Host Range Determinants of Pseudomonas savastanoi Pathovars of Woody Hosts Revealed by Comparative Genomics and Cross-Pathogenicity Tests.
Identifieur interne : 000140 ( Main/Exploration ); précédent : 000139; suivant : 000141Host Range Determinants of Pseudomonas savastanoi Pathovars of Woody Hosts Revealed by Comparative Genomics and Cross-Pathogenicity Tests.
Auteurs : Alba Moreno-Pérez [Espagne] ; Adrián Pintado [Espagne] ; Jesús Murillo [Espagne] ; Eloy Caballo-Ponce [Espagne] ; Stefania Tegli [Italie] ; Chiaraluce Moretti [Italie] ; Pablo Rodríguez-Palenzuela [Espagne] ; Cayo Ramos [Espagne]Source :
- Frontiers in plant science [ 1664-462X ] ; 2020.
Abstract
The study of host range determinants within the Pseudomonas syringae complex is gaining renewed attention due to its widespread distribution in non-agricultural environments, evidence of large variability in intra-pathovar host range, and the emergence of new epidemic diseases. This requires the establishment of appropriate model pathosystems facilitating integration of phenotypic, genomic and evolutionary data. Pseudomonas savastanoi pv. savastanoi is a model pathogen of the olive tree, and here we report a closed genome of strain NCPPB 3335, plus draft genome sequences of three strains isolated from oleander (pv. nerii), ash (pv. fraxini) and broom plants (pv. retacarpa). We then conducted a comparative genomic analysis of these four new genomes plus 16 publicly available genomes, representing 20 strains of these four P. savastanoi pathovars of woody hosts. Despite overlapping host ranges, cross-pathogenicity tests using four plant hosts clearly separated these pathovars and lead to pathovar reassignment of two strains. Critically, these functional assays were pivotal to reconcile phylogeny with host range and to define pathovar-specific genes repertoires. We report a pan-genome of 7,953 ortholog gene families and a total of 45 type III secretion system effector genes, including 24 core genes, four genes exclusive of pv. retacarpa and several genes encoding pathovar-specific truncations. Noticeably, the four pathovars corresponded with well-defined genetic lineages, with core genome phylogeny and hierarchical clustering of effector genes closely correlating with pathogenic specialization. Knot-inducing pathovars encode genes absent in the canker-inducing pv. fraxini, such as those related to indole acetic acid, cytokinins, rhizobitoxine, and a bacteriophytochrome. Other pathovar-exclusive genes encode type I, type II, type IV, and type VI secretion system proteins, the phytotoxine phevamine A, a siderophore, c-di-GMP-related proteins, methyl chemotaxis proteins, and a broad collection of transcriptional regulators and transporters of eight different superfamilies. Our combination of pathogenicity analyses and genomics tools allowed us to correctly assign strains to pathovars and to propose a repertoire of host range-related genes in the P. syringae complex.
DOI: 10.3389/fpls.2020.00973
PubMed: 32714356
PubMed Central: PMC7343908
Affiliations:
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Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga</wicri:regionArea><orgName type="university">Université de Malaga</orgName><placeName><settlement type="city">Malaga</settlement><region nuts="2" type="region">Andalousie</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga</wicri:regionArea><wicri:noRegion>Málaga</wicri:noRegion></affiliation></author><author><name sortKey="Pintado, Adrian" sort="Pintado, Adrian" uniqKey="Pintado A" first="Adrián" last="Pintado">Adrián Pintado</name><affiliation wicri:level="4"><nlm:affiliation>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga</wicri:regionArea><orgName type="university">Université de Malaga</orgName><placeName><settlement type="city">Malaga</settlement><region nuts="2" type="region">Andalousie</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga</wicri:regionArea><wicri:noRegion>Málaga</wicri:noRegion></affiliation></author><author><name sortKey="Murillo, Jesus" sort="Murillo, Jesus" uniqKey="Murillo J" first="Jesús" last="Murillo">Jesús Murillo</name><affiliation wicri:level="1"><nlm:affiliation>Institute for Multidisciplinary Research in Applied Biology, Universidad Pública de Navarra, Mutilva Baja, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Institute for Multidisciplinary Research in Applied Biology, Universidad Pública de Navarra, Mutilva Baja</wicri:regionArea><wicri:noRegion>Mutilva Baja</wicri:noRegion></affiliation></author><author><name sortKey="Caballo Ponce, Eloy" sort="Caballo Ponce, Eloy" uniqKey="Caballo Ponce E" first="Eloy" last="Caballo-Ponce">Eloy Caballo-Ponce</name><affiliation wicri:level="4"><nlm:affiliation>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga</wicri:regionArea><orgName type="university">Université de Malaga</orgName><placeName><settlement type="city">Malaga</settlement><region nuts="2" type="region">Andalousie</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga</wicri:regionArea><wicri:noRegion>Málaga</wicri:noRegion></affiliation></author><author><name sortKey="Tegli, Stefania" sort="Tegli, Stefania" uniqKey="Tegli S" first="Stefania" last="Tegli">Stefania Tegli</name><affiliation wicri:level="1"><nlm:affiliation>Dipartimento di Scienze e Tecnologie Agrarie, Alimentari Ambientali e Forestali (DAGRI), Laboratorio di Patologia Vegetale Molecolare, University of Florence, Firenze, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Dipartimento di Scienze e Tecnologie Agrarie, Alimentari Ambientali e Forestali (DAGRI), Laboratorio di Patologia Vegetale Molecolare, University of Florence, Firenze</wicri:regionArea><wicri:noRegion>Firenze</wicri:noRegion></affiliation></author><author><name sortKey="Moretti, Chiaraluce" sort="Moretti, Chiaraluce" uniqKey="Moretti C" first="Chiaraluce" last="Moretti">Chiaraluce Moretti</name><affiliation wicri:level="1"><nlm:affiliation>Department of Agricultural, Food and Environmental Science, University of Perugia, Perugia, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Agricultural, Food and Environmental Science, University of Perugia, Perugia</wicri:regionArea><wicri:noRegion>Perugia</wicri:noRegion></affiliation></author><author><name sortKey="Rodriguez Palenzuela, Pablo" sort="Rodriguez Palenzuela, Pablo" uniqKey="Rodriguez Palenzuela P" first="Pablo" last="Rodríguez-Palenzuela">Pablo Rodríguez-Palenzuela</name><affiliation wicri:level="3"><nlm:affiliation>Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation><affiliation wicri:level="3"><nlm:affiliation>Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, UPM, Madrid, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, UPM, Madrid</wicri:regionArea><placeName><settlement type="city">Madrid</settlement><region nuts="2" type="region">Communauté de Madrid</region></placeName></affiliation></author><author><name sortKey="Ramos, Cayo" sort="Ramos, Cayo" uniqKey="Ramos C" first="Cayo" last="Ramos">Cayo Ramos</name><affiliation wicri:level="4"><nlm:affiliation>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga</wicri:regionArea><orgName type="university">Université de Malaga</orgName><placeName><settlement type="city">Malaga</settlement><region nuts="2" type="region">Andalousie</region></placeName></affiliation><affiliation wicri:level="1"><nlm:affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga</wicri:regionArea><wicri:noRegion>Málaga</wicri:noRegion></affiliation></author></analytic><series><title level="j">Frontiers in plant science</title><idno type="ISSN">1664-462X</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">The study of host range determinants within the <i>Pseudomonas syringae</i> complex is gaining renewed attention due to its widespread distribution in non-agricultural environments, evidence of large variability in intra-pathovar host range, and the emergence of new epidemic diseases. This requires the establishment of appropriate model pathosystems facilitating integration of phenotypic, genomic and evolutionary data. <i>Pseudomonas savastanoi</i> pv. savastanoi is a model pathogen of the olive tree, and here we report a closed genome of strain NCPPB 3335, plus draft genome sequences of three strains isolated from oleander (pv. nerii), ash (pv. fraxini) and broom plants (pv. retacarpa). We then conducted a comparative genomic analysis of these four new genomes plus 16 publicly available genomes, representing 20 strains of these four <i>P. savastanoi</i> pathovars of woody hosts. Despite overlapping host ranges, cross-pathogenicity tests using four plant hosts clearly separated these pathovars and lead to pathovar reassignment of two strains. Critically, these functional assays were pivotal to reconcile phylogeny with host range and to define pathovar-specific genes repertoires. We report a pan-genome of 7,953 ortholog gene families and a total of 45 type III secretion system effector genes, including 24 core genes, four genes exclusive of pv. retacarpa and several genes encoding pathovar-specific truncations. Noticeably, the four pathovars corresponded with well-defined genetic lineages, with core genome phylogeny and hierarchical clustering of effector genes closely correlating with pathogenic specialization. Knot-inducing pathovars encode genes absent in the canker-inducing pv. fraxini, such as those related to indole acetic acid, cytokinins, rhizobitoxine, and a bacteriophytochrome. Other pathovar-exclusive genes encode type I, type II, type IV, and type VI secretion system proteins, the phytotoxine phevamine A, a siderophore, c-di-GMP-related proteins, methyl chemotaxis proteins, and a broad collection of transcriptional regulators and transporters of eight different superfamilies. Our combination of pathogenicity analyses and genomics tools allowed us to correctly assign strains to pathovars and to propose a repertoire of host range-related genes in the <i>P. syringae</i> complex.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32714356</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-462X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in plant science</Title><ISOAbbreviation>Front Plant Sci</ISOAbbreviation></Journal><ArticleTitle>Host Range Determinants of <i>Pseudomonas savastanoi</i> Pathovars of Woody Hosts Revealed by Comparative Genomics and Cross-Pathogenicity Tests.</ArticleTitle><Pagination><MedlinePgn>973</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fpls.2020.00973</ELocationID><Abstract><AbstractText>The study of host range determinants within the <i>Pseudomonas syringae</i> complex is gaining renewed attention due to its widespread distribution in non-agricultural environments, evidence of large variability in intra-pathovar host range, and the emergence of new epidemic diseases. This requires the establishment of appropriate model pathosystems facilitating integration of phenotypic, genomic and evolutionary data. <i>Pseudomonas savastanoi</i> pv. savastanoi is a model pathogen of the olive tree, and here we report a closed genome of strain NCPPB 3335, plus draft genome sequences of three strains isolated from oleander (pv. nerii), ash (pv. fraxini) and broom plants (pv. retacarpa). We then conducted a comparative genomic analysis of these four new genomes plus 16 publicly available genomes, representing 20 strains of these four <i>P. savastanoi</i> pathovars of woody hosts. Despite overlapping host ranges, cross-pathogenicity tests using four plant hosts clearly separated these pathovars and lead to pathovar reassignment of two strains. Critically, these functional assays were pivotal to reconcile phylogeny with host range and to define pathovar-specific genes repertoires. We report a pan-genome of 7,953 ortholog gene families and a total of 45 type III secretion system effector genes, including 24 core genes, four genes exclusive of pv. retacarpa and several genes encoding pathovar-specific truncations. Noticeably, the four pathovars corresponded with well-defined genetic lineages, with core genome phylogeny and hierarchical clustering of effector genes closely correlating with pathogenic specialization. Knot-inducing pathovars encode genes absent in the canker-inducing pv. fraxini, such as those related to indole acetic acid, cytokinins, rhizobitoxine, and a bacteriophytochrome. Other pathovar-exclusive genes encode type I, type II, type IV, and type VI secretion system proteins, the phytotoxine phevamine A, a siderophore, c-di-GMP-related proteins, methyl chemotaxis proteins, and a broad collection of transcriptional regulators and transporters of eight different superfamilies. Our combination of pathogenicity analyses and genomics tools allowed us to correctly assign strains to pathovars and to propose a repertoire of host range-related genes in the <i>P. syringae</i> complex.</AbstractText><CopyrightInformation>Copyright © 2020 Moreno-Pérez, Pintado, Murillo, Caballo-Ponce, Tegli, Moretti, Rodríguez-Palenzuela and Ramos.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Moreno-Pérez</LastName><ForeName>Alba</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pintado</LastName><ForeName>Adrián</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Murillo</LastName><ForeName>Jesús</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Institute for Multidisciplinary Research in Applied Biology, Universidad Pública de Navarra, Mutilva Baja, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Caballo-Ponce</LastName><ForeName>Eloy</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tegli</LastName><ForeName>Stefania</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Dipartimento di Scienze e Tecnologie Agrarie, Alimentari Ambientali e Forestali (DAGRI), Laboratorio di Patologia Vegetale Molecolare, University of Florence, Firenze, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Moretti</LastName><ForeName>Chiaraluce</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Agricultural, Food and Environmental Science, University of Perugia, Perugia, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rodríguez-Palenzuela</LastName><ForeName>Pablo</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Centro de Biotecnología y Genómica de Plantas, Universidad Politécnica de Madrid (UPM)-Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Madrid, Spain.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Departamento de Biotecnología-Biología Vegetal, Escuela Técnica Superior de Ingeniería Agronómica, Alimentaria y de Biosistemas, UPM, Madrid, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ramos</LastName><ForeName>Cayo</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Área de Genética, Facultad de Ciencias, Universidad de Málaga, Málaga, Spain.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Instituto de Hortofruticultura Subtropical y Mediterránea "La Mayora", Consejo Superior de Investigaciones Científicas (IHSM-UMA-CSIC), Málaga, Spain.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>07</Month><Day>02</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Plant Sci</MedlineTA><NlmUniqueID>101568200</NlmUniqueID><ISSNLinking>1664-462X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Pseudomonas savastanoi pathovars</Keyword><Keyword MajorTopicYN="N">Pseudomonas syringae</Keyword><Keyword MajorTopicYN="N">comparative genomics</Keyword><Keyword MajorTopicYN="N">host range</Keyword><Keyword MajorTopicYN="N">phytotoxins</Keyword><Keyword MajorTopicYN="N">type III effectors</Keyword><Keyword MajorTopicYN="N">virulence factors</Keyword><Keyword MajorTopicYN="N">woody hosts</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate 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