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

In: BMC Genomics, Vol. 17, No. 1, 953, 22.11.2016.

Research output: Contribution to journalArticlepeer-review

Harvard

Penselin, D, Münsterkötter, M, Kirsten, S, Felder, M, Taudien, S, Platzer, M, Ashelford, K, Paskiewicz, KH, Harrison, RJ, Hughes, DJ, Wolf, T, Shelest, E, Graap, J, Hoffmann, J, Wenzel, C, Wöltje, N, King, KM, Fitt, BDL, Güldener, U, Avrova, A & Knogge, W 2016, 'Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses', BMC Genomics, vol. 17, no. 1, 953. https://doi.org/10.1186/s12864-016-3299-5

APA

Penselin, D., Münsterkötter, M., Kirsten, S., Felder, M., Taudien, S., Platzer, M., Ashelford, K., Paskiewicz, K. H., Harrison, R. J., Hughes, D. J., Wolf, T., Shelest, E., Graap, J., Hoffmann, J., Wenzel, C., Wöltje, N., King, K. M., Fitt, B. D. L., Güldener, U., ... Knogge, W. (2016). Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses. BMC Genomics, 17(1), [953]. https://doi.org/10.1186/s12864-016-3299-5

Vancouver

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. / Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses. In: BMC Genomics. 2016 ; Vol. 17, No. 1.

Bibtex

@article{90176da9476148828c2d5752f5f39d7d,
title = "Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses",
abstract = "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.",
keywords = "CAZymes, Effectors, Host specificity, Leotiomycetes, Non-ribosomal peptide synthetases, Phylogenetic evolution, Polyketide synthases, Rhynchosporium, Sex-related genes, Whole genome sequencing",
author = "Daniel Penselin and Martin M{\"u}nsterk{\"o}tter and Susanne Kirsten and Marius Felder and Stefan Taudien and Matthias Platzer and Kevin Ashelford and Paskiewicz, {Konrad H.} and Harrison, {Richard J.} and Hughes, {David J.} and Thomas Wolf and Ekaterina Shelest and Jenny Graap and Jan Hoffmann and Claudia Wenzel and Nadine W{\"o}ltje and King, {Kevin M.} and Fitt, {Bruce D L} and Ulrich G{\"u}ldener and Anna Avrova and Wolfgang Knogge",
note = "{\textcopyright} The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.",
year = "2016",
month = nov,
day = "22",
doi = "10.1186/s12864-016-3299-5",
language = "English",
volume = "17",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",
number = "1",

}

RIS

TY - JOUR

T1 - Comparative genomics to explore phylogenetic relationship, cryptic sexual potential and host specificity of Rhynchosporium species on grasses

AU - Penselin, Daniel

AU - Münsterkötter, Martin

AU - Kirsten, Susanne

AU - Felder, Marius

AU - Taudien, Stefan

AU - Platzer, Matthias

AU - Ashelford, Kevin

AU - Paskiewicz, Konrad H.

AU - Harrison, Richard J.

AU - Hughes, David J.

AU - Wolf, Thomas

AU - Shelest, Ekaterina

AU - Graap, Jenny

AU - Hoffmann, Jan

AU - Wenzel, Claudia

AU - Wöltje, Nadine

AU - King, Kevin M.

AU - Fitt, Bruce D L

AU - Güldener, Ulrich

AU - Avrova, Anna

AU - Knogge, Wolfgang

N1 - © The Author(s). 2016 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

PY - 2016/11/22

Y1 - 2016/11/22

N2 - 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.

AB - 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.

KW - CAZymes

KW - Effectors

KW - Host specificity

KW - Leotiomycetes

KW - Non-ribosomal peptide synthetases

KW - Phylogenetic evolution

KW - Polyketide synthases

KW - Rhynchosporium

KW - Sex-related genes

KW - Whole genome sequencing

UR - http://www.scopus.com/inward/record.url?scp=85003441492&partnerID=8YFLogxK

U2 - 10.1186/s12864-016-3299-5

DO - 10.1186/s12864-016-3299-5

M3 - Article

AN - SCOPUS:85003441492

VL - 17

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 953

ER -