TY - JOUR

T1 - Evolutionary relics dominate the small number of secondary metabolism genes in the hemibiotrophic fungus Dothistroma septosporum

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.

PY - 2019/5

Y1 - 2019/5

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.

AB - 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.

KW - Dothideomycete

KW - Fungal gene cluster

KW - Nonribosomal peptide

KW - Polyketide

KW - Secondary metabolite

KW - Squalestatin

UR - http://www.scopus.com/inward/record.url?scp=85062426648&partnerID=8YFLogxK

U2 - 10.1016/j.funbio.2019.02.006

DO - 10.1016/j.funbio.2019.02.006

M3 - Article

C2 - 31053329

AN - SCOPUS:85062426648

VL - 123

SP - 397

EP - 407

JO - Fungal biology

JF - Fungal biology

SN - 1878-6146

IS - 5

ER -