Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen Phytophthora infestans.
Identifieur interne : 000183 ( Main/Exploration ); précédent : 000182; suivant : 000184Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen Phytophthora infestans.
Auteurs : Brian J. Knaus [États-Unis] ; Javier F. Tabima [États-Unis] ; Shankar K. Shakya [États-Unis] ; Howard S. Judelson [États-Unis] ; Niklaus J. GrünwaldSource :
- mBio [ 2150-7511 ] ; 2020.
Abstract
The plant pathogen that caused the Irish potato famine, Phytophthora infestans, continues to reemerge globally. These modern epidemics are caused by clonally reproducing lineages. In contrast, a sexual mode of reproduction is observed at its center of origin in Mexico. We conducted a comparative genomic analysis of 47 high-coverage genomes to infer changes in genic copy number. We included samples from sexual populations at the center of origin as well as several dominant clonal lineages sampled worldwide. We conclude that sexual populations at the center of origin are diploid, as was the lineage that caused the famine, while modern clonal lineages showed increased copy number (3×). Copy number variation (CNV) was found genome-wide and did not to adhere to the two-speed genome hypothesis. Although previously reported, tetraploidy was not found in any of the genomes evaluated. We propose a model of dominant clone emergence supported by the epidemiological record (e.g., EU_13_A2, US-11, US-23) whereby a higher copy number provides fitness, leading to replacement of prior clonal lineages.IMPORTANCE The plant pathogen implicated in the Irish potato famine, Phytophthora infestans, continues to reemerge globally. Understanding changes in the genome during emergence can provide insights useful for managing this pathogen. Previous work has relied on studying individuals from the United States, South America, Europe, and China reporting that these can occur as diploids, triploids, or tetraploids and are clonal. We studied variation in sexual populations at the pathogen's center of origin, in Mexico, where it has been reported to reproduce sexually as well as within clonally reproducing, dominant clones from the United States and Europe. Our results newly show that sexual populations at the center of origin are diploid, whereas populations elsewhere are more variable and show genome-wide variation in gene copy number. We propose a model of evolution whereby new pathogen clones emerge predominantly by increasing the gene copy number genome-wide.
DOI: 10.1128/mBio.00326-20
PubMed: 32576669
PubMed Central: PMC7315116
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Knaus</name><affiliation wicri:level="2"><nlm:affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Tabima, Javier F" sort="Tabima, Javier F" uniqKey="Tabima J" first="Javier F" last="Tabima">Javier F. Tabima</name><affiliation wicri:level="2"><nlm:affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Shakya, Shankar K" sort="Shakya, Shankar K" uniqKey="Shakya S" first="Shankar K" last="Shakya">Shankar K. Shakya</name><affiliation wicri:level="2"><nlm:affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon</wicri:regionArea><placeName><region type="state">Oregon</region></placeName></affiliation></author><author><name sortKey="Judelson, Howard S" sort="Judelson, Howard S" uniqKey="Judelson H" first="Howard S" last="Judelson">Howard S. Judelson</name><affiliation wicri:level="2"><nlm:affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, California, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Microbiology and Plant Pathology, University of California, Riverside, California</wicri:regionArea><placeName><region type="state">Californie</region></placeName></affiliation></author><author><name sortKey="Grunwald, Niklaus J" sort="Grunwald, Niklaus J" uniqKey="Grunwald N" first="Niklaus J" last="Grünwald">Niklaus J. Grünwald</name><affiliation><nlm:affiliation>Horticultural Crop Research Unit, United States Department of Agriculture, Agricultural Research Service, Corvallis, Oregon, USA nik.grunwald@ars.usda.gov.</nlm:affiliation><wicri:noCountry code="subField">USA nik.grunwald@ars.usda.gov.</wicri:noCountry></affiliation></author></analytic><series><title level="j">mBio</title><idno type="eISSN">2150-7511</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 plant pathogen that caused the Irish potato famine, <i>Phytophthora infestans</i>, continues to reemerge globally. These modern epidemics are caused by clonally reproducing lineages. In contrast, a sexual mode of reproduction is observed at its center of origin in Mexico. We conducted a comparative genomic analysis of 47 high-coverage genomes to infer changes in genic copy number. We included samples from sexual populations at the center of origin as well as several dominant clonal lineages sampled worldwide. We conclude that sexual populations at the center of origin are diploid, as was the lineage that caused the famine, while modern clonal lineages showed increased copy number (3×). Copy number variation (CNV) was found genome-wide and did not to adhere to the two-speed genome hypothesis. Although previously reported, tetraploidy was not found in any of the genomes evaluated. We propose a model of dominant clone emergence supported by the epidemiological record (e.g., EU_13_A2, US-11, US-23) whereby a higher copy number provides fitness, leading to replacement of prior clonal lineages.<b>IMPORTANCE</b> The plant pathogen implicated in the Irish potato famine, <i>Phytophthora infestans</i>, continues to reemerge globally. Understanding changes in the genome during emergence can provide insights useful for managing this pathogen. Previous work has relied on studying individuals from the United States, South America, Europe, and China reporting that these can occur as diploids, triploids, or tetraploids and are clonal. We studied variation in sexual populations at the pathogen's center of origin, in Mexico, where it has been reported to reproduce sexually as well as within clonally reproducing, dominant clones from the United States and Europe. Our results newly show that sexual populations at the center of origin are diploid, whereas populations elsewhere are more variable and show genome-wide variation in gene copy number. We propose a model of evolution whereby new pathogen clones emerge predominantly by increasing the gene copy number genome-wide.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32576669</PMID><DateRevised><Year>2020</Year><Month>07</Month><Day>23</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2150-7511</ISSN><JournalIssue CitedMedium="Internet"><Volume>11</Volume><Issue>3</Issue><PubDate><Year>2020</Year><Month>06</Month><Day>23</Day></PubDate></JournalIssue><Title>mBio</Title><ISOAbbreviation>mBio</ISOAbbreviation></Journal><ArticleTitle>Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen Phytophthora infestans.</ArticleTitle><ELocationID EIdType="pii" ValidYN="Y">e00326-20</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1128/mBio.00326-20</ELocationID><Abstract><AbstractText>The plant pathogen that caused the Irish potato famine, <i>Phytophthora infestans</i>, continues to reemerge globally. These modern epidemics are caused by clonally reproducing lineages. In contrast, a sexual mode of reproduction is observed at its center of origin in Mexico. We conducted a comparative genomic analysis of 47 high-coverage genomes to infer changes in genic copy number. We included samples from sexual populations at the center of origin as well as several dominant clonal lineages sampled worldwide. We conclude that sexual populations at the center of origin are diploid, as was the lineage that caused the famine, while modern clonal lineages showed increased copy number (3×). Copy number variation (CNV) was found genome-wide and did not to adhere to the two-speed genome hypothesis. Although previously reported, tetraploidy was not found in any of the genomes evaluated. We propose a model of dominant clone emergence supported by the epidemiological record (e.g., EU_13_A2, US-11, US-23) whereby a higher copy number provides fitness, leading to replacement of prior clonal lineages.<b>IMPORTANCE</b> The plant pathogen implicated in the Irish potato famine, <i>Phytophthora infestans</i>, continues to reemerge globally. Understanding changes in the genome during emergence can provide insights useful for managing this pathogen. Previous work has relied on studying individuals from the United States, South America, Europe, and China reporting that these can occur as diploids, triploids, or tetraploids and are clonal. We studied variation in sexual populations at the pathogen's center of origin, in Mexico, where it has been reported to reproduce sexually as well as within clonally reproducing, dominant clones from the United States and Europe. Our results newly show that sexual populations at the center of origin are diploid, whereas populations elsewhere are more variable and show genome-wide variation in gene copy number. We propose a model of evolution whereby new pathogen clones emerge predominantly by increasing the gene copy number genome-wide.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Knaus</LastName><ForeName>Brian J</ForeName><Initials>BJ</Initials><Identifier Source="ORCID">0000-0003-1665-4343</Identifier><AffiliationInfo><Affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tabima</LastName><ForeName>Javier F</ForeName><Initials>JF</Initials><Identifier Source="ORCID">0000-0002-3603-2691</Identifier><AffiliationInfo><Affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Shakya</LastName><ForeName>Shankar K</ForeName><Initials>SK</Initials><Identifier Source="ORCID">0000-0002-8439-9009</Identifier><AffiliationInfo><Affiliation>Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Judelson</LastName><ForeName>Howard S</ForeName><Initials>HS</Initials><Identifier Source="ORCID">0000-0001-7865-6235</Identifier><AffiliationInfo><Affiliation>Department of Microbiology and Plant Pathology, University of California, Riverside, California, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Grünwald</LastName><ForeName>Niklaus J</ForeName><Initials>NJ</Initials><Identifier Source="ORCID">0000-0003-1656-7602</Identifier><AffiliationInfo><Affiliation>Horticultural Crop Research Unit, United States Department of Agriculture, Agricultural Research Service, Corvallis, Oregon, USA nik.grunwald@ars.usda.gov.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013486">Research Support, U.S. Gov't, Non-P.H.S.</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>23</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>mBio</MedlineTA><NlmUniqueID>101519231</NlmUniqueID></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">Irish famine</Keyword><Keyword MajorTopicYN="Y">Phytophthora
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