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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 species Clonostachys rosea are used commercially as biological control agents for the control of fungal plant diseases in agricultural crop production. Further improvements of the use and efficacy of C. rosea in biocontrol require a mechanistic understanding of the factors that determines the outcome of the interaction between C. rosea and plant pathogenic fungi. Here, we determined the genome sequences of 11 Clonostachys strains, representing five species in Clonostachys subgenus Bionectria, 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 the Bionectria subgenus 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. Most Clonostachys species 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 the C. rosea genome 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 gene abcG6 in C. rosea was induced (p ? .009) by exposure to the antifungal Fusarium mycotoxin zearalenone (1121-fold) and various fungicides. Deletion of abcG6 resulted 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 in Clonostachys subgenus Bionectria.

SUBMITTER: Broberg M

PROVIDER: S-EPMC7896725 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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

Broberg Martin M Dubey Mukesh M Iqbal Mudassir M Gudmundssson Mikael M Ihrmark Katarina K Schroers Hans-Josef HJ Funck Jensen Dan D Brandström Durling Mikael M Karlsson Magnus M

Evolutionary applications 20200928 2

Various strains of the mycoparasitic fungal species Clonostachys rosea are used commercially as biological control agents for the control of fungal plant diseases in agricultural crop production. Further improvements of the use and efficacy of C. rosea in biocontrol require a mechanistic understanding of the factors that determines the outcome of the interaction between C. rosea and plant pathogenic fungi. Here, we determined the genome sequences of 11 Clonostachys st ...[more]

PMID: 33664789

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Project description:Serine proteases are a group of important hydrolytic enzymes that play vital roles in various cellular processes in fungi. In this study, the S8 serine protease-encoding gene CrKP43 was identified in the highly efficient Clonostachys chloroleuca 67-1 (formerly C. rosea 67-1) strain, which was markedly upregulated when parasitizing Sclerotinia sclerotiorum. The function of CrKP43 was investigated using gene deletion and complementation, and the results indicated that the lack of CrKP43 resulted in deformed fungal hyphae and cell morphology, inhibition of conidiation, and decreased antagonistic activity toward the pathogenic fungus Fusarium oxysporum f. sp. cucumerinum. Moreover, the mutants displayed much weaker mycoparasitic ability to S. sclerotiorum sclerotia and lower control efficiency against soybean Sclerotinia rot compared with the wild-type strain. All biological characteristics and biocontrol activities were recovered when the CrKP43 gene was reinserted into the fungus. Using qRT-PCR analysis and protein-protein interaction assays, it was further proved that the CrKP43 protein interacted with the mitogen-activated protein kinase (MAPK) Crmapk, suggesting serine proteases might be involved in the mycoparasitism of C. chloroleuca with the regulation of Crmapk. The findings improve our knowledge of serine proteases and their regulation in mycoparasites and help to illuminate the mechanisms underlying mycoparasitism of C. chloroleuca. IMPORTANCE Mycoparasites play important roles in the biocontrol of plant fungal diseases, during which they secret multiple hydrolases such as serine proteases to degrade their fungal hosts. In this study, we demonstrated that the serine protease CrKP43 was involved in C. chloroleuca development and mycoparasitism with the regulation of Crmapk. To the best of our knowledge, it is the first report on the functions and regulatory mechanisms of serine proteases in C. chloroleuca. Our findings will provide new insight into the regulatory mechanisms of serine proteases in mycoparasites and contribute to clarifying the mechanisms underlying mycoparasitism of C. chloroleuca, which will facilitate the development of highly efficient fungal biocontrol agents as well.

Dataset Information

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

Publications

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

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