A new esophageal gland transcriptome reveals signatures of large scale de novo effector birth in the root lesion nematode Pratylenchus penetrans.
Identifieur interne : 000230 ( Main/Exploration ); précédent : 000229; suivant : 000231A new esophageal gland transcriptome reveals signatures of large scale de novo effector birth in the root lesion nematode Pratylenchus penetrans.
Auteurs : Paulo Vieira [États-Unis] ; Jonathan Shao [États-Unis] ; Paramasivan Vijayapalani [États-Unis] ; Thomas R. Maier [États-Unis] ; Clement Pellegrin [Royaume-Uni] ; Sebastian Eves-Van Den Akker [Royaume-Uni] ; Thomas J. Baum [États-Unis] ; Lev G. Nemchinov [États-Unis]Source :
- BMC genomics [ 1471-2164 ] ; 2020.
Abstract
BACKGROUND
The root lesion nematode Pratylenchus penetrans is a migratory plant-parasitic nematode responsible for economically important losses in a wide number of crops. Despite the importance of P. penetrans, the molecular mechanisms employed by this nematode to promote virulence remain largely unknown.
RESULTS
Here we generated a new and comprehensive esophageal glands-specific transcriptome library for P. penetrans. In-depth analysis of this transcriptome enabled a robust identification of a catalogue of 30 new candidate effector genes, which were experimentally validated in the esophageal glands by in situ hybridization. We further validated the expression of a multifaceted network of candidate effectors during the interaction with different plants. To advance our understanding of the "effectorome" of P. penetrans, we adopted a phylogenetic approach and compared the expanded effector repertoire of P. penetrans to the genome/transcriptome of other nematode species with similar or contrasting parasitism strategies. Our data allowed us to infer plausible evolutionary histories that shaped the effector repertoire of P. penetrans, as well as other close and distant plant-parasitic nematodes. Two remarkable trends were apparent: 1) large scale effector birth in the Pratylenchidae in general and P. penetrans in particular, and 2) large scale effector death in sedentary (endo) plant-parasitic nematodes.
CONCLUSIONS
Our study doubles the number of validated Pratylenchus penetrans effectors reported in the literature. The dramatic effector gene gain in P. penetrans could be related to the remarkable ability of this nematode to parasitize a large number of plants. Our data provide valuable insights into nematode parasitism and contribute towards basic understating of the adaptation of P. penetrans and other root lesion nematodes to specific host plants.
DOI: 10.1186/s12864-020-07146-0
PubMed: 33096989
PubMed Central: PMC7585316
Affiliations:
- Royaume-Uni, États-Unis
- Angleterre, Angleterre de l'Est, Iowa
- Ames (Iowa), Cambridge
- Université d'État de l'Iowa, Université de Cambridge
Links toward previous steps (curation, corpus...)
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Maier</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011</wicri:regionArea><orgName type="university">Université d'État de l'Iowa</orgName><placeName><settlement type="city">Ames (Iowa)</settlement><region type="state">Iowa</region></placeName></affiliation></author><author><name sortKey="Pellegrin, Clement" sort="Pellegrin, Clement" uniqKey="Pellegrin C" first="Clement" last="Pellegrin">Clement Pellegrin</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Plant Sciences, University of Cambridge, Cambridge</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="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, UK.</nlm:affiliation><country xml:lang="fr">Royaume-Uni</country><wicri:regionArea>Department of Plant Sciences, University of Cambridge, Cambridge</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="Baum, Thomas J" sort="Baum, Thomas J" uniqKey="Baum T" first="Thomas J" last="Baum">Thomas J. Baum</name><affiliation wicri:level="4"><nlm:affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011</wicri:regionArea><orgName type="university">Université d'État de l'Iowa</orgName><placeName><settlement type="city">Ames (Iowa)</settlement><region type="state">Iowa</region></placeName></affiliation></author><author><name sortKey="Nemchinov, Lev G" sort="Nemchinov, Lev G" uniqKey="Nemchinov L" first="Lev G" last="Nemchinov">Lev G. Nemchinov</name><affiliation wicri:level="1"><nlm:affiliation>USDA-ARS, Molecular Plant Pathology Laboratory, Beltsville, MD, 20705-2350, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>USDA-ARS, Molecular Plant Pathology Laboratory, Beltsville, MD, 20705-2350</wicri:regionArea><wicri:noRegion>20705-2350</wicri:noRegion></affiliation></author></analytic><series><title level="j">BMC genomics</title><idno type="eISSN">1471-2164</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"><p><b>BACKGROUND</b></p><p>The root lesion nematode Pratylenchus penetrans is a migratory plant-parasitic nematode responsible for economically important losses in a wide number of crops. Despite the importance of P. penetrans, the molecular mechanisms employed by this nematode to promote virulence remain largely unknown.</p></div><div type="abstract" xml:lang="en"><p><b>RESULTS</b></p><p>Here we generated a new and comprehensive esophageal glands-specific transcriptome library for P. penetrans. In-depth analysis of this transcriptome enabled a robust identification of a catalogue of 30 new candidate effector genes, which were experimentally validated in the esophageal glands by in situ hybridization. We further validated the expression of a multifaceted network of candidate effectors during the interaction with different plants. To advance our understanding of the "effectorome" of P. penetrans, we adopted a phylogenetic approach and compared the expanded effector repertoire of P. penetrans to the genome/transcriptome of other nematode species with similar or contrasting parasitism strategies. Our data allowed us to infer plausible evolutionary histories that shaped the effector repertoire of P. penetrans, as well as other close and distant plant-parasitic nematodes. Two remarkable trends were apparent: 1) large scale effector birth in the Pratylenchidae in general and P. penetrans in particular, and 2) large scale effector death in sedentary (endo) plant-parasitic nematodes.</p></div><div type="abstract" xml:lang="en"><p><b>CONCLUSIONS</b></p><p>Our study doubles the number of validated Pratylenchus penetrans effectors reported in the literature. The dramatic effector gene gain in P. penetrans could be related to the remarkable ability of this nematode to parasitize a large number of plants. Our data provide valuable insights into nematode parasitism and contribute towards basic understating of the adaptation of P. penetrans and other root lesion nematodes to specific host plants.</p></div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">33096989</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>27</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">1471-2164</ISSN><JournalIssue CitedMedium="Internet"><Volume>21</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>Oct</Month><Day>23</Day></PubDate></JournalIssue><Title>BMC genomics</Title><ISOAbbreviation>BMC Genomics</ISOAbbreviation></Journal><ArticleTitle>A new esophageal gland transcriptome reveals signatures of large scale de novo effector birth in the root lesion nematode Pratylenchus penetrans.</ArticleTitle><Pagination><MedlinePgn>738</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1186/s12864-020-07146-0</ELocationID><Abstract><AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">The root lesion nematode Pratylenchus penetrans is a migratory plant-parasitic nematode responsible for economically important losses in a wide number of crops. Despite the importance of P. penetrans, the molecular mechanisms employed by this nematode to promote virulence remain largely unknown.</AbstractText><AbstractText Label="RESULTS" NlmCategory="RESULTS">Here we generated a new and comprehensive esophageal glands-specific transcriptome library for P. penetrans. In-depth analysis of this transcriptome enabled a robust identification of a catalogue of 30 new candidate effector genes, which were experimentally validated in the esophageal glands by in situ hybridization. We further validated the expression of a multifaceted network of candidate effectors during the interaction with different plants. To advance our understanding of the "effectorome" of P. penetrans, we adopted a phylogenetic approach and compared the expanded effector repertoire of P. penetrans to the genome/transcriptome of other nematode species with similar or contrasting parasitism strategies. Our data allowed us to infer plausible evolutionary histories that shaped the effector repertoire of P. penetrans, as well as other close and distant plant-parasitic nematodes. Two remarkable trends were apparent: 1) large scale effector birth in the Pratylenchidae in general and P. penetrans in particular, and 2) large scale effector death in sedentary (endo) plant-parasitic nematodes.</AbstractText><AbstractText Label="CONCLUSIONS" NlmCategory="CONCLUSIONS">Our study doubles the number of validated Pratylenchus penetrans effectors reported in the literature. The dramatic effector gene gain in P. penetrans could be related to the remarkable ability of this nematode to parasitize a large number of plants. Our data provide valuable insights into nematode parasitism and contribute towards basic understating of the adaptation of P. penetrans and other root lesion nematodes to specific host plants.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Vieira</LastName><ForeName>Paulo</ForeName><Initials>P</Initials><Identifier Source="ORCID">http://orcid.org/0000-0001-5627-2628</Identifier><AffiliationInfo><Affiliation>USDA-ARS, Molecular Plant Pathology Laboratory, Beltsville, MD, 20705-2350, USA. pvieira@vt.edu.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>School of Plant and Environmental Science, Virginia Tech, Blacksburg, VA, 24061, USA. pvieira@vt.edu.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shao</LastName><ForeName>Jonathan</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>USDA-ARS, Molecular Plant Pathology Laboratory, Beltsville, MD, 20705-2350, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Vijayapalani</LastName><ForeName>Paramasivan</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Maier</LastName><ForeName>Thomas R</ForeName><Initials>TR</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pellegrin</LastName><ForeName>Clement</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>Department of Plant Sciences, University of Cambridge, Cambridge, UK.</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, UK.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Baum</LastName><ForeName>Thomas J</ForeName><Initials>TJ</Initials><AffiliationInfo><Affiliation>Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, 50011, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Nemchinov</LastName><ForeName>Lev G</ForeName><Initials>LG</Initials><AffiliationInfo><Affiliation>USDA-ARS, Molecular Plant Pathology Laboratory, Beltsville, MD, 20705-2350, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><GrantList CompleteYN="Y"><Grant><GrantID>8042-21000-300-00D</GrantID><Agency>Agricultural Research Service</Agency><Country></Country></Grant><Grant><GrantID>125034/359149/3</GrantID><Agency>Department for Environment, Food and Rural Affairs</Agency><Country></Country></Grant><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>MSCA-IF-EF-ST-882941-NEMABOX</GrantID><Agency>H2020 Marie Skłodowska-Curie Actions</Agency><Country></Country></Grant></GrantList><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>10</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>BMC Genomics</MedlineTA><NlmUniqueID>100965258</NlmUniqueID><ISSNLinking>1471-2164</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">Esophageal gland cells</Keyword><Keyword MajorTopicYN="N">Host-pathogen interaction</Keyword><Keyword MajorTopicYN="N">Pioneer 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first="Paulo" last="Vieira">Paulo Vieira</name></noRegion><name sortKey="Baum, Thomas J" sort="Baum, Thomas J" uniqKey="Baum T" first="Thomas J" last="Baum">Thomas J. Baum</name><name sortKey="Maier, Thomas R" sort="Maier, Thomas R" uniqKey="Maier T" first="Thomas R" last="Maier">Thomas R. Maier</name><name sortKey="Nemchinov, Lev G" sort="Nemchinov, Lev G" uniqKey="Nemchinov L" first="Lev G" last="Nemchinov">Lev G. 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