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

Yu-Han Lin, Meng-Yun Xu, Chuan-Chih Hsu, Florensia Ariani Damei, Hui-Chun Lee, Wei-Lun Tsai, Cuong V. Hoang, Yin-Ru Chiang and Lay-Sun Ma ()
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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

Nature Communications, 2023, vol. 14, issue 1, 1-14

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-41459-4

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