EIN3-binding F-box protein SlEBF3 modulates resistance against Botrytis cinerea and carotenoid biosynthesis by degradation of BBX20 in tomato

Abstract

EIN3 binding F-box (EBF) proteins have been reported to play important roles in ethylene signaling pathway by mediating the ubiquitin-dependent degradation of EIN3-Like (EIL) proteins, but little is known about their roles in postharvest disease resistance. Here, we showed that SlEBF3 confers resistance against Botrytis cinerea by ubiquitin-mediated degradation of SlBBX20. Overexpression of SlEBF3 enhanced resistance to B. cinerea and increased the expression levels of genes related to PR (pathogenesis-related) and JA (jasmonic acid) in tomato, while knockdown of SlEBF3 does not affect tomato resistance to B. cinerea. Further study demonstrated that SlEBF3 interacts with SlBBX20 the interaction between SlEBF3 and SlBBX20 promotes SlBBX20 degradation via the 26S proteasome, which confers enhanced resistance to B. cinerea through the JA signaling pathway mediated by the SlBBX20-SlMYC2-SlMED25 module. Meanwhile, SlEBF3 extends fruit shelf life by remodeling cell wall composition and promoting cuticular accumulation. Additionally, SlEBF3 is involved in carotenoid metabolism regulation by interacting with SlBBX20, SlRIN, SlFUL1, and SlTAGL1, which is independent of the degradation of EIL proteins. Overall, this study revealed the molecular mechanism by which SlEBF3 responds to JA signaling to regulate B. cinerea resistance, enriched the roles of SlEBF3 in the regulatory network of carotenoids metabolism, and provided new insights into the extension of fruit shelf life.

Acknowledgements

This work was supported in part by the National Natural Science Foundation of China (nos 32302622, 32372780, 32172643, and 32172271), the Technology Innovation and Application Development Program of Chongqing (no. cstc2021jscx-cylhX0001), the Natural Science Foundation of Sichuan Province, China (nos 2023NSFSC1991 and 2024NSFSC1302), and the China Postdoctoral Science Foundation (2023 M732486).

Author contributions

M.W., M.L., and M.B. planned and designed the research. Z.G., H.D., X.H., Y.Y., C.Y., G.J., and T.M. performed experiments. Z.G. analyzed data. Z.G. and M.W. wrote the manuscript.

Data availability

The authors confirm that all the experimental data are available and accessible via the main text and/or the supplemental data.

Conflict of interest statement

The authors declare no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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