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The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins

Author

Listed:
  • Lay-Sun Ma

    (Max Planck Institute for Terrestrial Microbiology)

  • Lei Wang

    (Max Planck Institute for Terrestrial Microbiology
    Max Planck Institute for Heart and Lung Research)

  • Christine Trippel

    (Max Planck Institute for Terrestrial Microbiology
    Georg-August-University-Göttingen)

  • Artemio Mendoza-Mendoza

    (Max Planck Institute for Terrestrial Microbiology
    Lincoln University)

  • Steffen Ullmann

    (Max Planck Institute for Terrestrial Microbiology)

  • Marino Moretti

    (Max Planck Institute for Terrestrial Microbiology)

  • Alexander Carsten

    (Max Planck Institute for Terrestrial Microbiology)

  • Jörg Kahnt

    (Max Planck Institute for Terrestrial Microbiology)

  • Stefanie Reissmann

    (Max Planck Institute for Terrestrial Microbiology)

  • Bernd Zechmann

    (Baylor University)

  • Gert Bange

    (Philipps-Universität Marburg)

  • Regine Kahmann

    (Max Planck Institute for Terrestrial Microbiology)

Abstract

To cause disease in maize, the biotrophic fungus Ustilago maydis secretes a large arsenal of effector proteins. Here, we functionally characterize the repetitive effector Rsp3 (repetitive secreted protein 3), which shows length polymorphisms in field isolates and is highly expressed during biotrophic stages. Rsp3 is required for virulence and anthocyanin accumulation. During biotrophic growth, Rsp3 decorates the hyphal surface and interacts with at least two secreted maize DUF26-domain family proteins (designated AFP1 and AFP2). AFP1 binds mannose and displays antifungal activity against the rsp3 mutant but not against a strain constitutively expressing rsp3. Maize plants silenced for AFP1 and AFP2 partially rescue the virulence defect of rsp3 mutants, suggesting that blocking the antifungal activity of AFP1 and AFP2 by the Rsp3 effector is an important virulence function. Rsp3 orthologs are present in all sequenced smut fungi, and the ortholog from Sporisorium reilianum can complement the rsp3 mutant of U. maydis, suggesting a novel widespread fungal protection mechanism.

Suggested Citation

  • Lay-Sun Ma & Lei Wang & Christine Trippel & Artemio Mendoza-Mendoza & Steffen Ullmann & Marino Moretti & Alexander Carsten & Jörg Kahnt & Stefanie Reissmann & Bernd Zechmann & Gert Bange & Regine Kahm, 2018. "The Ustilago maydis repetitive effector Rsp3 blocks the antifungal activity of mannose-binding maize proteins," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-04149-0
    DOI: 10.1038/s41467-018-04149-0
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    Cited by:

    1. Yu-Han Lin & Meng-Yun Xu & Chuan-Chih Hsu & Florensia Ariani Damei & Hui-Chun Lee & Wei-Lun Tsai & Cuong V. Hoang & Yin-Ru Chiang & Lay-Sun Ma, 2023. "Ustilago maydis PR-1-like protein has evolved two distinct domains for dual virulence activities," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    2. Weiliang Zuo & Jasper R. L. Depotter & Sara Christina Stolze & Hirofumi Nakagami & Gunther Doehlemann, 2023. "A transcriptional activator effector of Ustilago maydis regulates hyperplasia in maize during pathogen-induced tumor formation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.

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