Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>

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 compar...

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Autores principales: Brian J. Knaus, Javier F. Tabima, Shankar K. Shakya, Howard S. Judelson, Niklaus J. Grünwald
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:f0506aa211534f23ba1c8a973d8b10fc2021-11-15T15:56:46ZGenome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>10.1128/mBio.00326-202150-7511https://doaj.org/article/f0506aa211534f23ba1c8a973d8b10fc2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00326-20https://doaj.org/toc/2150-7511ABSTRACT 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.Brian J. KnausJavier F. TabimaShankar K. ShakyaHoward S. JudelsonNiklaus J. GrünwaldAmerican Society for MicrobiologyarticleIrish faminePhytophthoracopy number variationoomycetesplant pathogenplant pathologyMicrobiologyQR1-502ENmBio, Vol 11, Iss 3 (2020)
institution DOAJ
collection DOAJ
language EN
topic Irish famine
Phytophthora
copy number variation
oomycetes
plant pathogen
plant pathology
Microbiology
QR1-502
spellingShingle Irish famine
Phytophthora
copy number variation
oomycetes
plant pathogen
plant pathology
Microbiology
QR1-502
Brian J. Knaus
Javier F. Tabima
Shankar K. Shakya
Howard S. Judelson
Niklaus J. Grünwald
Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>
description 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.
format article
author Brian J. Knaus
Javier F. Tabima
Shankar K. Shakya
Howard S. Judelson
Niklaus J. Grünwald
author_facet Brian J. Knaus
Javier F. Tabima
Shankar K. Shakya
Howard S. Judelson
Niklaus J. Grünwald
author_sort Brian J. Knaus
title Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>
title_short Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>
title_full Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>
title_fullStr Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>
title_full_unstemmed Genome-Wide Increased Copy Number is Associated with Emergence of Dominant Clones of the Irish Potato Famine Pathogen <named-content content-type="genus-species">Phytophthora infestans</named-content>
title_sort genome-wide increased copy number is associated with emergence of dominant clones of the irish potato famine pathogen <named-content content-type="genus-species">phytophthora infestans</named-content>
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/f0506aa211534f23ba1c8a973d8b10fc
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