Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari.
Identifieur interne : 000052 ( Main/Exploration ); précédent : 000051; suivant : 000053Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari.
Auteurs : Somnath S. Pokhare [Allemagne, Inde] ; Peter Thorpe [Royaume-Uni] ; Pete Hedley [Royaume-Uni] ; Jennifer Morris [Royaume-Uni] ; Samer S. Habash [Allemagne] ; Abdelnaser Elashry [Allemagne] ; Sebastian Eves-Van Den Akker [Royaume-Uni] ; Florian M W. Grundler [Allemagne] ; John T. Jones [Royaume-Uni]Source :
- The Plant journal : for cell and molecular biology [ 1365-313X ] ; 2020.
Abstract
Interactions between plant-parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari, a cyst nematode parasite of rice (Oryza sativa) and sugarcane (Saccharum officinarum). A multi-gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot-parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non-effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non-effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant-peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION-like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant-parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co-occurred with the transition from a dicot-parasitic to a monocot-parasitic lifestyle.
DOI: 10.1111/tpj.14910
PubMed: 32623778
Affiliations:
- Allemagne, Inde, Royaume-Uni
- Angleterre, Angleterre de l'Est, District de Cologne, Rhénanie-du-Nord-Westphalie
- Bonn, Cambridge
- Université de Cambridge
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Habash</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Elashry, Abdelnaser" sort="Elashry, Abdelnaser" uniqKey="Elashry A" first="Abdelnaser" last="Elashry">Abdelnaser Elashry</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Eves Van Den Akker, Sebastian" sort="Eves Van Den Akker, Sebastian" uniqKey="Eves Van Den Akker S" first="Sebastian" last="Eves-Van Den Akker">Sebastian Eves-Van Den Akker</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Grundler, Florian M W" sort="Grundler, Florian M W" uniqKey="Grundler F" first="Florian M W" last="Grundler">Florian M W. Grundler</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Jones, John T" sort="Jones, John T" uniqKey="Jones J" first="John T" last="Jones">John T. Jones</name><affiliation wicri:level="1"><nlm:affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Biology, University of St Andrews, North Haugh, St Andrews, KY16 9TZ, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Biology, University of St Andrews, North Haugh, St Andrews, KY16 9TZ</wicri:regionArea><wicri:noRegion>KY16 9TZ</wicri:noRegion></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2020">2020</date><idno type="RBID">pubmed:32623778</idno><idno type="pmid">32623778</idno><idno type="doi">10.1111/tpj.14910</idno><idno type="wicri:Area/Main/Corpus">000202</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Corpus" wicri:corpus="PubMed">000202</idno><idno type="wicri:Area/Main/Curation">000202</idno><idno type="wicri:explorRef" wicri:stream="Main" wicri:step="Curation">000202</idno><idno type="wicri:Area/Main/Exploration">000202</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari.</title><author><name sortKey="Pokhare, Somnath S" sort="Pokhare, Somnath S" uniqKey="Pokhare S" first="Somnath S" last="Pokhare">Somnath S. Pokhare</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Crop Protection Division, ICAR-National Rice Research Institute, Cuttack, Odisha, 753006, India.</nlm:affiliation><country xml:lang="fr">Inde</country><wicri:regionArea>Crop Protection Division, ICAR-National Rice Research Institute, Cuttack, Odisha, 753006</wicri:regionArea><wicri:noRegion>753006</wicri:noRegion></affiliation></author><author><name sortKey="Thorpe, Peter" sort="Thorpe, Peter" uniqKey="Thorpe P" first="Peter" last="Thorpe">Peter Thorpe</name><affiliation wicri:level="1"><nlm:affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Medicine, University of St Andrews, North Haugh, St Andrews, KY16 9TZ, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Medicine, University of St Andrews, North Haugh, St Andrews, KY16 9TZ</wicri:regionArea><wicri:noRegion>KY16 9TZ</wicri:noRegion></affiliation></author><author><name sortKey="Hedley, Pete" sort="Hedley, Pete" uniqKey="Hedley P" first="Pete" last="Hedley">Pete Hedley</name><affiliation wicri:level="1"><nlm:affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Morris, Jennifer" sort="Morris, Jennifer" uniqKey="Morris J" first="Jennifer" last="Morris">Jennifer Morris</name><affiliation wicri:level="1"><nlm:affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation></author><author><name sortKey="Habash, Samer S" sort="Habash, Samer S" uniqKey="Habash S" first="Samer S" last="Habash">Samer S. Habash</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Elashry, Abdelnaser" sort="Elashry, Abdelnaser" uniqKey="Elashry A" first="Abdelnaser" last="Elashry">Abdelnaser Elashry</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Eves Van Den Akker, Sebastian" sort="Eves Van Den Akker, Sebastian" uniqKey="Eves Van Den Akker S" first="Sebastian" last="Eves-Van Den Akker">Sebastian Eves-Van Den Akker</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA</wicri:regionArea><orgName type="university">Université de Cambridge</orgName><placeName><settlement type="city">Cambridge</settlement><region type="country">Angleterre</region><region type="région" nuts="1">Angleterre de l'Est</region></placeName></affiliation></author><author><name sortKey="Grundler, Florian M W" sort="Grundler, Florian M W" uniqKey="Grundler F" first="Florian M W" last="Grundler">Florian M W. Grundler</name><affiliation wicri:level="3"><nlm:affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</nlm:affiliation><country xml:lang="fr">Allemagne</country><wicri:regionArea>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Jones, John T" sort="Jones, John T" uniqKey="Jones J" first="John T" last="Jones">John T. Jones</name><affiliation wicri:level="1"><nlm:affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA</wicri:regionArea><wicri:noRegion>DD2 5DA</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:affiliation>School of Biology, University of St Andrews, North Haugh, St Andrews, KY16 9TZ, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>School of Biology, University of St Andrews, North Haugh, St Andrews, KY16 9TZ</wicri:regionArea><wicri:noRegion>KY16 9TZ</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="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Interactions between plant-parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari, a cyst nematode parasite of rice (Oryza sativa) and sugarcane (Saccharum officinarum). A multi-gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot-parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non-effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non-effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant-peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION-like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant-parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co-occurred with the transition from a dicot-parasitic to a monocot-parasitic lifestyle.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32623778</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>17</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1365-313X</ISSN><JournalIssue CitedMedium="Internet"><Volume>103</Volume><Issue>4</Issue><PubDate><Year>2020</Year><Month>08</Month></PubDate></JournalIssue><Title>The Plant journal : for cell and molecular biology</Title><ISOAbbreviation>Plant J</ISOAbbreviation></Journal><ArticleTitle>Signatures of adaptation to a monocot host in the plant-parasitic cyst nematode Heterodera sacchari.</ArticleTitle><Pagination><MedlinePgn>1263-1274</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1111/tpj.14910</ELocationID><Abstract><AbstractText>Interactions between plant-parasitic nematodes and their hosts are mediated by effectors, i.e. secreted proteins that manipulate the plant to the benefit of the pathogen. To understand the role of effectors in host adaptation in nematodes, we analysed the transcriptome of Heterodera sacchari, a cyst nematode parasite of rice (Oryza sativa) and sugarcane (Saccharum officinarum). A multi-gene phylogenetic analysis showed that H. sacchari and the cereal cyst nematode Heterodera avenae share a common evolutionary origin and that they evolved to parasitise monocot plants from a common dicot-parasitic ancestor. We compared the effector repertoires of H. sacchari with those of the dicot parasites Heterodera glycines and Globodera rostochiensis to understand the consequences of this transition. While, in general, effector repertoires are similar between the species, comparing effectors and non-effectors of H. sacchari and G. rostochiensis shows that effectors have accumulated more mutations than non-effectors. Although most effectors show conserved spatiotemporal expression profiles and likely function, some H. sacchari effectors are adapted to monocots. This is exemplified by the plant-peptide hormone mimics, the CLAVATA3/EMBRYO SURROUNDING REGION-like (CLE) effectors. Peptide hormones encoded by H. sacchari CLE effectors are more similar to those from rice than those from other plants, or those from other plant-parasitic nematodes. We experimentally validated the functional significance of these observations by demonstrating that CLE peptides encoded by H. sacchari induce a short root phenotype in rice, whereas those from a related dicot parasite do not. These data provide a functional example of effector evolution that co-occurred with the transition from a dicot-parasitic to a monocot-parasitic lifestyle.</AbstractText><CopyrightInformation>© 2020 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Pokhare</LastName><ForeName>Somnath S</ForeName><Initials>SS</Initials><AffiliationInfo><Affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Crop Protection Division, ICAR-National Rice Research Institute, Cuttack, Odisha, 753006, India.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Thorpe</LastName><ForeName>Peter</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Medicine, University of St Andrews, North Haugh, St Andrews, KY16 9TZ, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hedley</LastName><ForeName>Pete</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Morris</LastName><ForeName>Jennifer</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Habash</LastName><ForeName>Samer S</ForeName><Initials>SS</Initials><AffiliationInfo><Affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Elashry</LastName><ForeName>Abdelnaser</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Eves-van den Akker</LastName><ForeName>Sebastian</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, CB2 3EA, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Grundler</LastName><ForeName>Florian M W</ForeName><Initials>FMW</Initials><AffiliationInfo><Affiliation>Department of Molecular Phytomedicine, Institute of Crop Science and Resource Conservation, University of Bonn, Bonn, 53115, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jones</LastName><ForeName>John T</ForeName><Initials>JT</Initials><Identifier Source="ORCID">0000-0003-2074-0551</Identifier><AffiliationInfo><Affiliation>The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Biology, University of St Andrews, North Haugh, St Andrews, KY16 9TZ, UK.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>BB/R011311/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>BB/S006397/1</GrantID><Acronym>BB_</Acronym><Agency>Biotechnology and Biological Sciences Research Council</Agency><Country>United Kingdom</Country></Grant><Grant><GrantID>105621/Z/14/Z</GrantID><Acronym>WT_</Acronym><Agency>Wellcome Trust</Agency><Country>United Kingdom</Country></Grant></GrantList><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>07</Month><Day>22</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Plant J</MedlineTA><NlmUniqueID>9207397</NlmUniqueID><ISSNLinking>0960-7412</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><CommentsCorrectionsList><CommentsCorrections RefType="CommentIn"><RefSource>Plant J. 2020 Aug;103(4):1261-1262</RefSource><PMID Version="1">32805072</PMID></CommentsCorrections></CommentsCorrectionsList><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Heterodera sacchari
</Keyword><Keyword MajorTopicYN="Y">Peptide hormone mimics</Keyword><Keyword MajorTopicYN="Y">effectors</Keyword><Keyword MajorTopicYN="Y">transcriptomics</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2019</Year><Month>01</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>18</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>7</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>7</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>7</Month><Day>6</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate></History><PublicationStatus>ppublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32623778</ArticleId><ArticleId IdType="doi">10.1111/tpj.14910</ArticleId></ArticleIdList><ReferenceList><Title>REFERENCES</Title><Reference><Citation>Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 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Pokhare</name></region><name sortKey="Elashry, Abdelnaser" sort="Elashry, Abdelnaser" uniqKey="Elashry A" first="Abdelnaser" last="Elashry">Abdelnaser Elashry</name><name sortKey="Grundler, Florian M W" sort="Grundler, Florian M W" uniqKey="Grundler F" first="Florian M W" last="Grundler">Florian M W. Grundler</name><name sortKey="Habash, Samer S" sort="Habash, Samer S" uniqKey="Habash S" first="Samer S" last="Habash">Samer S. Habash</name></country><country name="Inde"><noRegion><name sortKey="Pokhare, Somnath S" sort="Pokhare, Somnath S" uniqKey="Pokhare S" first="Somnath S" last="Pokhare">Somnath S. Pokhare</name></noRegion></country><country name="Royaume-Uni"><noRegion><name sortKey="Thorpe, Peter" sort="Thorpe, Peter" uniqKey="Thorpe P" first="Peter" last="Thorpe">Peter Thorpe</name></noRegion><name sortKey="Eves Van Den Akker, Sebastian" sort="Eves Van Den Akker, Sebastian" uniqKey="Eves Van Den Akker S" first="Sebastian" last="Eves-Van Den Akker">Sebastian Eves-Van Den Akker</name><name sortKey="Hedley, Pete" sort="Hedley, Pete" uniqKey="Hedley P" first="Pete" last="Hedley">Pete Hedley</name><name sortKey="Jones, John T" sort="Jones, John T" uniqKey="Jones J" first="John T" last="Jones">John T. Jones</name><name sortKey="Jones, John T" sort="Jones, John T" uniqKey="Jones J" first="John T" last="Jones">John T. Jones</name><name sortKey="Morris, Jennifer" sort="Morris, Jennifer" uniqKey="Morris J" first="Jennifer" last="Morris">Jennifer Morris</name><name sortKey="Thorpe, Peter" sort="Thorpe, Peter" uniqKey="Thorpe P" first="Peter" last="Thorpe">Peter Thorpe</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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