The VAMP-associated protein VAP27-1 plays a crucial role in plant resistance to ER stress by modulating ER-PM contact architecture in Arabidopsis

Yi Man; Yue Zhang; Linghui Chen; Junhui Zhou; Yufen Bu; Xi Zhang; Xiaojuan Li; Yun Li; Yanping Jing; Jinxing Lin

doi:10.1016/j.xplc.2024.100929

The VAMP-associated protein VAP27-1 plays a crucial role in plant resistance to ER stress by modulating ER-PM contact architecture in Arabidopsis

Plant Commun. 2024 Apr 27:100929. doi: 10.1016/j.xplc.2024.100929. Online ahead of print.

Authors

Yi Man¹, Yue Zhang¹, Linghui Chen¹, Junhui Zhou¹, Yufen Bu¹, Xi Zhang¹, Xiaojuan Li¹, Yun Li¹, Yanping Jing², Jinxing Lin²

Affiliations

¹ National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China; Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, China.
² National Engineering Research Center of Tree Breeding and Ecological Restoration, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, 100083, China; Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing Forestry University, Beijing, 100083, China. Electronic address: ypjing@bjfu.edu.cn.

PMID: 38678366
DOI: 10.1016/j.xplc.2024.100929

Abstract

The endoplasmic reticulum (ER) and the plasma membrane (PM) form ER-PM contact sites (EPCSs) that allow the ER and PM to exchange material and information. Stress-induced disruption of protein folding triggers ER stress and the cell initiates the unfolded protein response (UPR) to resist the stress. However, whether EPCSs in plants play a role in ER stress remain unclear. VESICLE-ASSOCIATED MEMBRANE PROTEIN (VAMP)-ASSOCIATED PROTEIN 27-1 (VAP27-1) functions in EPCS tethering and is encoded by a family of ten genes (VAP27-1-10) in Arabidopsis thaliana. Here, we used CRISPR/Cas9-mediated genome editing to obtain a homozygous vap27-1 vap27-3 vap27-4 (vap27-1/3/4) triple mutant lacking three of the key VAP27 family members in Arabidopsis. The vap27-1/3/4 mutant exhibited defects in ER-PM connectivity and EPCS architecture, and excessive UPR signaling. We further showed that relocation of VAP27-1 to the PM mediates specific VAP27-1-related EPCS remodeling and expansion under ER stress. Moreover, the spatiotemporal dynamics of VAP27-1 at the PM increase ER-PM connectivity and enhance Arabidopsis resistance to ER stress. In addition, we uncovered an important role for intracellular calcium homeostasis in the regulation of UPR signaling. Taken together, our results broaden the understanding of the molecular and cellular mechanisms of ER stress and UPR signaling in plants, providing additional clues for improving plant broad-spectrum resistance to different stresses.

Keywords: Arabidopsis; ER stress; ER-PM contact sites; VAP27-1; unfolded protein response.