The adenylate cyclase UvAc1 and phosphodiesterase UvPdeH control the intracellular cAMP level, development, and pathogenicity of the rice false smut fungus Ustilaginoidea virens

Guo, Weiwen; Gao, Yixin; Yu, Zhaomeng; Xiao, Yuhan; Zhang, Haifeng

doi:10.1016/j.fgb.2019.04.017

Cited by 34 publications

(36 citation statements)

References 53 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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“…In U. virens, UvPmk1, UvCdc2, UvPro1, UvBI-1, UvAc1, UvPdeh, UvPsr1, UvCom1, UvHox2, and UvAtg8 are involved in both various stresses responses and pathogenesis (Lv et al, 2016, Guo et al, 2019, Tang et al, 2019. However, it is not clear whether and how defects of stress responses affect the pathogenesis processes of U. virens.…”

Section: Discussionmentioning

confidence: 99%

“…Rice false smut disease is caused by the ascomycete filamentous fungus Ustilaginoidea virens, which has emerged to be one of the most devastating rice fungal diseases in the rice-cultivated areas (Fan et al, 2016, Liang et al, 2018, Guo et al, 2019, Sun et al, 2020. The occurrence of rice false smut seriously affects high and stable yield and quality of rice (Lu et al, 2015, Zheng et al, 2017, Lin et al, 2018.…”

Section: Introductionmentioning

confidence: 99%

“…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%

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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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“…This result suggested that knockout of mrPDE could inhibit the cAMP degradation, which led to a higher intracellular cAMP concentration. It has been reported that deletion of PDE gene in Ustilaginoidea virens and Magnaporthe oryzae both resulted in double-fold increase in cAMP concentration [21,34]. Thus, it was ascertained that deletion of PDE gene could e ciently increase cAMP concentration in M. purpureus HJ11.…”

Section: Activation Of Camp Signalling Pathway By Mrpde Knockoutmentioning

confidence: 99%

Enhancement of Monascus Azaphilone Pigments Production by Activating the cAMP Signalling Pathway in Monascus Purpureus HJ11

Liu

et al. 2020

Preprint

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Background: Monascus azaphilone pigments (MonAzPs), which were produced by Monascus species, have been used as important food colorant and food supplements for more than one billion people during their daily life. Moreover, MonAzPs recently have received more attention because of their diverse physiological activities. However, the high microbial production of MonAzPs is still not always guaranteed. Herein, the aim of this study was to develop an efficient biotechnological process for MonAzPs production.Results: In this study, exogenous cyclic adenosine monophosphate (cAMP) treatment not only induced MonAzPs production, but also stimulated the expression of a cAMP phosphodiesterase gene, named as mrPDE, in M. purpureus HJ11. Subsequently, MrPDE was identified as a cAMP phosphodiesterase by in vitro enzymatic reaction with purified enzyme. Further, a gene knockout mutant of mrPDE was constructed to verify the activation of cAMP signalling pathway. Deletion of mrPDE in M. purpureus HJ11 improved cAMP concentration by 378 % and enhanced PKA kinase activity 1.5-fold, indicating that activation of cAMP signalling pathway was achieved. The ΔmrPDE strain produced MonAzPs at 8563 U/g, with a 2.3-fold increase compared with the WT strain. Moreover, the NAPDH/NADP+ ratio of the ΔmrPDE strain was obviously higher than that of the wild type strain, which led to a higher proportion of yellow MonAzPs. With fed-batch fermentation of the ΔmrPDE strain, the production and yield of MonAzPs achieved 332.1 U/mL and 8739 U/g.Conclusions: A engineered M. purpureus strain for high MonAzPs production was successfully developed by activating the cAMP signalling pathway. This study not only describes a novel strategy for development of MonAzPs-producing strain, but also provides a roadmap for engineering efforts towards the production of secondary metabolism in other filamentous fungi.

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The adenylate cyclase UvAc1 and phosphodiesterase UvPdeH control the intracellular cAMP level, development, and pathogenicity of the rice false smut fungus Ustilaginoidea virens

Cited by 34 publications

References 53 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

UvWHI2 is Required for Stress Response and Pathogenicity in Ustilaginonidea Virens

Enhancement of Monascus Azaphilone Pigments Production by Activating the cAMP Signalling Pathway in Monascus Purpureus HJ11

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