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

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.

MoPce1, a Cap/PR Domain Containing Effector Is Required for the Pathogenicity of Magnaporthe oryzae by Interacting with the OsDi19-5 in Rice

“…Although direct evidence is still lacking for the role of sterol binding of CAP domain during infection of fungal pathogens, study in tobacco PR-1 revealed that plants could inhibit pathogen growth through the sequestration of sterol from pathogens by PR-1 protein [42]. In U. maydis, UmPR-1La not only participates in sensing phenolics and eliciting hyphal-like formation, but also releases CAPE-like peptides to subvert plant immunity [31]. Besides, pathogens evolved specific clade of CAP protein lacking the conserved cysteine residues required for intramolecular disulfide bridges, and were proposed to bind novel ligands [36].…”

“…In Cytospora chrysosperma, CcCAP1 is required for the suppression of immunity in poplar plants [29]. So far, only a few studies demonstrated that the CAP proteins are required for lipid export and sterol binding in fungus [30], and a recent study in Ustilago maydis uncovered that it could hijack maize cathepsin B-like 3 (CatB3) to cleave the PR1-like protein UmPR-1La, leading to the release of functional CAPE-like peptides for the interruption of plant CAPE mediated immunity [31]. However, whether these CAP proteins function could target other ligands or proteins during infection remain largely unknown.…”

How plants manage pathogen infection

“…2C ). Nevertheless, the importance of PR1 in plant immunity is evident, reflected by the fact that pathogen effectors target PR1 (Breen et al, 2016 ; Li et al, 2022 ; Lin et al 2023 ). Other PR proteins such as PR2, PR5, defensin (PR12), and thionin (PR13) appear to have an activity to disrupt pathogen cell walls and the plasma membrane (Boccardo et al, 2019 ; Rayapuram et al, 2008 ; Zribi et al, 2021 ).…”