Red light induces salicylic acid accumulation by activating CaHY5 to enhance pepper resistance against Phytophthora capsici

Abstract

Pepper (Capsicum annuum L.) is frequently challenged by various pathogens, among which Phytophthora capsici is the most devastating to pepper production. Red light signal acts as a positive induction of plant resistance against multiple pathogens. However, little is known about how the red light signal affects pepper resistance to P. capsici infection (PCI). Here, we report that red light regulates salicylic acid (SA) accumulation by activating elongated hypocotyl5 (CaHY5), a basic leucine zipper (bZIP) transcription factor, thereby decreasing pepper susceptibility to PCI. Exogenous SA treatment reduced pepper susceptibility to PCI, while silencing of CaPHYB (a red light photoreceptor) increased its susceptibility. PCI significantly induced CaHY5 expression, and silencing of CaHY5 reduced SA accumulation, accompanied by decreases in the expression levels of phenylalanine ammonia-lyase 3 (CaPAL3), CaPAL7, pathogenesis-related 1 (CaPR1), and CaPR1L, which finally resulted in higher susceptibility of pepper to PCI. Moreover, CaHY5 was found to activate the expression of CaPAL3 and CaPAL7, which are essential for SA biosynthesis, by directly binding to their promoters. Further analysis revealed that exogenous SA treatment could restore the resistance of CaHY5-silenced pepper plants to PCI. Collectively, this study reveals a critical mechanism through which red light induces SA accumulation by regulating CaHY5-mediated CaPAL3 and CaPAL7 expression, leading to enhanced resistance to PCI. Moreover, red light-induced CaHY5 regulates pepper resistance to PCI, which may have implications for PCI control in protected vegetable production.

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (32002030), Major Discipline Academic and Technical Leaders Training Program of Jiangxi Province, China-Young Talents Project (20204BCJL23044), the China Postdoctoral Science Foundation (2020 M682732), the Yan’an University Doctoral Research Initiation Project (YAU202313800), China Agriculture Research System of MOF and MARA (CARS-24-B-01), and the earmarked fund for Jiangxi Agriculture Research System (JXARS-06).

Author contributions

F.D. and Y.Y. conceived the project. F.D. and Y.Y. designed the experiments. Y.Y., Y.G., J.L., Y.L., Y.Z., T.Y., and F.F.D. performed most of the experiments. J.L. performed EMSA analysis. F.D., Y.W., F.F.D., Y.Z., and Y.Y. analysed and discussed the data. F.D., Y.Z., and Y.Y. wrote the manuscript with comments from all authors. All the authors revised the manuscript.

Data availability

All relevant data supporting our findings are available in the manuscript file, supplementary data, and publicly available RNA sequencing data (number: SRP106410 and SRP119199) in the National Center for Biotechnology Information (NCBI) Sequence Read Archive database (https://www.ncbi.nlm.nih.gov/sra).

Conflict of interest

The authors declare no competing interests.

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