Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast

Jiang, Lihui; Zhang, Xiaoyan; Zhao, Yiting; Zhu, Haiyan; Fu, Qijing; Lu, Xinqi; Huang, Wuying; Yang, Xinyue; Zhou, Xuan; Wu, Lixia; Yang, Ao; He, Xie; Dong, Man; Peng, Ziai; Yang, Jing; Guo, Liwei; Wen, Jiancheng; Huang, Huichuan; Xie, Yong; Zhu, Shusheng; Li, Chengyun; He, Xiahong; Zhu, Youyong; Friml, Jiří; Du, Yunlong

Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast

Jiang L, Zhang X, Zhao Y, Zhu H, Fu Q, Lu X, Huang W, Yang X, Zhou X, Wu L, Yang A, He X, Dong M, Peng Z, Yang J, Guo L, Wen J, Huang H, Xie Y, Zhu S, Li C, He X, Zhu Y, Friml J, Du Y. 2024. Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast. Nature Communications. 15, 3437.

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DOI

10.1038/s41467-024-47746-y

Journal Article | Published | English

Scopus indexed

Author

Jiang, Lihui; Zhang, Xiaoyan; Zhao, Yiting; Zhu, Haiyan; Fu, Qijing; Lu, Xinqi; Huang, Wuying; Yang, Xinyue; Zhou, Xuan; Wu, Lixia; Yang, Ao; He, Xie
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Department

Friml Group

Abstract

Phytoalexin sakuranetin functions in resistance against rice blast. However, the mechanisms underlying the effects of sakuranetin remains elusive. Here, we report that rice lines expressing resistance (R) genes were found to contain high levels of sakuranetin, which correlates with attenuated endocytic trafficking of plasma membrane (PM) proteins. Exogenous and endogenous sakuranetin attenuates the endocytosis of various PM proteins and the fungal effector PWL2. Moreover, accumulation of the avirulence protein AvrCO39, resulting from uptake into rice cells by Magnaporthe oryzae, was reduced following treatment with sakuranetin. Pharmacological manipulation of clathrin-mediated endocytic (CME) suggests that this pathway is targeted by sakuranetin. Indeed, attenuation of CME by sakuranetin is sufficient to convey resistance against rice blast. Our data reveals a mechanism of rice against M. oryzae by increasing sakuranetin levels and repressing the CME of pathogen effectors, which is distinct from the action of many R genes that mainly function by modulating transcription.

Publishing Year

2024

Date Published

2024-04-23

Journal Title

Nature Communications

Acknowledgement

We thank Professor Jianqiang Wu (Kunming Institute of Botany, Chinese Academy of Sciences) for his generous support with the sakuranetin measurement. We thank International Rice Research Institute (IRRI) for provision of the rice NILs. We thank Professor Zhongkai Zhang (Yunnan Academy of Agricultural Sciences) for his generous support with subcellular structure observation of rice roots. We thank Professor Barbara Valent (Kansas State University) for her generously provision of the plasmid containing the PWL2 gene. We thank Professor Zuhua He (Chinese Academy of Sciences) for the gift of the transgenic rice line expressing the Pigm gene, OsNPR1-RNAi mutant line and ROD1-overexpression rice line. We thank Professor Yinong Yang (The Pennsylvania State University) for provision of the rice line NahG. We thank Professor Muyuan Zhu (Zhejiang University) for provision of the transgenic plants overexpressing miR393a. We thank Professor Zhengge Zhu (Hebei Normal University) for provision of the rice line overexpressing OsPIN3t-GFP. We thank Professor Yanhua Qi (Zhejiang University) for provision of the arf12 mutant line. Thanks also go to Professor Jean-Benoit Morel (Plant Health Institute of Montpellier) for provision of the fungus M. oryzae strain Guy11 (AvrCo39-mRFP). This work was supported by grants from the National Natural Science Foundation of China (Grant Nos. 32260085, 31460453, 31660501, 31860064, 31760500 and 31901870), the Major Special Program for Scientific Research, Education Department of Yunnan Province (Grant No. ZD2015005). The project was also sponsored by SRF for ROCS, SEM (Grant No. [2013] 1792), the Key Projects of Applied Basic Research Plan of Yunnan Province (Grant No. 2017FA018, 202301AS070082), the Major Science and Technology Project in Yunnan Province (202102AE090042, 202202AE090036 and 202102AE090017), the Young and Middle-Aged Academic and Technical Leaders Reserve Talent Program in Yunnan Province (202205AC160076), the China Postdoctoral Science Foundation (2019M653849XB) and the National Key Research and Development Program of China (2023YFE0107500).

Volume

Article Number

3437

ISSN

2041-1723

IST-REx-ID

17103

Cite this

Jiang L, Zhang X, Zhao Y, et al. Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast. Nature Communications. 2024;15. doi:10.1038/s41467-024-47746-y

Jiang, L., Zhang, X., Zhao, Y., Zhu, H., Fu, Q., Lu, X., … Du, Y. (2024). Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast. Nature Communications. Springer Nature. https://doi.org/10.1038/s41467-024-47746-y

Jiang, Lihui, Xiaoyan Zhang, Yiting Zhao, Haiyan Zhu, Qijing Fu, Xinqi Lu, Wuying Huang, et al. “Phytoalexin Sakuranetin Attenuates Endocytosis and Enhances Resistance to Rice Blast.” Nature Communications. Springer Nature, 2024. https://doi.org/10.1038/s41467-024-47746-y.

L. Jiang et al., “Phytoalexin sakuranetin attenuates endocytosis and enhances resistance to rice blast,” Nature Communications, vol. 15. Springer Nature, 2024.

Jiang, Lihui, et al. “Phytoalexin Sakuranetin Attenuates Endocytosis and Enhances Resistance to Rice Blast.” Nature Communications, vol. 15, 3437, Springer Nature, 2024, doi:10.1038/s41467-024-47746-y.

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