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Ustilago maydis PR-1-like protein has evolved two distinct domains for dual virulence activities

Author

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  • Yu-Han Lin

    (Institute of Plant and Microbial Biology, Academia Sinica)

  • Meng-Yun Xu

    (Institute of Plant and Microbial Biology, Academia Sinica)

  • Chuan-Chih Hsu

    (Institute of Plant and Microbial Biology, Academia Sinica)

  • Florensia Ariani Damei

    (Institute of Plant and Microbial Biology, Academia Sinica)

  • Hui-Chun Lee

    (Institute of Plant and Microbial Biology, Academia Sinica)

  • Wei-Lun Tsai

    (Institute of Plant and Microbial Biology, Academia Sinica)

  • Cuong V. Hoang

    (Institute of Plant and Microbial Biology, Academia Sinica)

  • Yin-Ru Chiang

    (Biodiversity Research Center, Academia Sinica)

  • Lay-Sun Ma

    (Institute of Plant and Microbial Biology, Academia Sinica)

Abstract

The diversification of effector function, driven by a co-evolutionary arms race, enables pathogens to establish compatible interactions with hosts. Structurally conserved plant pathogenesis-related PR-1 and PR-1-like (PR-1L) proteins are involved in plant defense and fungal virulence, respectively. It is unclear how fungal PR-1L counters plant defense. Here, we show that Ustilago maydis UmPR-1La and yeast ScPRY1, with conserved phenolic resistance functions, are Ser/Thr-rich region mediated cell-surface localization proteins. However, UmPR-1La has gained specialized activity in sensing phenolics and eliciting hyphal-like formation to guide fungal growth in plants. Additionally, U. maydis hijacks maize cathepsin B-like 3 (CatB3) to release functional CAPE-like peptides by cleaving UmPR-1La’s conserved CNYD motif, subverting plant CAPE-primed immunity and promoting fungal virulence. Surprisingly, CatB3 avoids cleavage of plant PR-1s, despite the presence of the same conserved CNYD motif. Our work highlights that UmPR-1La has acquired additional dual roles to suppress plant defense and sustain the infection process of fungal pathogens.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41459-4
    DOI: 10.1038/s41467-023-41459-4
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    References listed on IDEAS

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    1. Jörg Kämper & Regine Kahmann & Michael Bölker & Li-Jun Ma & Thomas Brefort & Barry J. Saville & Flora Banuett & James W. Kronstad & Scott E. Gold & Olaf Müller & Michael H. Perlin & Han A. B. Wösten &, 2006. "Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis," Nature, Nature, vol. 444(7115), pages 97-101, November.
    2. 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.
    3. Johana C. Misas Villamil & André N. Mueller & Fatih Demir & Ute Meyer & Bilal Ökmen & Jan Schulze Hüynck & Marlen Breuer & Helen Dauben & Joe Win & Pitter F. Huesgen & Gunther Doehlemann, 2019. "A fungal substrate mimicking molecule suppresses plant immunity via an inter-kingdom conserved motif," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    4. Ying-Lan Chen & Fan-Wei Lin & Kai-Tan Cheng & Chi-Hsin Chang & Sheng-Chi Hung & Thomas Efferth & Yet-Ran Chen, 2023. "XCP1 cleaves Pathogenesis-related protein 1 into CAPE9 for systemic immunity in Arabidopsis," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
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