Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses

Background: The Rhynchosporium species complex consists of hemibiotrophic fungal pathogens specialized to different sweet grass species including the cereal crops barley and rye. A sexual stage has not been described, but several lines of evidence suggest the occurrence of sexual reproduction. Therefore, a comparative genomics approach was carried out to disclose the evolutionary relationship of the species and to identify genes demonstrating the potential for a sexual cycle. Furthermore, due to the evolutionary very young age of the five species currently known, this genus appears to be well-suited to address the question at the molecular level of how pathogenic fungi adapt to their hosts. Results: The genomes of the different Rhynchosporium species were sequenced, assembled and annotated using ab initio gene predictors trained on several fungal genomes as well as on Rhynchosporium expressed sequence tags. Structures of the rDNA regions and genome-wide single nucleotide polymorphisms provided a hypothesis for intra-genus evolution. Homology screening detected core meiotic genes along with most genes crucial for sexual recombination in ascomycete fungi. In addition, a large number of cell wall-degrading enzymes that is characteristic for hemibiotrophic and necrotrophic fungi infecting monocotyledonous hosts were found. Furthermore, the Rhynchosporium genomes carry a repertoire of genes coding for polyketide synthases and non-ribosomal peptide synthetases. Several of these genes are missing from the genome of the closest sequenced relative, the poplar pathogen Marssonina brunnea, and are possibly involved in adaptation to the grass hosts. Most importantly, six species-specific genes coding for protein effectors were identified in R. commune. Their deletion yielded mutants that grew more vigorously in planta than the wild type. Conclusion: Both cryptic sexuality and secondary metabolites may have contributed to host adaptation. Most importantly, however, the growth-retarding activity of the species-specific effectors suggests that host adaptation of R. commune aims at extending the biotrophic stage at the expense of the necrotrophic stage of pathogenesis. Like other apoplastic fungi Rhynchosporium colonizes the intercellular matrix of host leaves relatively slowly without causing symptoms, reminiscent of the development of endophytic fungi. Rhynchosporium may therefore become an object for studying the mutualism-parasitism transition.

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Main Authors: Penselin, Daniel, Münsterkötter, Martin, Kirsten, Susanne, Felder, Marius, Taudien, Stefan, Platzer, Matthias, Ashelford, Kevin, Paskiewicz, Konrad H., Harrison, Richard J., Hughes, David J., Wolf, Thomas, Shelest, Ekaterina, Graap, Jenny, Hoffmann, Jan, Wenzel, Claudia, Wöltje, Nadine, King, Kevin M., Fitt, Bruce D.L., Güldener, Ulrich, Avrova, Anna, Knogge, Wolfgang
Format: Article/Letter to editor biblioteca
Language:English
Subjects:CAZymes, Effectors, Host specificity, Leotiomycetes, Non-ribosomal peptide synthetases, Phylogenetic evolution, Polyketide synthases, Rhynchosporium, Sex-related genes, Whole genome sequencing,
Online Access:https://research.wur.nl/en/publications/comparative-genomics-to-explore-phylogenetic-relationship-cryptic
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spelling dig-wur-nl-wurpubs-6049682024-12-04 Penselin, Daniel Münsterkötter, Martin Kirsten, Susanne Felder, Marius Taudien, Stefan Platzer, Matthias Ashelford, Kevin Paskiewicz, Konrad H. Harrison, Richard J. Hughes, David J. Wolf, Thomas Shelest, Ekaterina Graap, Jenny Hoffmann, Jan Wenzel, Claudia Wöltje, Nadine King, Kevin M. Fitt, Bruce D.L. Güldener, Ulrich Avrova, Anna Knogge, Wolfgang Article/Letter to editor BMC Genomics 17 (2016) ISSN: 1471-2164 Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses 2016 Background: The Rhynchosporium species complex consists of hemibiotrophic fungal pathogens specialized to different sweet grass species including the cereal crops barley and rye. A sexual stage has not been described, but several lines of evidence suggest the occurrence of sexual reproduction. Therefore, a comparative genomics approach was carried out to disclose the evolutionary relationship of the species and to identify genes demonstrating the potential for a sexual cycle. Furthermore, due to the evolutionary very young age of the five species currently known, this genus appears to be well-suited to address the question at the molecular level of how pathogenic fungi adapt to their hosts. Results: The genomes of the different Rhynchosporium species were sequenced, assembled and annotated using ab initio gene predictors trained on several fungal genomes as well as on Rhynchosporium expressed sequence tags. Structures of the rDNA regions and genome-wide single nucleotide polymorphisms provided a hypothesis for intra-genus evolution. Homology screening detected core meiotic genes along with most genes crucial for sexual recombination in ascomycete fungi. In addition, a large number of cell wall-degrading enzymes that is characteristic for hemibiotrophic and necrotrophic fungi infecting monocotyledonous hosts were found. Furthermore, the Rhynchosporium genomes carry a repertoire of genes coding for polyketide synthases and non-ribosomal peptide synthetases. Several of these genes are missing from the genome of the closest sequenced relative, the poplar pathogen Marssonina brunnea, and are possibly involved in adaptation to the grass hosts. Most importantly, six species-specific genes coding for protein effectors were identified in R. commune. Their deletion yielded mutants that grew more vigorously in planta than the wild type. Conclusion: Both cryptic sexuality and secondary metabolites may have contributed to host adaptation. Most importantly, however, the growth-retarding activity of the species-specific effectors suggests that host adaptation of R. commune aims at extending the biotrophic stage at the expense of the necrotrophic stage of pathogenesis. Like other apoplastic fungi Rhynchosporium colonizes the intercellular matrix of host leaves relatively slowly without causing symptoms, reminiscent of the development of endophytic fungi. Rhynchosporium may therefore become an object for studying the mutualism-parasitism transition. en text/html https://research.wur.nl/en/publications/comparative-genomics-to-explore-phylogenetic-relationship-cryptic 10.1186/s12864-016-3299-5 https://edepot.wur.nl/581509 CAZymes Effectors Host specificity Leotiomycetes Non-ribosomal peptide synthetases Phylogenetic evolution Polyketide synthases Rhynchosporium Sex-related genes Whole genome sequencing https://creativecommons.org/licenses/by/4.0/ Wageningen University & Research
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collection DSpace
country Países bajos
countrycode NL
component Bibliográfico
access En linea
databasecode dig-wur-nl
tag biblioteca
region Europa del Oeste
libraryname WUR Library Netherlands
language English
topic CAZymes
Effectors
Host specificity
Leotiomycetes
Non-ribosomal peptide synthetases
Phylogenetic evolution
Polyketide synthases
Rhynchosporium
Sex-related genes
Whole genome sequencing
CAZymes
Effectors
Host specificity
Leotiomycetes
Non-ribosomal peptide synthetases
Phylogenetic evolution
Polyketide synthases
Rhynchosporium
Sex-related genes
Whole genome sequencing
spellingShingle CAZymes
Effectors
Host specificity
Leotiomycetes
Non-ribosomal peptide synthetases
Phylogenetic evolution
Polyketide synthases
Rhynchosporium
Sex-related genes
Whole genome sequencing
CAZymes
Effectors
Host specificity
Leotiomycetes
Non-ribosomal peptide synthetases
Phylogenetic evolution
Polyketide synthases
Rhynchosporium
Sex-related genes
Whole genome sequencing
Penselin, Daniel
Münsterkötter, Martin
Kirsten, Susanne
Felder, Marius
Taudien, Stefan
Platzer, Matthias
Ashelford, Kevin
Paskiewicz, Konrad H.
Harrison, Richard J.
Hughes, David J.
Wolf, Thomas
Shelest, Ekaterina
Graap, Jenny
Hoffmann, Jan
Wenzel, Claudia
Wöltje, Nadine
King, Kevin M.
Fitt, Bruce D.L.
Güldener, Ulrich
Avrova, Anna
Knogge, Wolfgang
Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses
description Background: The Rhynchosporium species complex consists of hemibiotrophic fungal pathogens specialized to different sweet grass species including the cereal crops barley and rye. A sexual stage has not been described, but several lines of evidence suggest the occurrence of sexual reproduction. Therefore, a comparative genomics approach was carried out to disclose the evolutionary relationship of the species and to identify genes demonstrating the potential for a sexual cycle. Furthermore, due to the evolutionary very young age of the five species currently known, this genus appears to be well-suited to address the question at the molecular level of how pathogenic fungi adapt to their hosts. Results: The genomes of the different Rhynchosporium species were sequenced, assembled and annotated using ab initio gene predictors trained on several fungal genomes as well as on Rhynchosporium expressed sequence tags. Structures of the rDNA regions and genome-wide single nucleotide polymorphisms provided a hypothesis for intra-genus evolution. Homology screening detected core meiotic genes along with most genes crucial for sexual recombination in ascomycete fungi. In addition, a large number of cell wall-degrading enzymes that is characteristic for hemibiotrophic and necrotrophic fungi infecting monocotyledonous hosts were found. Furthermore, the Rhynchosporium genomes carry a repertoire of genes coding for polyketide synthases and non-ribosomal peptide synthetases. Several of these genes are missing from the genome of the closest sequenced relative, the poplar pathogen Marssonina brunnea, and are possibly involved in adaptation to the grass hosts. Most importantly, six species-specific genes coding for protein effectors were identified in R. commune. Their deletion yielded mutants that grew more vigorously in planta than the wild type. Conclusion: Both cryptic sexuality and secondary metabolites may have contributed to host adaptation. Most importantly, however, the growth-retarding activity of the species-specific effectors suggests that host adaptation of R. commune aims at extending the biotrophic stage at the expense of the necrotrophic stage of pathogenesis. Like other apoplastic fungi Rhynchosporium colonizes the intercellular matrix of host leaves relatively slowly without causing symptoms, reminiscent of the development of endophytic fungi. Rhynchosporium may therefore become an object for studying the mutualism-parasitism transition.
format Article/Letter to editor
topic_facet CAZymes
Effectors
Host specificity
Leotiomycetes
Non-ribosomal peptide synthetases
Phylogenetic evolution
Polyketide synthases
Rhynchosporium
Sex-related genes
Whole genome sequencing
author Penselin, Daniel
Münsterkötter, Martin
Kirsten, Susanne
Felder, Marius
Taudien, Stefan
Platzer, Matthias
Ashelford, Kevin
Paskiewicz, Konrad H.
Harrison, Richard J.
Hughes, David J.
Wolf, Thomas
Shelest, Ekaterina
Graap, Jenny
Hoffmann, Jan
Wenzel, Claudia
Wöltje, Nadine
King, Kevin M.
Fitt, Bruce D.L.
Güldener, Ulrich
Avrova, Anna
Knogge, Wolfgang
author_facet Penselin, Daniel
Münsterkötter, Martin
Kirsten, Susanne
Felder, Marius
Taudien, Stefan
Platzer, Matthias
Ashelford, Kevin
Paskiewicz, Konrad H.
Harrison, Richard J.
Hughes, David J.
Wolf, Thomas
Shelest, Ekaterina
Graap, Jenny
Hoffmann, Jan
Wenzel, Claudia
Wöltje, Nadine
King, Kevin M.
Fitt, Bruce D.L.
Güldener, Ulrich
Avrova, Anna
Knogge, Wolfgang
author_sort Penselin, Daniel
title Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses
title_short Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses
title_full Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses
title_fullStr Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses
title_full_unstemmed Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses
title_sort comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of rhynchosporium species on grasses
url https://research.wur.nl/en/publications/comparative-genomics-to-explore-phylogenetic-relationship-cryptic
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