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Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum.

Identifieur interne : 000C09 ( Main/Exploration ); précédent : 000C08; suivant : 000C10

Host-induced aneuploidy and phenotypic diversification in the Sudden Oak Death pathogen Phytophthora ramorum.

Auteurs : Takao Kasuga [États-Unis] ; Mai Bui [États-Unis] ; Elizabeth Bernhardt [États-Unis] ; Tedmund Swiecki [États-Unis] ; Kamyar Aram [États-Unis] ; Liliana M. Cano [États-Unis] ; Joan Webber [Royaume-Uni] ; Clive Brasier [Royaume-Uni] ; Caroline Press [États-Unis] ; Niklaus J. Grünwald [États-Unis] ; David M. Rizzo [États-Unis] ; Matteo Garbelotto [États-Unis]

Source :

RBID : pubmed:27206972

Descripteurs français

English descriptors

Abstract

BACKGROUND

Aneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous. For example, aneuploidy confers resistance to antifungal drugs in human pathogenic fungi. Aneuploidy has also been observed in invasive fungal and oomycete plant pathogens in the field. Environments conducive to the generation of aneuploids, the underlying genetic mechanisms, and the contribution of aneuploidy to invasiveness are underexplored. We studied phenotypic diversification and associated genome changes in Phytophthora ramorum, a highly destructive oomycete pathogen with a wide host-range that causes Sudden Oak Death in western North America and Sudden Larch Death in the UK. Introduced populations of the pathogen are exclusively clonal. In California, oak (Quercus spp.) isolates obtained from trunk cankers frequently exhibit host-dependent, atypical phenotypes called non-wild type (nwt), apparently without any host-associated population differentiation. Based on a large survey of genotypes from different hosts, we previously hypothesized that the environment in oak cankers may be responsible for the observed phenotypic diversification in P. ramorum.

RESULTS

We show that both normal wild type (wt) and nwt phenotypes were obtained when wt P. ramorum isolates from the foliar host California bay (Umbellularia californica) were re-isolated from cankers of artificially-inoculated canyon live oak (Q. chrysolepis). We also found comparable nwt phenotypes in P. ramorum isolates from a bark canker of Lawson cypress (Chamaecyparis lawsoniana) in the UK; previously nwt was not known to occur in this pathogen population. High-throughput sequencing-based analyses identified major genomic alterations including partial aneuploidy and copy-neutral loss of heterozygosity predominantly in nwt isolates. Chromosomal breakpoints were located at or near transposons.

CONCLUSION

This work demonstrates that major genome alterations of a pathogen can be induced by its host species. This is an undocumented type of plant-microbe interaction, and its contribution to pathogen evolution is yet to be investigated, but one of the potential collateral effects of nwt phenotypes may be host survival.


DOI: 10.1186/s12864-016-2717-z
PubMed: 27206972
PubMed Central: PMC4875591


Affiliations:


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Le document en format XML

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<term>Aneuploidy (MeSH)</term>
<term>California (MeSH)</term>
<term>DNA Copy Number Variations (MeSH)</term>
<term>DNA Transposable Elements (MeSH)</term>
<term>Gene Duplication (MeSH)</term>
<term>Gene Expression Profiling (MeSH)</term>
<term>Genetic Linkage (MeSH)</term>
<term>Genotype (MeSH)</term>
<term>Loss of Heterozygosity (MeSH)</term>
<term>Phenotype (MeSH)</term>
<term>Phytophthora (genetics)</term>
<term>Plant Diseases (microbiology)</term>
<term>Polymorphism, Single Nucleotide (MeSH)</term>
<term>Quercus (microbiology)</term>
<term>Transcriptome (MeSH)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Analyse de profil d'expression de gènes (MeSH)</term>
<term>Aneuploïdie (MeSH)</term>
<term>Californie (MeSH)</term>
<term>Duplication de gène (MeSH)</term>
<term>Génotype (MeSH)</term>
<term>Liaison génétique (MeSH)</term>
<term>Maladies des plantes (microbiologie)</term>
<term>Perte d'hétérozygotie (MeSH)</term>
<term>Phytophthora (génétique)</term>
<term>Phénotype (MeSH)</term>
<term>Polymorphisme de nucléotide simple (MeSH)</term>
<term>Quercus (microbiologie)</term>
<term>Transcriptome (MeSH)</term>
<term>Variations de nombre de copies de segment d'ADN (MeSH)</term>
<term>Éléments transposables d'ADN (MeSH)</term>
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<term>DNA Transposable Elements</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en">
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Phytophthora</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Maladies des plantes</term>
<term>Quercus</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>Plant Diseases</term>
<term>Quercus</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Aneuploidy</term>
<term>California</term>
<term>DNA Copy Number Variations</term>
<term>Gene Duplication</term>
<term>Gene Expression Profiling</term>
<term>Genetic Linkage</term>
<term>Genotype</term>
<term>Loss of Heterozygosity</term>
<term>Phenotype</term>
<term>Polymorphism, Single Nucleotide</term>
<term>Transcriptome</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Analyse de profil d'expression de gènes</term>
<term>Aneuploïdie</term>
<term>Californie</term>
<term>Duplication de gène</term>
<term>Génotype</term>
<term>Liaison génétique</term>
<term>Perte d'hétérozygotie</term>
<term>Phénotype</term>
<term>Polymorphisme de nucléotide simple</term>
<term>Transcriptome</term>
<term>Variations de nombre de copies de segment d'ADN</term>
<term>Éléments transposables d'ADN</term>
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<p>
<b>BACKGROUND</b>
</p>
<p>Aneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous. For example, aneuploidy confers resistance to antifungal drugs in human pathogenic fungi. Aneuploidy has also been observed in invasive fungal and oomycete plant pathogens in the field. Environments conducive to the generation of aneuploids, the underlying genetic mechanisms, and the contribution of aneuploidy to invasiveness are underexplored. We studied phenotypic diversification and associated genome changes in Phytophthora ramorum, a highly destructive oomycete pathogen with a wide host-range that causes Sudden Oak Death in western North America and Sudden Larch Death in the UK. Introduced populations of the pathogen are exclusively clonal. In California, oak (Quercus spp.) isolates obtained from trunk cankers frequently exhibit host-dependent, atypical phenotypes called non-wild type (nwt), apparently without any host-associated population differentiation. Based on a large survey of genotypes from different hosts, we previously hypothesized that the environment in oak cankers may be responsible for the observed phenotypic diversification in P. ramorum.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>RESULTS</b>
</p>
<p>We show that both normal wild type (wt) and nwt phenotypes were obtained when wt P. ramorum isolates from the foliar host California bay (Umbellularia californica) were re-isolated from cankers of artificially-inoculated canyon live oak (Q. chrysolepis). We also found comparable nwt phenotypes in P. ramorum isolates from a bark canker of Lawson cypress (Chamaecyparis lawsoniana) in the UK; previously nwt was not known to occur in this pathogen population. High-throughput sequencing-based analyses identified major genomic alterations including partial aneuploidy and copy-neutral loss of heterozygosity predominantly in nwt isolates. Chromosomal breakpoints were located at or near transposons.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>CONCLUSION</b>
</p>
<p>This work demonstrates that major genome alterations of a pathogen can be induced by its host species. This is an undocumented type of plant-microbe interaction, and its contribution to pathogen evolution is yet to be investigated, but one of the potential collateral effects of nwt phenotypes may be host survival.</p>
</div>
</front>
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<Day>11</Day>
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<Month>11</Month>
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<Title>BMC genomics</Title>
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<AbstractText Label="BACKGROUND">Aneuploidy can result in significant phenotypic changes, which can sometimes be selectively advantageous. For example, aneuploidy confers resistance to antifungal drugs in human pathogenic fungi. Aneuploidy has also been observed in invasive fungal and oomycete plant pathogens in the field. Environments conducive to the generation of aneuploids, the underlying genetic mechanisms, and the contribution of aneuploidy to invasiveness are underexplored. We studied phenotypic diversification and associated genome changes in Phytophthora ramorum, a highly destructive oomycete pathogen with a wide host-range that causes Sudden Oak Death in western North America and Sudden Larch Death in the UK. Introduced populations of the pathogen are exclusively clonal. In California, oak (Quercus spp.) isolates obtained from trunk cankers frequently exhibit host-dependent, atypical phenotypes called non-wild type (nwt), apparently without any host-associated population differentiation. Based on a large survey of genotypes from different hosts, we previously hypothesized that the environment in oak cankers may be responsible for the observed phenotypic diversification in P. ramorum.</AbstractText>
<AbstractText Label="RESULTS">We show that both normal wild type (wt) and nwt phenotypes were obtained when wt P. ramorum isolates from the foliar host California bay (Umbellularia californica) were re-isolated from cankers of artificially-inoculated canyon live oak (Q. chrysolepis). We also found comparable nwt phenotypes in P. ramorum isolates from a bark canker of Lawson cypress (Chamaecyparis lawsoniana) in the UK; previously nwt was not known to occur in this pathogen population. High-throughput sequencing-based analyses identified major genomic alterations including partial aneuploidy and copy-neutral loss of heterozygosity predominantly in nwt isolates. Chromosomal breakpoints were located at or near transposons.</AbstractText>
<AbstractText Label="CONCLUSION">This work demonstrates that major genome alterations of a pathogen can be induced by its host species. This is an undocumented type of plant-microbe interaction, and its contribution to pathogen evolution is yet to be investigated, but one of the potential collateral effects of nwt phenotypes may be host survival.</AbstractText>
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<ForeName>Takao</ForeName>
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<Affiliation>Crops Pathology and Genetics Research Unit, USDA Agricultural Research Service, Davis, California, 95616, USA.</Affiliation>
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<ForeName>Mai</ForeName>
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<Affiliation>Crops Pathology and Genetics Research Unit, USDA Agricultural Research Service, Davis, California, 95616, USA.</Affiliation>
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<ForeName>Tedmund</ForeName>
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<Affiliation>Department of Plant Pathology, University of California, Davis, California, 95616, USA.</Affiliation>
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<ForeName>Matteo</ForeName>
<Initials>M</Initials>
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<Affiliation>Department of Environmental Science, Policy, and Management, University of California, Berkeley, California, 947020, USA. matteog@berkeley.edu.</Affiliation>
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<Month>05</Month>
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