Evolutionary relics dominate the small number of secondary metabolism genes in the hemibiotrophic fungus Dothistroma septosporum

Research output: Contribution to journalArticleResearchpeer review

Authors

  • I. Kutay Ozturk
  • Pierre Yves Dupont
  • Pranav Chettri
  • Rebecca McDougal
  • Ole Jacob Böhl
  • Russell John Cox
  • Rosie E. Bradshaw

Research Organisations

External Research Organisations

  • Massey University
  • Environmental Sciences Research
  • New Zealand Forest Research Institute Limited
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Details

Original languageEnglish
Pages (from-to)397-407
Number of pages11
JournalFungal biology
Volume123
Issue number5
Early online date27 Feb 2019
Publication statusPublished - May 2019

Abstract

Fungal secondary metabolites have important functions for the fungi that produce them, such as roles in virulence and competition. The hemibiotrophic pine needle pathogen Dothistroma septosporum has one of the lowest complements of secondary metabolite (SM) backbone genes of plant pathogenic fungi, indicating that this fungus produces a limited range of SMs. Amongst these SMs is dothistromin, a well-characterised polyketide toxin and virulence factor that is required for expansion of disease lesions in Dothistroma needle blight disease. Dothistromin genes are dispersed across six loci on one chromosome, rather than being clustered as for most SM genes. We explored other D. septosporum SM genes to determine if they are associated with gene clusters, and to predict what their likely products and functions might be. Of nine functional SM backbone genes in the D. septosporum genome, only four were expressed under a range of in planta and in culture conditions, one of which was the dothistromin PKS backbone gene. Of the other three expressed genes, gene knockout studies suggested that DsPks1 and DsPks2 are not required for virulence and attempts to determine a functional squalestatin-like SM product for DsPks2 were not successful. However preliminary evidence suggested that DsNps3, the only SM backbone gene to be most highly expressed in the early stage of disease, appears to be a virulence factor. Thus, despite the small number of SM backbone genes in D. septosporum, most of them appear to be poorly expressed or dispensable for virulence in planta. This work contributes to a growing body of evidence that many fungal secondary metabolite gene clusters might be non-functional and may be evolutionary relics.

Keywords

    Dothideomycete, Fungal gene cluster, Nonribosomal peptide, Polyketide, Secondary metabolite, Squalestatin

ASJC Scopus subject areas

Sustainable Development Goals

Cite this

Evolutionary relics dominate the small number of secondary metabolism genes in the hemibiotrophic fungus Dothistroma septosporum. / Ozturk, I. Kutay; Dupont, Pierre Yves; Chettri, Pranav et al.
In: Fungal biology, Vol. 123, No. 5, 05.2019, p. 397-407.

Research output: Contribution to journalArticleResearchpeer review

Ozturk IK, Dupont PY, Chettri P, McDougal R, Böhl OJ, Cox RJ et al. Evolutionary relics dominate the small number of secondary metabolism genes in the hemibiotrophic fungus Dothistroma septosporum. Fungal biology. 2019 May;123(5):397-407. Epub 2019 Feb 27. doi: 10.1016/j.funbio.2019.02.006
Ozturk, I. Kutay ; Dupont, Pierre Yves ; Chettri, Pranav et al. / Evolutionary relics dominate the small number of secondary metabolism genes in the hemibiotrophic fungus Dothistroma septosporum. In: Fungal biology. 2019 ; Vol. 123, No. 5. pp. 397-407.
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title = "Evolutionary relics dominate the small number of secondary metabolism genes in the hemibiotrophic fungus Dothistroma septosporum",
abstract = "Fungal secondary metabolites have important functions for the fungi that produce them, such as roles in virulence and competition. The hemibiotrophic pine needle pathogen Dothistroma septosporum has one of the lowest complements of secondary metabolite (SM) backbone genes of plant pathogenic fungi, indicating that this fungus produces a limited range of SMs. Amongst these SMs is dothistromin, a well-characterised polyketide toxin and virulence factor that is required for expansion of disease lesions in Dothistroma needle blight disease. Dothistromin genes are dispersed across six loci on one chromosome, rather than being clustered as for most SM genes. We explored other D. septosporum SM genes to determine if they are associated with gene clusters, and to predict what their likely products and functions might be. Of nine functional SM backbone genes in the D. septosporum genome, only four were expressed under a range of in planta and in culture conditions, one of which was the dothistromin PKS backbone gene. Of the other three expressed genes, gene knockout studies suggested that DsPks1 and DsPks2 are not required for virulence and attempts to determine a functional squalestatin-like SM product for DsPks2 were not successful. However preliminary evidence suggested that DsNps3, the only SM backbone gene to be most highly expressed in the early stage of disease, appears to be a virulence factor. Thus, despite the small number of SM backbone genes in D. septosporum, most of them appear to be poorly expressed or dispensable for virulence in planta. This work contributes to a growing body of evidence that many fungal secondary metabolite gene clusters might be non-functional and may be evolutionary relics.",
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AU - Ozturk, I. Kutay

AU - Dupont, Pierre Yves

AU - Chettri, Pranav

AU - McDougal, Rebecca

AU - Böhl, Ole Jacob

AU - Cox, Russell John

AU - Bradshaw, Rosie E.

N1 - Funding information: This work was supported by Massey University and the Tertiary Education Commission (NZ) through the Bio-Protection Research Center. We acknowledge the assistance of Karen Lebe (University of Hannover) for the synthesis of benzoyl SNAC, and DFG (grant INST 187/621) for the provision of LCMS equipment, Matthew Savoian (Massey University) for SEM imaging, Carla Eaton (Massey University) and Scott Griffiths (Westerdijk Fungal Biodiversity Institute) for early project planning, Paul Maclean (AgResearch NZ) for bioinformatics, Austen Ganley and Margaret Coe (University of Auckland) for preliminary LCMS analysis.

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N2 - Fungal secondary metabolites have important functions for the fungi that produce them, such as roles in virulence and competition. The hemibiotrophic pine needle pathogen Dothistroma septosporum has one of the lowest complements of secondary metabolite (SM) backbone genes of plant pathogenic fungi, indicating that this fungus produces a limited range of SMs. Amongst these SMs is dothistromin, a well-characterised polyketide toxin and virulence factor that is required for expansion of disease lesions in Dothistroma needle blight disease. Dothistromin genes are dispersed across six loci on one chromosome, rather than being clustered as for most SM genes. We explored other D. septosporum SM genes to determine if they are associated with gene clusters, and to predict what their likely products and functions might be. Of nine functional SM backbone genes in the D. septosporum genome, only four were expressed under a range of in planta and in culture conditions, one of which was the dothistromin PKS backbone gene. Of the other three expressed genes, gene knockout studies suggested that DsPks1 and DsPks2 are not required for virulence and attempts to determine a functional squalestatin-like SM product for DsPks2 were not successful. However preliminary evidence suggested that DsNps3, the only SM backbone gene to be most highly expressed in the early stage of disease, appears to be a virulence factor. Thus, despite the small number of SM backbone genes in D. septosporum, most of them appear to be poorly expressed or dispensable for virulence in planta. This work contributes to a growing body of evidence that many fungal secondary metabolite gene clusters might be non-functional and may be evolutionary relics.

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