Protein disulfide isomerase MoPdi1 regulates fungal development, virulence, and endoplasmic reticulum homeostasis in Magnaporthe oryzae

doi:10.1016/j.jia.2024.03.054

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Protein disulfide isomerase MoPdi1 regulates fungal development, virulence, and endoplasmic reticulum homeostasis in Magnaporthe oryzae

Yu Wang^{1, 2*}, Xiaoru Kang^{1, 2}^*, Xinyue Cui^{1, 2}^*, Jinmei Hu^{1, 2}, Yuemin Pan^{1, 2}, Yizhen Deng³, Shulin Zhang^{1, 2}

1 Department of Plant Pathology, College of Plant Protection, Anhui Agricultural University, Hefei 230036, China

2 Anhui Province Key Laboratory of Crop Integrated Pest Management, Anhui Agricultural University, Hefei 230036, China

3 State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Integrative Microbiology Research Centre, South China Agricultural University, Guangzhou, Guangdong, China

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摘要由稻瘟病菌侵染水稻引起的稻瘟病严重威胁水稻安全生产。在稻瘟病菌侵染寄主的过程中，病原菌通过分泌效应蛋白以克服寄主免疫反应。在效应蛋白分泌至寄主细胞之前，效应蛋白需在内质网中合成、修饰以及成熟。由蛋白质二硫键异构酶Pdi1催化形成的二硫键在蛋白质折叠和成熟过程中发挥重要作用。然而，其在稻瘟病菌中的功能尚不清楚。鉴于此，本研究在稻瘟病菌中鉴定到一个内质网定位蛋白MoPdi1，生物信息学分析显示，其含有a, b, b’, a’和c结构域，并且在a和a’结构域中具有CGHC保守基序。为了明确MoPDI1在稻瘟病菌中的生物学功能，本研究采用同源重组策略对该基因进行敲除，获得敲除突变体∆Mopdi1。表型分析结果表明，MoPDI1参与调控稻瘟病菌产孢、细胞壁完整性、寄主活性氧清除和致病力。同时，本研究获得了CGHC保守基序的突变体，研究结果显示，该保守基序突变导致稻瘟病菌产孢和致病力显著下降。此外，我们发现， MoPdi1影响稻瘟病菌对内质网胁迫因子的敏感性，并且正向调控内质网自噬，表明MoPdi1参与维持稻瘟病菌内质网稳态。在此基础上，本研究通过蛋白互作技术证实了在稻瘟病菌中MoPdi1与MoHut1互作，并且MoPDI1缺失导致MoHut1不能够形成二聚体。我们也提供证据表明，当MoPDI1或MoHUT1缺失后，稻瘟病菌胞质效应子AVR-Pia的分泌异常。进一步通过基因缺失和表型分析显示， MoHUT1影响稻瘟病菌的营养生长、产孢和致病力。综上所述，本研究揭示了MoPdi1通过调控内质网稳态、底物二硫键形成以及胞质效应蛋白的分泌从而影响稻瘟病菌的发育和致病力，同时可为环境友好型杀菌剂的研发提供新的参考靶点。

Abstract Rice blast, caused by Magnaporthe oryzae, is a fungal disease that causes devastating damage to rice production worldwide. During infection, pathogens secrete effector proteins that modulate plant immunity. Disulfide bond formation catalyzed by protein disulfide isomerases (PDI) is essential for protein folding and maturation. However, the biological function of Pdi1 in M. oryzae has not yet been characterized. In this study, we identified the endoplasmic reticulum (ER)-located protein, MoPdi1, in M. oryzae. MoPdi1 regulates conidiation, cell wall stress, and pathogenicity of M. oryzae. Furthermore, the CGHC active sites in the a and a’ redox domain of MoPdi1 were essential for the biological function of MoPDI1. Further tests demonstrated that MoPdi1 was involved in the regulation of ER stress and positively regulated ER phagy. We also found that MoPdi1 interacted with MoHut1. Deletion of MoPDI1 led to the bereft of MoHut1 dimerization, which depends on the formation of disulfide bonds. In addition, MoPdi1 affected the normal secretion of the cytoplasmic effector AVR-Pia. We provided evidence that MoHut1 is important for the vegetative growth, conidiation, and pathogenicity in M. oryzae. Therefore, our findings could provide a suitable target point for designing antifungal agrochemicals against rice blast fungus.

Keywords: Magnaporthe oryzae protein disulfide isomerase MoPdi1 fungal development pathogenesis

Online: 16 April 2024

Fund: This study was supported by the National Natural Science Foundation of China (32202253), the Natural Science Foundation of Anhui Higher Education Institutions (KJ2020A0102) and the Talent Research Project of Anhui Agricultural University (rc342001). We are grateful to Prof. Jianping Lu of Zhejiang University, Prof. Xiaolin Chen of Huazhong Agricultural University, Prof. Haifeng Zhang and Dr. Xinyu Liu of Nanjing Agriculture University for providing pKO1B, pKD2-YFP^CTF, pKD5-YFP^NTF, pKN-RP27FlAG, MoLhs1-RFP, MoSlp1-GFP and AVR-Pia-GFP plasmids. We also would like to thank KetengEdit (https://www.ketengedit.com) for linguistic assistance during the preparation of this manuscript.

About author: Yu Wang, E-mail: wangyu2811@163.com, Xiaoru Kang, E-mail: 1737812015@qq.com, Xinyue Cui, E-mail: 1612376752@qq.com; #Correspondence Shulin Zhang, E-mail: zhangsl80h@ahau.edu.cn; Yizhen Deng, E-mail: dengyz@scau.edu.cn; Yuemin Pan, E-mail: panyuemin2008@163.com * indicates the authors who contributed equally to this study

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Yu Wang, Xiaoru Kang, Xinyue Cui, Jinmei Hu, Yuemin Pan, Yizhen Deng, Shulin Zhang. 2024. Protein disulfide isomerase MoPdi1 regulates fungal development, virulence, and endoplasmic reticulum homeostasis in Magnaporthe oryzae. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2024.03.054

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