The Flower-Infecting Fungus Ustilaginoidea virens Subverts Plant Immunity by Secreting a Chitin-Binding Protein

Abstract

Ustilaginoidea virens is a biotrophic fungal pathogen specifically colonizing rice floral organ and causes false smut disease of rice. This disease has emerged as a serious problem that hinders the application of high-yield rice cultivars, by reducing grain yield and quality as well as introducing mycotoxins. However, the pathogenic mechanisms of U. virens are still enigmatic. Here we demonstrate that U. virens employs a secreted protein UvCBP1 to manipulate plant immunity. In planta expression of UvCBP1 led to compromised chitin-induced defense responses in Arabidopsis and rice, including burst of reactive oxygen species (ROS), callose deposition, and expression of defense-related genes. In vitro-purified UvCBP1 protein competes with rice chitin receptor OsCEBiP to bind to free chitin, thus impairing chitin-triggered rice immunity. Moreover, UvCBP1 could significantly promote infection of U. virens in rice flowers. Our results uncover a mechanism of a floral fungus suppressing plant immunity and pinpoint a universal role of chitin-battlefield during plant–fungi interactions.

Ustilaginoidea virens‐secreted effector Uv1809 suppresses rice immunity by enhancing OsSRT2‐mediated histone deacetylation

“…Recently, the RNAi‐based approach host‐induced gene silencing (HIGS) was developed as an alternative strategy to control fungal diseases. In this strategy, siRNAs targeting selected genes of the invading pathogen are produced by transgenic host plants to silence fungal genes during infection (Chen et al ., 2022c ; Li et al ., 2021a , b ; Machado et al ., 2018 ; Nowara et al ., 2010 ). For example, HIGS of FgChs3b , FgCYP51 , FgSGE1 , FgFGP1 , or FgSTE12 conferred resistance to Fusarium head blight fungus Fusarium graminearum in wheat ( Triticum aestivum ) (Cheng et al ., 2015 ; Koch et al ., 2013 ; Wang et al ., 2020a , b ).…”

“…virens based on genomic analysis (Zhang et al ., 2014, 2021). Recent studies have demonstrated that a number of these effectors play critical roles in infection, including SCRE1, SCRE4, SCRE6, SGP1, UvCBP1, UvPr1a, and UvSec117 (Chen et al ., 2022a,b; Li et al ., 2021a; Qiu et al ., 2022; Song et al ., 2021; Yang et al ., 2022; Zhang et al., 2020; Zheng et al ., 2022). For example, the effector SCRE6 acts as a tyrosine phosphatase that dephosphorylates the negative defence regulator OsMPK6 (MAP Kinase) to enhance its accumulation, thereby inhibiting rice immunity (Zheng et al ., 2022).…”

Golovinomyces cichoracearum effector‐associated nuclear localization of RPW8.2 amplifies its expression to boost immunity in Arabidopsis

“…To verify the functionality of GcR8IP1 signal peptide, plasmids of pSUC2‐GcR8IP1 16aa , pSUC2‐GcR8IP1 26aa , pSUC2‐GcR8IP1 40aa , pSUC2‐Avr1b SP , and pSUC2‐Mg87 N were separately transformed into yeast strain YTK12 and subjected to yeast secretion assay as performed previously (Li et al ., 2021). To further confirm the functionality of GcR8IP1 40aa in secretion, GcR8IP1 40aa ‐GFP was transiently expressed in N. benthamiana leaves and treated with/without 12% (w/v) sucrose solution for 10 min, before observation under a confocal laser scanning microscope (Nikon A1).…”

SnRK1A‐mediated phosphorylation of a cytosolic ATPase positively regulates rice innate immunity and is inhibited by Ustilaginoidea virens effector SCRE1

“…SCRE6 functions as a tyrosine phosphatase and dephosphorylates the negative immune regulator OsMPK6, thus stabilizing OsMPK6 and inhibiting rice immunity (Zheng et al ., 2022). The chitin‐binding protein UvCBP1 in U. virens competes with rice chitin receptor OsCEBiP for chitin binding, and thereby subverts pattern‐triggered immunity (Li et al ., 2021). Interestingly, a Ser‐Thr‐rich GPI‐anchored protein (SGP1) in U. virens functions as a PAMP and induces plant immune responses, although the protein is critical for pathogen virulence (Song et al ., 2021).…”