UvWhi2 Is Required for Stress Response and Pathogenicity in Ustilaginoidea virens
Received date: 2020-11-13
Accepted date: 2021-03-02
Online published: 2021-12-20
Some stress response-related genes have been identified in Ustilaginoidea virens, but it is not clear whether and how defects of stress responses affect the pathogenesis processes of U. virens. In this study, we identified a general stress response factor 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 mycelial growth, increased conidiation in the potato sucrose medium and a defect in pathogenicity. In addition, the RNA-Seq and phenotypic analysis showed that UvWHI2 was involved in response to oxidative, hyperosmotic, cell wall stress 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. 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 can affect the formation of secondary spores on the rice surface, and then compromise the pathogenicity of U. virens.
Key words： Whi2; rice false smut; Ustilaginoidea virens; pathogenesis; secondary spore
Meng Shuai, Qiu Jiehua, Xiong Meng, Liu Zhiquan, Jane Sadhna Jagernath, Lin Fucheng, Shi Huanbin, Kou Yanjun . UvWhi2 Is Required for Stress Response and Pathogenicity in Ustilaginoidea virens[J]. Rice Science, 2022 , 29(1) : 47 -54 . DOI: 10.1016/j.rsci.2021.12.004
| [1] | Boeckstaens M, Llinares E, van Vooren P, Marini A M. 2014. The TORC1 effector kinase Npr1 fine tunes the inherent activity of the Mep2 ammonium transport protein. Nat Commun, 5(1): 3101. |
| [2] | Chen X H, Wang G Q, Zhang Y, Dayhoff-Brannigan M, Diny N L, Zhao M J, He G, Sing C N, Metz K A, Stolp Z D, Aouacheria A, Cheng W C, Hardwick J M, Teng X C. 2018. Whi2 is a conserved negative regulator of TORC1 in response to low amino acids. PLoS Genet, 14(8): e1007592. |
| [3] | Chen X Y, Hai D, Tang J T, Liu H, Huang J B, Luo C X, Hsiang T, Zheng L. 2020. UvCom1 is an important regulator required for development and infection in the rice false smut fungus Ustilaginoidea virens. Phytopathology, 110(2): 483-493. |
| [4] | Egan M J, Wang Z Y, Jones M A, Smirnoff N, Talbot N J. 2007. Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci USA, 104(28): 11772-11777. |
| [5] | Fan J, Guo X Y, Huang F, Li Y, Liu Y F, Li L, Xu Y J, Zhao J Q, Xiong H, Yu J J, Wang W. 2014. Epiphytic colonization of Ustilaginoidea virens on biotic and abiotic surfaces implies the widespread presence of primary inoculum for rice false smut disease. Plant Pathol, 63(4): 937-945. |
| [6] | Fan J, Yang J, Wang Y Q, Li G B, Li Y, Huang F, Wang W M. 2016. Current understanding on Villosiclava virens, a unique flower- infecting fungus causing rice false smut disease. Mol Plant Pathol, 17(9): 1321-1330. |
| [7] | Fang A F, Gao H, Zhang N, Zheng X H, Qiu S S, Li Y J, Zhou S, Cui F H, Sun W X. 2019. A novel effector gene SCRE2 contributes to full virulence of Ustilaginoidea virens to rice. Front Microbiol, 10: 845. |
| [8] | Guo W W, Gao Y X, Yu Z M, Xiao Y H, Zhang Z G, Zhang H F. 2019. The adenylate cyclase UvAc1 and phosphodiesterase UvPdeH control the intracellular cAMP level, development, and pathogenicity of the rice false smut fungus Ustilaginoidea virens. Fungal Genet Biol, 129: 65-73. |
| [9] | Harata K, Nishiuchi T, Kubo Y. 2016. Colletotrichum orbiculare WHI2, a yeast stress-response regulator homolog, controls the biotrophic stage of hemibiotrophic infection through TOR signaling. Mol Plant Microbe Interact, 29(6): 468-483. |
| [10] | Kaida D, Yashiroda H, Toh-E A, Kikuchi Y. 2002. Yeast Whi2 and Psr1-phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells, 7(6): 543-552. |
| [11] | Leadsham J E, Miller K, Ayscough K R, Colombo S, Martegani E, Sudbery P, Gourlay C W. 2009. Whi2p links nutritional sensing to actin-dependent Ras-cAMP-PKA regulation and apoptosis in yeast. J Cell Sci, 122(5): 706-715. |
| [12] | Li M Y, Liu X Y, Liu Z X, Sun Y, Liu M X, Wang X L, Zhang H F, Zheng X B, Zhang Z G. 2016. Glycoside hydrolase MoGls2 controls asexual/sexual development, cell wall integrity and infectious growth in the rice blast fungus. PLoS One, 11(9): e0162243. |
| [13] | Lin X Y, Bian Y F, Mou R X, Cao Z Y, Cao Z Z, Zhu Z W, Chen M X. 2018. Isolation, identification, and characterization of Ustilaginoidea virens from rice false smut balls with high ustilotoxin production potential. J Basic Microbiol, 58(8): 670-678. |
| [14] | Lu S Q, Sun W B, Meng J J, Wang A L, Wang X H, Tian J, Fu X X, Dai J G, Liu Y, Lai D W, Zhou L G. 2015. Bioactive bis-naphtho- γ-pyrones from rice false smut pathogen Ustilaginoidea virens. J Agric Food Chem, 63(13): 3501-3508. |
| [15] | Lv B, Zheng L, Liu H, Tang J T, Hsiang T, Huang J B. 2016. Use of random T-DNA mutagenesis in identification of gene UvPRO1, a regulator of conidiation, stress response, and virulence in Ustilaginoidea virens. Front Microbiol, 7: 2086. |
| [16] | Maršíková J, Pavlíčková M, Wilkinson D, Váchová L, Hlaváček O, Hatáková L, Palková Z. 2020. The Whi2p-Psr1p/Psr2p complex regulates interference competition and expansion of cells with competitive advantage in yeast colonies. Proc Natl Acad Sci USA, 117(26): 15123-15131. |
| [17] | Mendl N, Occhipinti A, Müller M, Wild P, Dikic I, Reichert A S. 2011. Mitophagy in yeast is independent of mitochondrial fission and requires the stress response gene WHI2. J Cell Sci, 124(8): 1339-1350. |
| [18] | Meng S, Xiong M, Jagernath J S, Wang C C, Qiu J H, Shi H B, Kou Y J. 2020. UvAtg8-mediated autophagy regulates fungal growth, stress responses, conidiation, and pathogenesis in Ustilaginoidea virens. Rice, 13(1): 56. |
| [19] | Müller M, Reichert A S. 2011. Mitophagy, mitochondrial dynamics and the general stress response in yeast. Biochem Soc Trans, 39(5): 1514-1519. |
| [20] | Qiu J H, Meng S, Deng Y Z, Huang S W, Kou Y J. 2019. Ustilaginoidea virens: A fungus infects rice flower and threats world rice production. Rice Sci, 26(4): 199-206. |
| [21] | Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res, 42: 320-324. |
| [22] | Sadeh A, Movshovich N, Volokh M, Gheber L, Aharoni A. 2011. Fine-tuning of the Msn2/4-mediated yeast stress responses as revealed by systematic deletion of Msn2/4 partners. Mol Biol Cell, 22(17): 3127-3138. |
| [23] | Song W W, Dou X Y, Qi Z Q, Wang Q, Zhang X, Zhang H F, Guo M, Dong S M, Zhang Z G, Wang P, Zheng X B. 2010. R-SNARE homolog MoSec22 is required for conidiogenesis, cell wall integrity, and pathogenesis of Magnaporthe oryzae. PLoS One, 5(10): e13193. |
| [24] | Sun W B, Wang A L, Xu D, Wang W X, Meng J J, Dai J G, Liu Y, Lai D W, Zhou L G. 2017. New ustilaginoidins from rice false smut balls caused by Villosiclava virens and their phytotoxic and cytotoxic activities. J Agric Food Chem, 65(25): 5151-5160. |
| [25] | Sun W X, Fan J, Fang A F, Li Y J, Tariqjaveed M, Li D Y, Hu D W, Wang W M. 2020. Ustilaginoidea virens: Insights into an emerging rice pathogen. Annu Rev Phytopathol, 58(1): 363-385. |
| [26] | Tang J T, Bai J, Chen X Y, Zheng L, Liu H, Huang J B. 2020. Two protein kinases UvPmk1 and UvCdc2 with significant functions in conidiation, stress response and pathogenicity of rice false smut fungus Ustilaginoidea virens. Curr Genet, 66(2): 409-420. |
| [27] | Teng X C, Yau E, Sing C, Hardwick J M. 2018. Whi2 signals low leucine availability to halt yeast growth and cell death. FEMS Yeast Res, 18(8): foy095. |
| [28] | Timpano H, Tong L C H, Gautier V, Lalucque H, Silar P. 2016. The PaPsr1 and PaWhi2 genes are members of the regulatory network that connect stationary phase to mycelium differentiation and reproduction in Podospora anserina. Fungal Genet Biol, 94: 1-10. |
| [29] | Wang X H, Wang J, Lai D W, Wang W X, Dai J G, Zhou L G, Liu Y. 2017. Ustiloxin G, a new cyclopeptide mycotoxin from rice false smut balls. Toxins, 9(2): 54. |
| [30] | Wang Y F, Wang F, Xie S L, Liu Y, Qu J S, Huang J B, Yin W X, Luo C X. 2019. Development of rice conidiation media for Ustilaginoidea virens. PLoS One, 14(10): e0217667. |
| [31] | Xie S L, Wang Y F, Wei W, Li C Y, Liu Y, Qu J S, Meng Q H, Lin Y, Yin W X, Yang Y N, Luo C X. 2019. The Bax inhibitor UvBI-1, a negative regulator of mycelial growth and conidiation, mediates stress response and is critical for pathogenicity of the rice false smut fungus Ustilaginoidea virens. Curr Genet, 65(5): 1185-1197. |
| [32] | Xiong M, Meng S, Qiu J H, Shi H B, Shen X L, Kou Y J. 2020. Putative phosphatase UvPsr1 is required for mycelial growth, conidiation, stress response and pathogenicity in Ustilaginoidea virens. Rice Sci, 27(6): 529-536. |
| [33] | Yu J J, Yu M N, Song T Q, Cao H J, Pan X Y, Yong M L, Qi Z Q, Du Y, Zhang R S, Yin X L, Liu Y F. 2019. A homeobox transcription factor UvHOX2 regulates chlamydospore formation, conidiogenesis, and pathogenicity in Ustilaginoidea virens. Front Microbiol, 10: 1071. |
| [34] | Yu M N, Yu J J, Hu J K, Huang L, Wang Y H, Yin X L, Nie Y F, Meng X K, Wang W D, Liu Y F. 2015. Identification of pathogenicity-related genes in the rice pathogen Ustilaginoidea virens through random insertional mutagenesis. Fungal Genet Biol, 76: 10-19. |
| [35] | Zheng D W, Wang Y, Han Y, Xu J R, Wang C F. 2016. UvHOG1 is important for hyphal growth and stress responses in the rice false smut fungus Ustilaginoidea virens. Sci Rep, 6: 24824. |
| [36] | Zheng M T, Ding H, Huang L, Wang Y H, Yu M N, Zheng R, Yu J J, Liu Y F. 2017. Low-affinity iron transport protein Uvt3277 is important for pathogenesis in the rice false smut fungus Ustilaginoidea virens. Curr Genet, 63(1): 131-144. |
/
| 〈 |
|
〉 |