Comparative genomics highlights the importance of drug efflux transporters during evolution of mycoparasitism in Clonostachys subgenus Bionectria (Fungi, Ascomycota, Hypocreales)

Abstract

Various strains of the mycoparasitic fungal speciesClonostachys roseaare used commercially as biological control agents for the control of fungal plant diseases in agricultural crop production. Further improvements of the use and efficacy ofC. roseain biocontrol require a mechanistic understanding of the factors that determines the outcome of the interaction betweenC. roseaand plant pathogenic fungi. Here, we determined the genome sequences of 11Clonostachysstrains, representing five species inClonostachyssubgenusBionectria, and performed a comparative genomic analysis with the aim to identify gene families evolving under selection for gene gains or losses. Several gene families predicted to encode proteins involved in biosynthesis of secondary metabolites, including polyketide synthases, nonribosomal peptide syntethases and cytochrome P450s, evolved under selection for gene gains (p <= .05) in theBionectriasubgenus lineage. This was accompanied with gene copy number increases (p <= .05) in ATP-binding cassette (ABC) transporters and major facilitator superfamily (MFS) transporters predicted to contribute to drug efflux. MostClonostachysspecies were also characterized by high numbers of auxiliary activity (AA) family 9 lytic polysaccharide monooxygenases, AA3 glucose-methanol-choline oxidoreductases and additional carbohydrate-active enzyme gene families with putative activity (or binding) towards xylan and rhamnose/pectin substrates. Particular features of theC. roseagenome included expansions (p <= .05) of the ABC-B4 multidrug resistance transporters, the ABC-C5 multidrug resistance-related transporters and the 2.A.1.3 drug:H + antiporter-2 MFS drug resistance transporters. The ABC-G1 pleiotropic drug resistance transporter geneabcG6inC. roseawas induced (p <= .009) by exposure to the antifungalFusariummycotoxin zearalenone (1121-fold) and various fungicides. Deletion ofabcG6resulted in mutants with reduced (p < .001) growth rates on media containing the fungicides boscalid, fenhexamid and iprodione. Our results emphasize the role of biosynthesis of, and protection against, secondary metabolites inClonostachyssubgenusBionectria.

Keywords

antagonism; biological control; Clonostachys; membrane transporter; mycoparasitism; xenobiotics

Published in

Evolutionary applications
2021, volume: 14, number: 2, pages: 476-497
Publisher: WILEY

SLU Authors

• Broberg, Martin

  • Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
    

• Dubey, Mukesh

  • Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
    

• Iqbal, Mudassir

  • Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
    

• Gudmundsson, Mikael

  • Department of Molecular Sciences, Swedish University of Agricultural Sciences
    

• Ihrmark, Katarina

  • Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
    

• Jensen, Dan Funck

  • Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
    

• Brandström Durling, Mikael

  • Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
    

• Karlsson, Magnus

  • Department of Forest Mycology and Plant Pathology, Swedish University of Agricultural Sciences
    

Associated SLU-program

SLU Plant Protection Network
AMR: Fungus

Global goals (SDG)

SDG2 Zero hunger
SDG3 Good health and well-being

UKÄ Subject classification

Evolutionary Biology

Publication identifier

• DOI: https://doi.org/10.1111/eva.13134

Permanent link to this page (URI)

https://res.slu.se/id/publ/108131