Pathogenomics Characterization of an Emerging Fungal Pathogen, Fusarium oxysporum f. sp. lycopersici in Greenhouse Tomato Production Systems.
Identifieur interne : 000088 ( Main/Exploration ); précédent : 000087; suivant : 000089Pathogenomics Characterization of an Emerging Fungal Pathogen, Fusarium oxysporum f. sp. lycopersici in Greenhouse Tomato Production Systems.
Auteurs : Tika B. Adhikari [États-Unis] ; Anne Gao [États-Unis] ; Thomas Ingram [États-Unis] ; Frank J. Louws [États-Unis]Source :
- Frontiers in microbiology [ 1664-302X ] ; 2020.
Abstract
In recent years, greenhouse-grown tomato (Solanum lycopersicum) plants showing vascular wilt and yellowing symptoms have been observed between 2015 and 2018 in North Carolina (NC) and considered as an emerging threat to profitability. In total, 38 putative isolates were collected from symptomatic tomatoes in 12 grower greenhouses and characterized to infer pathogenic and genomic diversity, and mating-type (MAT) idiomorphs distribution. Morphology and polymerase chain reaction (PCR) markers confirmed that all isolates were Fusarium oxysporum f. sp. lycopersici (FOL) and most of them were race 3. Virulence analysis on four different tomato cultivars revealed that virulence among isolates, resistance in tomato cultivars, and the interaction between the isolates and cultivars differed significantly (P < 0.001). Cultivar 'Happy Root' (I-1, I-2, and I-3 genes for resistance) was highly resistant to FOL isolates tested. We sequenced and examined for the presence of 15 pathogenicity genes from different classes (Fmk1, Fow1, Ftf1, Orx1, Pda1, PelA, PelD, Pep1, Pep2, eIF-3, Rho1, Scd1, Snf1, Ste12, and Sge1), and 14 Secreted In Xylem (SIX) genes to use as genetic markers to identify and differentiate pathogenic isolates of FOL. Sequence data analysis showed that five pathogenicity genes, Fmk1, PelA, Rho1, Sge1, and Ste12 were present in all isolates while Fow1, Ftf1, Orx1, Peda1, Pep1, eIF-3, Scd1, and Snf1 genes were dispersed among isolates. Two genes, Pep2 and PelD, were absent in all isolates. Of the 14 SIX genes assessed, SIX1, SIX3, SIX5, SIX6, SIX7, SIX8, SIX12, and SIX14 were identified in most isolates while the remaining SIX genes varied among isolates. All isolates harbored one of the two mating-type (MAT-1 or MAT-2) idiomorphs, but not both. The SIX4 gene was present only in race 1 isolates. Diversity assessments based on sequences of the effector SIX3- and the translation elongation factor 1-α encoding genes SIX3 and tef1-α, respectively were the most informative to differentiate pathogenic races of FOL and resulted in race 1, forming a monophyletic clade while race 3 comprised multiple clades. Furthermore, phylogeny-based on SIX3- and tef1-α gene sequences showed that the predominant race 3 from greenhouse production systems significantly overlapped with previously designated race 3 isolates from various regions of the globe.
DOI: 10.3389/fmicb.2020.01995
PubMed: 32973719
PubMed Central: PMC7482420
Affiliations:
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Adhikari</name><affiliation wicri:level="2"><nlm:affiliation>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation></author><author><name sortKey="Gao, Anne" sort="Gao, Anne" uniqKey="Gao A" first="Anne" last="Gao">Anne Gao</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Ingram, Thomas" sort="Ingram, Thomas" uniqKey="Ingram T" first="Thomas" last="Ingram">Thomas Ingram</name><affiliation wicri:level="2"><nlm:affiliation>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation></author><author><name sortKey="Louws, Frank J" sort="Louws, Frank J" uniqKey="Louws F" first="Frank J" last="Louws">Frank J. Louws</name><affiliation wicri:level="2"><nlm:affiliation>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Horticultural Science, North Carolina State University, Raleigh, NC, United States.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Horticultural Science, North Carolina State University, Raleigh, NC</wicri:regionArea><placeName><region type="state">Caroline du Nord</region></placeName></affiliation></author></analytic><series><title level="j">Frontiers in microbiology</title><idno type="ISSN">1664-302X</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">In recent years, greenhouse-grown tomato (<i>Solanum lycopersicum</i>) plants showing vascular wilt and yellowing symptoms have been observed between 2015 and 2018 in North Carolina (NC) and considered as an emerging threat to profitability. In total, 38 putative isolates were collected from symptomatic tomatoes in 12 grower greenhouses and characterized to infer pathogenic and genomic diversity, and mating-type (<i>MAT</i>) idiomorphs distribution. Morphology and polymerase chain reaction (PCR) markers confirmed that all isolates were <i>Fusarium oxysporum</i> f. sp. <i>lycopersici</i> (FOL) and most of them were race 3. Virulence analysis on four different tomato cultivars revealed that virulence among isolates, resistance in tomato cultivars, and the interaction between the isolates and cultivars differed significantly (<i>P</i> < 0.001). Cultivar 'Happy Root' (<i>I-1, I-2</i>, and <i>I-3</i> genes for resistance) was highly resistant to FOL isolates tested. We sequenced and examined for the presence of 15 pathogenicity genes from different classes (<i>Fmk1</i>, <i>Fow1</i>, <i>Ftf1</i>, <i>Orx1</i>, <i>Pda1</i>, <i>PelA</i>, <i>PelD, Pep1</i>, <i>Pep2</i>, <i>eIF-3</i>, <i>Rho1</i>, <i>Scd1</i>, <i>Snf1</i>, <i>Ste12</i>, and <i>Sge1</i>), and 14 <i>Secreted In Xylem</i> (<i>SIX</i>) genes to use as genetic markers to identify and differentiate pathogenic isolates of FOL. Sequence data analysis showed that five pathogenicity genes, <i>Fmk1, PelA</i>, <i>Rho1</i>, <i>Sge1</i>, and <i>Ste12</i> were present in all isolates while <i>Fow1</i>, <i>Ftf1</i>, <i>Orx1</i>, <i>Peda1</i>, <i>Pep1</i>, <i>eIF-3</i>, <i>Scd1</i>, and <i>Snf1</i> genes were dispersed among isolates. Two genes, <i>Pep2</i> and <i>PelD</i>, were absent in all isolates. Of the 14 <i>SIX</i> genes assessed, <i>SIX1, SIX3, SIX5, SIX6, SIX7, SIX8, SIX12</i>, and <i>SIX14</i> were identified in most isolates while the remaining <i>SIX</i> genes varied among isolates. All isolates harbored one of the two mating-type (<i>MAT-1</i> or <i>MAT-2</i>) idiomorphs, but not both. The <i>SIX4</i> gene was present only in race 1 isolates. Diversity assessments based on sequences of the effector SIX3<i>-</i> and the translation elongation factor 1-α encoding genes <i>SIX3</i> and <i>tef1-</i>α, respectively were the most informative to differentiate pathogenic races of FOL and resulted in race 1, forming a monophyletic clade while race 3 comprised multiple clades. Furthermore, phylogeny-based on <i>SIX3-</i> and <i>tef1-</i>α gene sequences showed that the predominant race 3 from greenhouse production systems significantly overlapped with previously designated race 3 isolates from various regions of the globe.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32973719</PMID><DateRevised><Year>2020</Year><Month>09</Month><Day>28</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Print">1664-302X</ISSN><JournalIssue CitedMedium="Print"><Volume>11</Volume><PubDate><Year>2020</Year></PubDate></JournalIssue><Title>Frontiers in microbiology</Title><ISOAbbreviation>Front Microbiol</ISOAbbreviation></Journal><ArticleTitle>Pathogenomics Characterization of an Emerging Fungal Pathogen, <i>Fusarium oxysporum</i> f. sp. <i>lycopersici</i> in Greenhouse Tomato Production Systems.</ArticleTitle><Pagination><MedlinePgn>1995</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.3389/fmicb.2020.01995</ELocationID><Abstract><AbstractText>In recent years, greenhouse-grown tomato (<i>Solanum lycopersicum</i>) plants showing vascular wilt and yellowing symptoms have been observed between 2015 and 2018 in North Carolina (NC) and considered as an emerging threat to profitability. In total, 38 putative isolates were collected from symptomatic tomatoes in 12 grower greenhouses and characterized to infer pathogenic and genomic diversity, and mating-type (<i>MAT</i>) idiomorphs distribution. Morphology and polymerase chain reaction (PCR) markers confirmed that all isolates were <i>Fusarium oxysporum</i> f. sp. <i>lycopersici</i> (FOL) and most of them were race 3. Virulence analysis on four different tomato cultivars revealed that virulence among isolates, resistance in tomato cultivars, and the interaction between the isolates and cultivars differed significantly (<i>P</i> < 0.001). Cultivar 'Happy Root' (<i>I-1, I-2</i>, and <i>I-3</i> genes for resistance) was highly resistant to FOL isolates tested. We sequenced and examined for the presence of 15 pathogenicity genes from different classes (<i>Fmk1</i>, <i>Fow1</i>, <i>Ftf1</i>, <i>Orx1</i>, <i>Pda1</i>, <i>PelA</i>, <i>PelD, Pep1</i>, <i>Pep2</i>, <i>eIF-3</i>, <i>Rho1</i>, <i>Scd1</i>, <i>Snf1</i>, <i>Ste12</i>, and <i>Sge1</i>), and 14 <i>Secreted In Xylem</i> (<i>SIX</i>) genes to use as genetic markers to identify and differentiate pathogenic isolates of FOL. Sequence data analysis showed that five pathogenicity genes, <i>Fmk1, PelA</i>, <i>Rho1</i>, <i>Sge1</i>, and <i>Ste12</i> were present in all isolates while <i>Fow1</i>, <i>Ftf1</i>, <i>Orx1</i>, <i>Peda1</i>, <i>Pep1</i>, <i>eIF-3</i>, <i>Scd1</i>, and <i>Snf1</i> genes were dispersed among isolates. Two genes, <i>Pep2</i> and <i>PelD</i>, were absent in all isolates. Of the 14 <i>SIX</i> genes assessed, <i>SIX1, SIX3, SIX5, SIX6, SIX7, SIX8, SIX12</i>, and <i>SIX14</i> were identified in most isolates while the remaining <i>SIX</i> genes varied among isolates. All isolates harbored one of the two mating-type (<i>MAT-1</i> or <i>MAT-2</i>) idiomorphs, but not both. The <i>SIX4</i> gene was present only in race 1 isolates. Diversity assessments based on sequences of the effector SIX3<i>-</i> and the translation elongation factor 1-α encoding genes <i>SIX3</i> and <i>tef1-</i>α, respectively were the most informative to differentiate pathogenic races of FOL and resulted in race 1, forming a monophyletic clade while race 3 comprised multiple clades. Furthermore, phylogeny-based on <i>SIX3-</i> and <i>tef1-</i>α gene sequences showed that the predominant race 3 from greenhouse production systems significantly overlapped with previously designated race 3 isolates from various regions of the globe.</AbstractText><CopyrightInformation>Copyright © 2020 Adhikari, Gao, Ingram and Louws.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Adhikari</LastName><ForeName>Tika B</ForeName><Initials>TB</Initials><AffiliationInfo><Affiliation>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gao</LastName><ForeName>Anne</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles, Los Angeles, CA, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ingram</LastName><ForeName>Thomas</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Louws</LastName><ForeName>Frank J</ForeName><Initials>FJ</Initials><AffiliationInfo><Affiliation>Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, NC, United States.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Horticultural Science, North Carolina State University, Raleigh, NC, United States.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>08</Month><Day>27</Day></ArticleDate></Article><MedlineJournalInfo><Country>Switzerland</Country><MedlineTA>Front Microbiol</MedlineTA><NlmUniqueID>101548977</NlmUniqueID><ISSNLinking>1664-302X</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Fusarium oxysporum f. sp. lycopersici</Keyword><Keyword MajorTopicYN="N">Fusarium wilt</Keyword><Keyword MajorTopicYN="N">SIX genes</Keyword><Keyword MajorTopicYN="N">fungal effectors</Keyword><Keyword MajorTopicYN="N">genetic diversity</Keyword><Keyword MajorTopicYN="N">host resistance</Keyword><Keyword MajorTopicYN="N">tomato (Solanum lycopersicum)</Keyword><Keyword MajorTopicYN="N">virulence</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>05</Month><Day>12</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>07</Month><Day>28</Day></PubMedPubDate><PubMedPubDate 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