A Novel Effector Gene SCRE2 Contributes to Full Virulence of Ustilaginoidea virens to Rice

Fang, Anfei; Gao, Han; Zhang, Nan; Zheng, Xinhang; Qiu, Shanshan; Li, Yuejiao; Zhou, Shuang; Cui, Fuhao; Sun, Wenxian

doi:10.3389/fmicb.2019.00845

Cited by 61 publications

(61 citation statements)

References 82 publications

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“…Although the genomic sequences of U. virens have been released, there are only a small number of pathogenicity-related genes which have been functionally characterized and experimentally verified as pathogenic factors (Qiu et al 2019). These pathogenic factors include low-affinity iron transporter Uvt3277, hypothetical protein UvPro1, adenylate cyclase UvAc1, phosphodiesterase UvPdeH, effector Scre2 (Uv-1261), Bax inhibitor UvBI-1, two protein kinases UvPmk1 and UvCDC2, and transcription factor UvCom1 (Zheng et al 2017;Xie et al 2019;Tang et al 2019;Lv et al 2016;Guo et al 2019;Fang et al 2019;Fan et al 2019;Chen et al 2019). In this study, UvATG8 was characterized as a pathogenic factor.…”

Section: Discussionmentioning

confidence: 99%

UvAtg8-Mediated Autophagy Regulates Fungal Growth, Stress Responses, Conidiation, and Pathogenesis in Ustilaginoidea virens

Meng

Xiong

Jagernath

et al. 2020

Rice

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Background: Ustilaginoidea virens has become one of the most devastating rice pathogens in China, as well as other rice-growing areas. Autophagy is an important process in normal cell differentiation and development among various organisms. To date, there has been no optimized experimental system introduced for the study of autophagy in U. virens. In addition, the function of autophagy in pathogenesis remains unknown in U. virens. Therefore, the functional analyses of UvAtg8 may potentially shed some light on the regulatory mechanism and function of autophagy in U. virens. Results: In this study, we characterized the functions of UvAtg8, which is a homolog of Saccharomyces cerevisiae ScAtg8, in the rice false smut fungus U. virens. The results showed that UvATG8 is essential for autophagy in U. virens. Also, the GFP-UvATG8 strain, which could serve as an appropriate marker for monitoring autophagy in U. virens, was generated. Furthermore, this study found that the ΔUvatg8 mutant was defective in the vegetative growth, conidiation, adaption to oxidative, hyperosmotic, cell wall stresses, and production of toxic compounds. Pathogenicity assays indicated that deletion of UvATG8 resulted in significant reduction in virulence of U. virens. Further microscopic examinations of the infection processes revealed that the severe virulence defects in the ΔUvatg8 were mainly caused by the highly reduced conidiation and secondary spore formation. Conclusions: Our results indicated that the UvAtg8 is necessary for the fungal growth, stresses responses, conidiation, secondary spore formation, and pathogenicity of U. virens. Moreover, our research finding will potentially assist in further clarifying the molecular mechanism of U. virens infection, as well as provide a good marker for autophagy in U. virens and a good reference value for the further development of effective fungicides based on gene targeting.

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Section: Discussionmentioning

confidence: 99%

UvAtg8-Mediated Autophagy Regulates Fungal Growth, Stress Responses, Conidiation, and Pathogenesis in Ustilaginoidea virens

Meng

Xiong

Jagernath

et al. 2020

Rice

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“…As controls, SCRE2‐mCherry was clearly observed in periplasmic spaces of plasmolysed cells, while SCRE2‐SP‐mCherry was not (Fig. ; Fang et al , ). Collectively, these data suggest that SCRE1, as a secreted protein, is taken up inside plant cells and functions as a suppressor of immunity‐associated cell death in plants.…”

Section: Resultsmentioning

confidence: 87%

“…A. tumefaciens strains carrying pGR107‐ INF1 or pGR107‐ BAX were infiltrated together with different truncated constructs of SCRE1 or at 6 h after infiltration of different SCRE1 constructs. Subcellular localization of SCRE1‐mCherry and SCRE1‐SP‐mCherry was performed as described previously (Fang et al , ).…”

Section: Methodsmentioning

confidence: 99%

“…On the other hand, when delivered by the type III secretion system of the bacterium Burkholderia glumae , many putative U. virens effectors were found to suppress B. glumae ‐induced hypersensitive cell death in N. benthamiana (Zhang et al ., ). The U. virens secreted cysteine‐rich effector (SCRE) SCRE2 (UV_1261) has been recently demonstrated to be an essential virulence factor (Fan et al , ; Fang et al , ).…”

Section: Introductionmentioning

confidence: 99%

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

Zhang

Yang

Fang

et al. 2020

Molecular Plant Pathology

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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.

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“…Thus far, only few pathogenesis-related proteins have been identified and characterized in U. virens, including the hypothetical protein UvPro1, the low-affinity iron transporter Uvt3277, two protein kinases UvPmk1 and UvCDC2, the cyclic adenosine monophosphate signaling proteins adenylate cyclase UvAc1 and phosphodiesterase UvPdeH, the Bax inhibitor UvBI-1, the effector Scre2 (Uv_1261), two transcriptional factors UvHox2 and UvCom1, the phosphatase UvPsr1, and the autophagy-related protein UvAtg8 (Lv et al, 2016, Zheng et al, 2017, Fang et al, 2019, Guo et al, 2019, Tang et al, 2019, Chen et al, 2020. Among these, UvPmk1, UvCdc2, UvPro1, UvBI-1, UvAc1, UvPdeh, UvPsr1, UvCom1, UvHox2, and UvAtg8 are involved in both various stresses responses and pathogenesis of U. virens.…”

Section: Introductionmentioning

confidence: 99%

UvWHI2 is Required for Stress Response and Pathogenicity in Ustilaginonidea Virens

Meng¹,

Qiu²,

Xiong³

et al. 2020

Preprint

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Background: Ustilaginoidea virens causes rice false smut disease, which emerges as a worldwide disease of rice. At present, some stress response related genes have been identified in U. virens , but it is not clear whether and how defects of stress responses affect the pathogenesis processes of U. virens . To answer this question, the function of a general stress response factor Whi2 was analyzed in U. virens . Results: In this study, we identified UvWhi2 as a homolog of Saccharomyces cerevisiae Whi2 in U. virens. The relative expression level of UvWhi2 was significantly up-regulated during infection, suggesting that UvWhi2 may be involved in pathogenesis. Furthermore, knockout of UvWhi2 showed decreased the mycelial growth, increased in conidiation in the PS (potato sucrose) medium and a defect in pathogenicity. In addition, the RNA-Seq and phenotypic analysis showed that UvWHI2 is involved in response to oxidative, hyperosmotic, cell wall stresses, and nutrient limitation. Further studies revealed that the defects of stress responses of the ∆ Uvwhi2 mutant affected the formation of secondary spores on the nutrient limited surface and the rice surface, resulting in a significant reduction of pathogenicity of U. virens . Conclusions: Our results suggest that UvWhi2 is necessary for fungal growth, stress responses, and the formation of secondary spores in U. virens . In addition, the defects of stress responses could affect the formation of secondary spores on the rice surface, and then compromise the pathogenicity of U. virens .

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A Novel Effector Gene SCRE2 Contributes to Full Virulence of Ustilaginoidea virens to Rice

Cited by 61 publications

References 82 publications

UvAtg8-Mediated Autophagy Regulates Fungal Growth, Stress Responses, Conidiation, and Pathogenesis in Ustilaginoidea virens

UvAtg8-Mediated Autophagy Regulates Fungal Growth, Stress Responses, Conidiation, and Pathogenesis in Ustilaginoidea virens

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

UvWHI2 is Required for Stress Response and Pathogenicity in Ustilaginonidea Virens

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