Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici.
Identifieur interne : 000594 ( Main/Corpus ); précédent : 000593; suivant : 000595Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici.
Auteurs : Sajid Ali ; Pierre Gladieux ; Marc Leconte ; Angélique Gautier ; Annemarie F. Justesen ; Mogens S. Hovm Ller ; Jérôme Enjalbert ; Claude De Vallavieille-PopeSource :
- PLoS pathogens [ 1553-7374 ] ; 2014.
English descriptors
- KwdEn :
- MESH :
- genetics : Basidiomycota, Plant Diseases.
- microbiology : Plant Diseases, Triticum.
- Genetic Variation, Genotype, Humans, Microsatellite Repeats.
Abstract
Analyses of large-scale population structure of pathogens enable the identification of migration patterns, diversity reservoirs or longevity of populations, the understanding of current evolutionary trajectories and the anticipation of future ones. This is particularly important for long-distance migrating fungal pathogens such as Puccinia striiformis f.sp. tritici (PST), capable of rapid spread to new regions and crop varieties. Although a range of recent PST invasions at continental scales are well documented, the worldwide population structure and the center of origin of the pathogen were still unknown. In this study, we used multilocus microsatellite genotyping to infer worldwide population structure of PST and the origin of new invasions based on 409 isolates representative of distribution of the fungus on six continents. Bayesian and multivariate clustering methods partitioned the set of multilocus genotypes into six distinct genetic groups associated with their geographical origin. Analyses of linkage disequilibrium and genotypic diversity indicated a strong regional heterogeneity in levels of recombination, with clear signatures of recombination in the Himalayan (Nepal and Pakistan) and near-Himalayan regions (China) and a predominant clonal population structure in other regions. The higher genotypic diversity, recombinant population structure and high sexual reproduction ability in the Himalayan and neighboring regions suggests this area as the putative center of origin of PST. We used clustering methods and approximate Bayesian computation (ABC) to compare different competing scenarios describing ancestral relationship among ancestral populations and more recently founded populations. Our analyses confirmed the Middle East-East Africa as the most likely source of newly spreading, high-temperature-adapted strains; Europe as the source of South American, North American and Australian populations; and Mediterranean-Central Asian populations as the origin of South African populations. Although most geographic populations are not markedly affected by recent dispersal events, this study emphasizes the influence of human activities on recent long-distance spread of the pathogen.
DOI: 10.1371/journal.ppat.1003903
PubMed: 24465211
PubMed Central: PMC3900651
Links to Exploration step
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Paris-Sud., CNRS-F, Orsay, France ; Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, United States of America.</nlm:affiliation></affiliation></author><author><name sortKey="Leconte, Marc" sort="Leconte, Marc" uniqKey="Leconte M" first="Marc" last="Leconte">Marc Leconte</name><affiliation><nlm:affiliation>INRA UR 1290 BIOGER-CPP, Thiverval-Grignon, France.</nlm:affiliation></affiliation></author><author><name sortKey="Gautier, Angelique" sort="Gautier, Angelique" uniqKey="Gautier A" first="Angélique" last="Gautier">Angélique Gautier</name><affiliation><nlm:affiliation>INRA UR 1290 BIOGER-CPP, Thiverval-Grignon, France.</nlm:affiliation></affiliation></author><author><name sortKey="Justesen, Annemarie F" sort="Justesen, Annemarie F" uniqKey="Justesen A" first="Annemarie F" last="Justesen">Annemarie F. Justesen</name><affiliation><nlm:affiliation>Department of Agroecology, Aarhus University, Slagelse, Denmark.</nlm:affiliation></affiliation></author><author><name sortKey="Hovm Ller, Mogens S" sort="Hovm Ller, Mogens S" uniqKey="Hovm Ller M" first="Mogens S" last="Hovm Ller">Mogens S. Hovm Ller</name><affiliation><nlm:affiliation>Department of Agroecology, Aarhus University, Slagelse, Denmark.</nlm:affiliation></affiliation></author><author><name sortKey="Enjalbert, Jerome" sort="Enjalbert, Jerome" uniqKey="Enjalbert J" first="Jérôme" last="Enjalbert">Jérôme Enjalbert</name><affiliation><nlm:affiliation>INRA UMR 320 Génétique Végétale, Ferme du Moulon, Gif sur Yvette, France.</nlm:affiliation></affiliation></author><author><name sortKey="De Vallavieille Pope, Claude" sort="De Vallavieille Pope, Claude" uniqKey="De Vallavieille Pope C" first="Claude" last="De Vallavieille-Pope">Claude De Vallavieille-Pope</name><affiliation><nlm:affiliation>INRA UR 1290 BIOGER-CPP, Thiverval-Grignon, France.</nlm:affiliation></affiliation></author></analytic><series><title level="j">PLoS pathogens</title><idno type="eISSN">1553-7374</idno><imprint><date when="2014" type="published">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Basidiomycota (genetics)</term><term>Genetic Variation (MeSH)</term><term>Genotype (MeSH)</term><term>Humans (MeSH)</term><term>Microsatellite Repeats (MeSH)</term><term>Plant Diseases (genetics)</term><term>Plant Diseases (microbiology)</term><term>Triticum (microbiology)</term></keywords><keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Basidiomycota</term><term>Plant Diseases</term></keywords><keywords scheme="MESH" qualifier="microbiology" xml:lang="en"><term>Plant Diseases</term><term>Triticum</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Genetic Variation</term><term>Genotype</term><term>Humans</term><term>Microsatellite Repeats</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Analyses of large-scale population structure of pathogens enable the identification of migration patterns, diversity reservoirs or longevity of populations, the understanding of current evolutionary trajectories and the anticipation of future ones. This is particularly important for long-distance migrating fungal pathogens such as Puccinia striiformis f.sp. tritici (PST), capable of rapid spread to new regions and crop varieties. Although a range of recent PST invasions at continental scales are well documented, the worldwide population structure and the center of origin of the pathogen were still unknown. In this study, we used multilocus microsatellite genotyping to infer worldwide population structure of PST and the origin of new invasions based on 409 isolates representative of distribution of the fungus on six continents. Bayesian and multivariate clustering methods partitioned the set of multilocus genotypes into six distinct genetic groups associated with their geographical origin. Analyses of linkage disequilibrium and genotypic diversity indicated a strong regional heterogeneity in levels of recombination, with clear signatures of recombination in the Himalayan (Nepal and Pakistan) and near-Himalayan regions (China) and a predominant clonal population structure in other regions. The higher genotypic diversity, recombinant population structure and high sexual reproduction ability in the Himalayan and neighboring regions suggests this area as the putative center of origin of PST. We used clustering methods and approximate Bayesian computation (ABC) to compare different competing scenarios describing ancestral relationship among ancestral populations and more recently founded populations. Our analyses confirmed the Middle East-East Africa as the most likely source of newly spreading, high-temperature-adapted strains; Europe as the source of South American, North American and Australian populations; and Mediterranean-Central Asian populations as the origin of South African populations. Although most geographic populations are not markedly affected by recent dispersal events, this study emphasizes the influence of human activities on recent long-distance spread of the pathogen. </div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">24465211</PMID><DateCompleted><Year>2015</Year><Month>02</Month><Day>12</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>05</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1553-7374</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>1</Issue><PubDate><Year>2014</Year><Month>Jan</Month></PubDate></JournalIssue><Title>PLoS pathogens</Title><ISOAbbreviation>PLoS Pathog</ISOAbbreviation></Journal><ArticleTitle>Origin, migration routes and worldwide population genetic structure of the wheat yellow rust pathogen Puccinia striiformis f.sp. tritici.</ArticleTitle><Pagination><MedlinePgn>e1003903</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.ppat.1003903</ELocationID><Abstract><AbstractText>Analyses of large-scale population structure of pathogens enable the identification of migration patterns, diversity reservoirs or longevity of populations, the understanding of current evolutionary trajectories and the anticipation of future ones. This is particularly important for long-distance migrating fungal pathogens such as Puccinia striiformis f.sp. tritici (PST), capable of rapid spread to new regions and crop varieties. Although a range of recent PST invasions at continental scales are well documented, the worldwide population structure and the center of origin of the pathogen were still unknown. In this study, we used multilocus microsatellite genotyping to infer worldwide population structure of PST and the origin of new invasions based on 409 isolates representative of distribution of the fungus on six continents. Bayesian and multivariate clustering methods partitioned the set of multilocus genotypes into six distinct genetic groups associated with their geographical origin. Analyses of linkage disequilibrium and genotypic diversity indicated a strong regional heterogeneity in levels of recombination, with clear signatures of recombination in the Himalayan (Nepal and Pakistan) and near-Himalayan regions (China) and a predominant clonal population structure in other regions. The higher genotypic diversity, recombinant population structure and high sexual reproduction ability in the Himalayan and neighboring regions suggests this area as the putative center of origin of PST. We used clustering methods and approximate Bayesian computation (ABC) to compare different competing scenarios describing ancestral relationship among ancestral populations and more recently founded populations. Our analyses confirmed the Middle East-East Africa as the most likely source of newly spreading, high-temperature-adapted strains; Europe as the source of South American, North American and Australian populations; and Mediterranean-Central Asian populations as the origin of South African populations. Although most geographic populations are not markedly affected by recent dispersal events, this study emphasizes the influence of human activities on recent long-distance spread of the pathogen. </AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Ali</LastName><ForeName>Sajid</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>INRA UR 1290 BIOGER-CPP, Thiverval-Grignon, France ; Institute of Biotechnology and Genetic Engineering, the University of Agriculture, Peshawar, Pakistan ; Department of Agroecology, Aarhus University, Slagelse, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gladieux</LastName><ForeName>Pierre</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>UMR 8079 Ecologie Systematique Evolution, Univ. Paris-Sud., CNRS-F, Orsay, France ; Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, California, United States of America.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Leconte</LastName><ForeName>Marc</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>INRA UR 1290 BIOGER-CPP, Thiverval-Grignon, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Gautier</LastName><ForeName>Angélique</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>INRA UR 1290 BIOGER-CPP, Thiverval-Grignon, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Justesen</LastName><ForeName>Annemarie F</ForeName><Initials>AF</Initials><AffiliationInfo><Affiliation>Department of Agroecology, Aarhus University, Slagelse, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hovmøller</LastName><ForeName>Mogens S</ForeName><Initials>MS</Initials><AffiliationInfo><Affiliation>Department of Agroecology, Aarhus University, Slagelse, Denmark.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Enjalbert</LastName><ForeName>Jérôme</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>INRA UMR 320 Génétique Végétale, Ferme du Moulon, Gif sur Yvette, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>de Vallavieille-Pope</LastName><ForeName>Claude</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>INRA UR 1290 BIOGER-CPP, Thiverval-Grignon, France.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2014</Year><Month>01</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>PLoS Pathog</MedlineTA><NlmUniqueID>101238921</NlmUniqueID><ISSNLinking>1553-7366</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D001487" MajorTopicYN="N">Basidiomycota</DescriptorName><QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D014644" MajorTopicYN="Y">Genetic Variation</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D005838" MajorTopicYN="Y">Genotype</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D018895" MajorTopicYN="Y">Microsatellite Repeats</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D010935" MajorTopicYN="N">Plant 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