Chloroplast protein StFC-II was manipulated by a Phytophthora effector to enhance host susceptibility

Abstract

Oomycete secretes a range of RxLR effectors into host cells to manipulate plant immunity by targeting proteins from several organelles. In this study, we report that chloroplast protein StFC-II is hijacked by a pathogen effector to enhance susceptibility. Phytophthora infestans RxLR effector Pi22922 is activated during the early stages of P.infestans colonization. Stable overexpression of Pi22922 in plants suppresses flg22-triggered reactive oxygen species (ROS) burst and enhances leaf colonization by P. infestans. A potato ferrochelatase 2 (FC-II, a nuclear-encoded chloroplast-targeted protein), a key enzyme for heme biosynthesis in chloroplast, was identified as a target of Pi22922 in the cytoplasm. The pathogenicity of Pi22922 in plants is partially dependent on FC-II. Overexpression of StFC-II decreases resistance of potato and Nicotiana benthamiana against P. infestans, and silencing of NbFC-II in N. benthamiana reduces P. infestans colonization . Overexpression of StFC-II increases heme content and reduces chlorophyll content and photosynthetic efficiency in potato leaves. Moreover, ROS accumulation both in chloroplast and cytoplasm is attenuated and defense-related genes are down-regulated in StFC-II overexpression transgenic potato and N. benthamiana leaves. Pi22922 inhibits E3 ubiquitin ligase StCHIP-mediated StFC-II degradation in the cytoplasm and promotes its accumulation in chloroplasts. In summary, this study characterizes a new mechanism that an oomycete RxLR effector suppresses host defenses by promoting StFC-II accumulation in chloroplasts, thereby compromising the host immunity and promoting susceptibility.

Acknowledgements

The authors express their gratitude to the National Key R&D Program of China (2023YFF1000404) and the National Natural Science Foundation of China for providing financial support (grant Nos. 32372172, 32072121, 31761143007).

Author contributions

Z.T. and M.X: organizing and designing; M.X, X.S, X.W., Y.Q., H.L., J.N., and Z.Y.: conducting experiments and analysing data; M.X., Z.T., and X.S.: writing with input from all authors.

Data availability statement

The data underlying this article are available in the article and in its online supplementary data.

Conflict of interests

The authors declare no conflicts of interest.

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