The essential effector SCRE1 in Ustilaginoidea virens suppresses rice immunity via a small peptide region

Abstract

Summary The biotrophic fungal pathogen Ustilaginoidea virens causes rice false smut, a newly emerging plant disease that has become epidemic worldwide in recent years. The U. virens genome encodes many putative effector proteins that, based on the study of other pathosystems, could play an essential role in fungal virulence. However, few studies have been reported on virulence functions of individual U. virens effectors. Here, we report our identification and characterization of the secreted cysteine‐rich protein SCRE1, which is an essential virulence effector in U. virens. When SCRE1 was heterologously expressed in Magnaporthe oryzae, the protein was secreted and translocated into plant cells during infection. SCRE1 suppresses the immunity‐associated hypersensitive response in the nonhost plant Nicotiana benthamiana. Induced expression of SCRE1 in rice also inhibits pattern‐triggered immunity and enhances disease susceptibility to rice bacterial and fungal pathogens. The immunosuppressive activity is localized to a small peptide region that contains an important ‘cysteine‐proline‐alanine‐arginine‐serine’ motif. Furthermore, the scre1 knockout mutant generated using the CRISPR/Cas9 system is attenuated in U. virens virulence to rice, which is greatly complemented by the full‐length SCRE1 gene. Collectively, this study indicates that the effector SCRE1 is able to inhibit host immunity and is required for full virulence of U. virens.

Mapping quantitative trait loci for disease resistance to false smut of rice

“…Interestingly, the pathogen might hijack rice nutrient supply system to benefit the formation of false smut balls by simulating ovule fertilization (Fan et al 2015;Song et al 2016). Furthermore, U. virens genome and the predicted protein-protein interaction network greatly accelerate progress in identifying pathogenicity factors and understanding effector biology in this pathogen (Zhang et al 2017;Fan et al 2019;Fang et al 2019;Sun et al 2020;Zhang et al 2020).…”

Insights into the susceptibility of rice to a floral disease

“…To further confirm whether UvChi1 could be secreted, a multiclonal antibody against UvChi1 in rabbits using the synthetic peptide GRADPSPQGEDLTTSC was raised at Hangzhou Hua'an Biotechnology Co., Ltd, China. U. virens PJ52 was cultured in PSB for seven days, and then mycelia and culture supernatant were separated for protein extraction following a previous report (Zhang et al, 2020). The proteins were separated in 10% SDS-PAGE gels and subjected to Western blot using anti-UvChi1 and anti-GAPDH antibodies.…”

“…Particularly, effector proteins such as SCRE1, UV_1261/SCRE2, and UV_5215 could inhibit cell death and/or pattern-triggered immunity (PTI) in plants. SCRE1 and UV_1261/SCRE2 both contribute to the virulence of U. virens in rice flower (Zhang et al, 2014; Fan et al, 2019; Fang et al, 2019; Zhang et al, 2020). However, their host targets and virulence mechanisms are unknown.…”

“…SCRE1 and UV_1261/SCRE2 both contribute to the virulence of U. virens in rice flower (Zhang et al, 2014;Fan et al, 2019;Fang et al, 2019;Zhang et al, 2020). However, their host targets and virulence mechanisms are unknown.…”

Candidate Effectors from Botryosphaeria dothidea Suppress Plant Immunity and Contribute to Virulence

“…Thirteen putative effectors from Ustilaginoidea virens caused necrosis or necrosis-like phenotypes in N. benthamiana [ 29 ]. In addition, U. virens effector SCRE1 could suppress rice immunity via a small peptide region [ 30 ]. In the woody plant pathogen Valsa mali , the VmHEP1 and VmHEP2 effectors were able to suppress PCD elicited by BAX in N. benthamiana leaves, and the double deletion of VmHEP1 and VmHEP2 notably attenuated V. mali virulence in both apple twigs and leaves [ 31 ].…”