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Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria.

Identifieur interne : 000153 ( Main/Exploration ); précédent : 000152; suivant : 000154

Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria.

Auteurs : Alice Feurtey [Allemagne] ; Cécile Lorrain [Allemagne, France] ; Daniel Croll [Suisse] ; Christoph Eschenbrenner [Allemagne] ; Michael Freitag [États-Unis] ; Michael Habig [Allemagne] ; Janine Haueisen [Allemagne] ; Mareike Möller [Allemagne, États-Unis] ; Klaas Schotanus [Allemagne, États-Unis] ; Eva H. Stukenbrock [Allemagne]

Source :

RBID : pubmed:32842972

Abstract

BACKGROUND

Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome structure may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and of sister species infecting wild grasses to address the evolution of genome composition and structure.

RESULTS

Using long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, predicted effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts.

CONCLUSION

Despite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genus Zymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome.


DOI: 10.1186/s12864-020-06871-w
PubMed: 32842972
PubMed Central: PMC7448473


Affiliations:


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<name sortKey="Schotanus, Klaas" sort="Schotanus, Klaas" uniqKey="Schotanus K" first="Klaas" last="Schotanus">Klaas Schotanus</name>
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<nlm:affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</nlm:affiliation>
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<nlm:affiliation>Department of Molecular Genetics and Microbiology, Duke University, Duke University Medical Center, Durham, NC, 27710, USA.</nlm:affiliation>
<country xml:lang="fr">États-Unis</country>
<wicri:regionArea>Department of Molecular Genetics and Microbiology, Duke University, Duke University Medical Center, Durham, NC, 27710</wicri:regionArea>
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<name sortKey="Stukenbrock, Eva H" sort="Stukenbrock, Eva H" uniqKey="Stukenbrock E" first="Eva H" last="Stukenbrock">Eva H. Stukenbrock</name>
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<nlm:affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</nlm:affiliation>
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<title level="j">BMC genomics</title>
<idno type="eISSN">1471-2164</idno>
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<date when="2020" type="published">2020</date>
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<div type="abstract" xml:lang="en">
<p>
<b>BACKGROUND</b>
</p>
<p>Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome structure may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and of sister species infecting wild grasses to address the evolution of genome composition and structure.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>RESULTS</b>
</p>
<p>Using long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, predicted effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts.</p>
</div>
<div type="abstract" xml:lang="en">
<p>
<b>CONCLUSION</b>
</p>
<p>Despite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genus Zymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome.</p>
</div>
</front>
</TEI>
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<DateRevised>
<Year>2020</Year>
<Month>08</Month>
<Day>29</Day>
</DateRevised>
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<Journal>
<ISSN IssnType="Electronic">1471-2164</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>21</Volume>
<Issue>1</Issue>
<PubDate>
<Year>2020</Year>
<Month>Aug</Month>
<Day>26</Day>
</PubDate>
</JournalIssue>
<Title>BMC genomics</Title>
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<ArticleTitle>Genome compartmentalization predates species divergence in the plant pathogen genus Zymoseptoria.</ArticleTitle>
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<Abstract>
<AbstractText Label="BACKGROUND" NlmCategory="BACKGROUND">Antagonistic co-evolution can drive rapid adaptation in pathogens and shape genome architecture. Comparative genome analyses of several fungal pathogens revealed highly variable genomes, for many species characterized by specific repeat-rich genome compartments with exceptionally high sequence variability. Dynamic genome structure may enable fast adaptation to host genetics. The wheat pathogen Zymoseptoria tritici with its highly variable genome, has emerged as a model organism to study genome evolution of plant pathogens. Here, we compared genomes of Z. tritici isolates and of sister species infecting wild grasses to address the evolution of genome composition and structure.</AbstractText>
<AbstractText Label="RESULTS" NlmCategory="RESULTS">Using long-read technology, we sequenced and assembled genomes of Z. ardabiliae, Z. brevis, Z. pseudotritici and Z. passerinii, together with two isolates of Z. tritici. We report a high extent of genome collinearity among Zymoseptoria species and high conservation of genomic, transcriptomic and epigenomic signatures of compartmentalization. We identify high gene content variability both within and between species. In addition, such variability is mainly limited to the accessory chromosomes and accessory compartments. Despite strong host specificity and non-overlapping host-range between species, predicted effectors are mainly shared among Zymoseptoria species, yet exhibiting a high level of presence-absence polymorphism within Z. tritici. Using in planta transcriptomic data from Z. tritici, we suggest different roles for the shared orthologs and for the accessory genes during infection of their hosts.</AbstractText>
<AbstractText Label="CONCLUSION" NlmCategory="CONCLUSIONS">Despite previous reports of high genomic plasticity in Z. tritici, we describe here a high level of conservation in genomic, epigenomic and transcriptomic composition and structure across the genus Zymoseptoria. The compartmentalized genome allows the maintenance of a functional core genome co-occurring with a highly variable accessory genome.</AbstractText>
</Abstract>
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<LastName>Feurtey</LastName>
<ForeName>Alice</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lorrain</LastName>
<ForeName>Cécile</ForeName>
<Initials>C</Initials>
<Identifier Source="ORCID">http://orcid.org/0000-0001-9727-2616</Identifier>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany. lorrain@evolbio.mpg.de.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany. lorrain@evolbio.mpg.de.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>INRA Centre Grand Est - Nancy, UMR 1136 INRA/Universite de Lorraine Interactions Arbres/Microorganismes, 54280, Champenoux, France. lorrain@evolbio.mpg.de.</Affiliation>
</AffiliationInfo>
</Author>
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<LastName>Croll</LastName>
<ForeName>Daniel</ForeName>
<Initials>D</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Evolutionary Genetics, Institute of Biology, University of Neuchâtel, 2000, Neuchâtel, Switzerland.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Eschenbrenner</LastName>
<ForeName>Christoph</ForeName>
<Initials>C</Initials>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Freitag</LastName>
<ForeName>Michael</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Department of Biochemistry and Biophysics, Oregon State University, Corvallis, OR, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Habig</LastName>
<ForeName>Michael</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Haueisen</LastName>
<ForeName>Janine</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Möller</LastName>
<ForeName>Mareike</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Biochemistry and Biophysics, Oregon State University, Corvallis, OR, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Schotanus</LastName>
<ForeName>Klaas</ForeName>
<Initials>K</Initials>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Molecular Genetics and Microbiology, Duke University, Duke University Medical Center, Durham, NC, 27710, USA.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Stukenbrock</LastName>
<ForeName>Eva H</ForeName>
<Initials>EH</Initials>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Max Planck Institute for Evolutionary Biology, 24306, Plön, Germany.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Environmental Genomics, Christian-Albrechts University of Kiel, 24118, Kiel, Germany.</Affiliation>
</AffiliationInfo>
</Author>
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<Language>eng</Language>
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<Year>2020</Year>
<Month>08</Month>
<Day>26</Day>
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<Keyword MajorTopicYN="N">Accessory genes</Keyword>
<Keyword MajorTopicYN="N">Effectors</Keyword>
<Keyword MajorTopicYN="N">Genome architecture</Keyword>
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