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Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence

Author

Listed:
  • Yaohua You

    (Wageningen University
    RWTH University)

  • H. M. Suraj

    (Wageningen University
    Technische Universität Braunschweig)

  • Linda Matz

    (Technische Universität Braunschweig)

  • A. Lorena Herrera Valderrama

    (Wageningen University)

  • Paul Ruigrok

    (Wageningen University)

  • Xiaoqian Shi-Kunne

    (Wageningen University)

  • Frank P. J. Pieterse

    (Wageningen University)

  • Anne Oostlander

    (Technische Universität Braunschweig)

  • Henriek G. Beenen

    (Wageningen University)

  • Edgar A. Chavarro-Carrero

    (Wageningen University)

  • Si Qin

    (Wageningen University
    University of California Davis)

  • Francel W. A. Verstappen

    (Wageningen University)

  • Iris F. Kappers

    (Wageningen University)

  • André Fleißner

    (Technische Universität Braunschweig)

  • Jan A. L. Kan

    (Wageningen University)

Abstract

Saponins are plant secondary metabolites comprising glycosylated triterpenoids, steroids or steroidal alkaloids with a broad spectrum of toxicity to microbial pathogens and pest organisms that contribute to basal plant defense to biotic attack. Secretion of glycosyl hydrolases that enzymatically convert saponins into less toxic products was thus far the only mechanism reported to enable fungal pathogens to colonize their saponin-containing host plant(s). We studied the mechanisms that the fungus Botrytis cinerea utilizes to be tolerant to well-characterized, structurally related saponins from tomato and Digitalis purpurea. By gene expression studies, comparative genomics, enzyme assays and testing a large panel of fungal (knockout and complemented) mutants, we unraveled four distinct cellular mechanisms that participate in the mitigation of the toxic activity of these saponins and in virulence on saponin-producing host plants. The enzymatic deglycosylation that we identified is novel and unique to this fungus-saponin combination. The other three tolerance mechanisms operate in the fungal membrane and are mediated by protein families that are widely distributed in the fungal kingdom. We present a spatial and temporal model on how these mechanisms jointly confer tolerance to saponins and discuss the repercussions of these findings for other plant pathogenic fungi, as well as human pathogens.

Suggested Citation

  • Yaohua You & H. M. Suraj & Linda Matz & A. Lorena Herrera Valderrama & Paul Ruigrok & Xiaoqian Shi-Kunne & Frank P. J. Pieterse & Anne Oostlander & Henriek G. Beenen & Edgar A. Chavarro-Carrero & Si Q, 2024. "Botrytis cinerea combines four molecular strategies to tolerate membrane-permeating plant compounds and to increase virulence," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50748-5
    DOI: 10.1038/s41467-024-50748-5
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    References listed on IDEAS

    as
    1. David Vela-Corcía & Dhruv Aditya Srivastava & Avis Dafa-Berger & Neta Rotem & Omer Barda & Maggie Levy, 2019. "MFS transporter from Botrytis cinerea provides tolerance to glucosinolate-breakdown products and is required for pathogenicity," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    2. Ying Chen & Fan Nie & Shang-Qian Xie & Ying-Feng Zheng & Qi Dai & Thomas Bray & Yao-Xin Wang & Jian-Feng Xing & Zhi-Jian Huang & De-Peng Wang & Li-Juan He & Feng Luo & Jian-Xin Wang & Yi-Zhi Liu & Chu, 2021. "Efficient assembly of nanopore reads via highly accurate and intact error correction," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    3. K. Bouarab & R. Melton & J. Peart & D. Baulcombe & A. Osbourn, 2002. "A saponin-detoxifying enzyme mediates suppression of plant defences," Nature, Nature, vol. 418(6900), pages 889-892, August.
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