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Article|28 May 2024|OPEN
Chloroplast protein StFC-II was manipulated by a Phytophthora effector to enhance host susceptibility
Meng Xu1,3,4 , Xinyuan Sun1,3,4 , Xinya Wu1,3,4 , Yetong Qi1,3,4 , Hongjun Li1,3,4 , Jiahui Nie1,3,4 , Zhu Yang1,3,4 , Zhendong Tian,1,2,3,4 ,
1National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, Huazhong Agricultural University (HZAU), Wuhan 430070, China
2Hubei Hongshan Laboratory (HZAU), Wuhan 430070, China
3Key Laboratory of Potato Biology and Biotechnology (HZAU), Ministry of Agriculture and Rural Affairs, Wuhan 430070, China
4Potato Engineering and Technology Research Center of Hubei Province (HZAU), Wuhan 430070, China
*Corresponding author. E-mail: tianzhd@mail.hzau.edu.cn

Horticulture Research 11,
Article number: uhae149 (2024)
doi: https://doi.org/10.1093/hr/uhae149
Views: 1224

Received: 16 Nov 2023
Accepted: 21 May 2024
Published online: 28 May 2024

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.