initials><AffiliationInfo><Affiliation>Department of Biochemistry and Microbiology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fillo</LastName><ForeName>Alexander</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kwon</LastName><ForeName>Junsu</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tran</LastName><ForeName>Lan T</ForeName><Initials>LT</Initials><AffiliationInfo><Affiliation>Department of Botany, University of British Columbia, Vancouver, BC, Canada.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ehlting</LastName><ForeName>Jürgen</ForeName><Initials>J</Initials><Identifier Source="ORCID">http://orcid.org/0000-0003-2302-696X</Identifier><AffiliationInfo><Affiliation>Department of Biology and Centre for Forest Biology, University of Victoria, PO Box 1700, Station CSC, Victoria, BC, V8W 2Y2, Canada.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2018</Year><Month>06</Month><Day>12</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Plant J</MedlineTA><NlmUniqueID>9207397</NlmUniqueID><ISSNLinking>0960-7412</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Chlamydomonas reinhardtii
</Keyword><Keyword MajorTopicYN="N">Physcomitrella patens
</Keyword><Keyword MajorTopicYN="N">Pinus taeda
</Keyword><Keyword MajorTopicYN="N">Populus trichocarpa
</Keyword><Keyword MajorTopicYN="N">Rhodopirellula baltica
</Keyword><Keyword MajorTopicYN="N">Selaginella moellendorfii
</Keyword><Keyword MajorTopicYN="N">molecular evolution</Keyword><Keyword MajorTopicYN="N">secondary metabolism</Keyword><Keyword MajorTopicYN="N">shikimate/quinate dehydrogenase</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2018</Year><Month>03</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2018</Year><Month>05</Month><Day>23</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2018</Year><Month>05</Month><Day>29</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2018</Year><Month>6</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2018</Year><Month>6</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2018</Year><Month>6</Month><Day>13</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">29894016</ArticleId><ArticleId IdType="doi">10.1111/tpj.13990</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Canada</li></country><region><li>Colombie-Britannique </li></region><settlement><li>Vancouver</li></settlement><orgName><li>Université de la Colombie-Britannique</li></orgName></list><tree><country name="Canada"><noRegion><name sortKey="Carrington, Yuriko" sort="Carrington, Yuriko" uniqKey="Carrington Y" first="Yuriko" last="Carrington">Yuriko Carrington</name></noRegion><name sortKey="Ehlting, Jurgen" sort="Ehlting, Jurgen" uniqKey="Ehlting J" first="Jürgen" last="Ehlting">Jürgen Ehlting</name><name sortKey="Fillo, Alexander" sort="Fillo, Alexander" uniqKey="Fillo A" first="Alexander" last="Fillo">Alexander Fillo</name><name sortKey="Guo, Jia" sort="Guo, Jia" uniqKey="Guo J" first="Jia" last="Guo">Jia Guo</name><name sortKey="Kwon, Junsu" sort="Kwon, Junsu" uniqKey="Kwon J" first="Junsu" last="Kwon">Junsu Kwon</name><name sortKey="Le, Cuong H" sort="Le, Cuong H" uniqKey="Le C" first="Cuong H" last="Le">Cuong H. Le</name><name sortKey="Tran, Lan T" sort="Tran, Lan T" uniqKey="Tran L" first="Lan T" last="Tran">Lan T. Tran</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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