Targeting and activation of BraATG8i by an RXLR effector DM459 contribute to downy mildew resistance in Brassica rapa

Abstract

Downy mildew, caused by the biotrophic oomycete Hyaloperonospora parasitica, is one of the most devastating diseases affecting global Brassica production. Despite its significant impact, the molecular and cellular mechanisms underlying both compatible and incompatible interactions of H. parasitica and Brassica rapa remain poorly understood. In this study, we identified an H. parasitica RXLR effector, DM459, which demonstrates the ability to induce autophagy by targeting BraATG8i, a key component of autophagosome formation, as confirmed by multiple in vivo and in vitro assays. BraATG8i is a positive regulator of defense against downy mildew, which was determined by the BraATG8i overexpression and RNA interference in B. rapa. Furthermore, the effector DM459 interacts with BraATG8i as well as BraATG4, BraATG3, and BraATG7-core proteins required for autophagosome assembly. This interaction-enhanced autophagy contributed to elevated disease resistance. Moreover, pathogen inoculation or DM459 presence stimulated salicylic acid (SA) biosynthesis, which in turn activated BraATG8i expression and further elevated autophagy. Collectively, our results demonstrated that the effector DM459 triggers autophagy by directly targeting BraATG proteins and simultaneously activates SA signaling, which consequently enhances plant resistance to downy mildew.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32102400, 32002045), grants from the Exploratory Research (TSXM202505) and the Scientist Training Program (JKZX202406) of Beijing Academy of Agriculture and Forestry Science, the earmarked fund for China Agriculture Research System (CARS-23-A03), and the Foundation for Reform and Development of BVRC (KYCX202502) of Beijing Vegetable Research Center.

Author contributions

N. Li, N. Liu, T.B.S. and S.C.Y. designed the experiments, analyzed the data, and wrote the manuscript. N. Li, Y.Y.C., P.R.L., G.Z.W., Y.X.H., Z.J.Z., X.Y.X., W.H.W., X.Y.Z., D.S.Z., Y.J.Y., T.B.S., and F.L.Z. performed the experiments. All authors read and approved the manuscript.

Data availability

All data required for evaluating the conclusions in the paper are available. All materials generated in this study are available from the corresponding author S.C.Y.

Conflicts of interest statement

The authors declare no conflicts of interest.

Supplementary material

Supplementary material is available at Horticulture Research online.

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