The VAMP-associated Protein VAP27-1 Plays a Crucial Role in Plant Resistance to ER Stress by Modulating ER-PM Contact Architecture in Arabidopsis

Overview

Journal Plant Commun

Specialty Biology

Date 2024 Apr 28

PMID 38678366

Authors

Yi Man

Yue Zhang

Linghui Chen

Junhui Zhou

Yufen Bu

Xi Zhang

Xiaojuan Li

Yun Li

Yanping Jing

Jinxing Lin

Affiliations

Soon will be listed here.

Abstract

The endoplasmic reticulum (ER) and the plasma membrane (PM) form ER-PM contact sites (EPCSs) that allow the ER and PM to exchange materials 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 play a role in ER stress in plants remains unclear. VESICLE-ASSOCIATED MEMBRANE PROTEIN (VAMP)-ASSOCIATED PROTEIN 27-1 (VAP27-1) functions in EPCS tethering and is encoded by a family of 10 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 exhibits defects in ER-PM connectivity and EPCS architecture, as well as 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 revealed an important role for intracellular calcium homeostasis in the regulation of UPR signaling. Taken together, these results broaden our 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.

References

Lewis J, Lazarowitz S . Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc Natl Acad Sci U S A. 2010; 107(6):2491-6. PMC: 2823903. DOI: 10.1073/pnas.0909080107. View

Williams B, Kabbage M, Britt R, Dickman M . AtBAG7, an Arabidopsis Bcl-2-associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc Natl Acad Sci U S A. 2010; 107(13):6088-93. PMC: 2851922. DOI: 10.1073/pnas.0912670107. View

Griffing L, Gao H, Sparkes I . ER network dynamics are differentially controlled by myosins XI-K, XI-C, XI-E, XI-I, XI-1, and XI-2. Front Plant Sci. 2014; 5:218. PMC: 4033215. DOI: 10.3389/fpls.2014.00218. View

Levy A, Zheng J, Lazarowitz S . Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr Biol. 2015; 25(15):2018-25. PMC: 4526382. DOI: 10.1016/j.cub.2015.06.015. View

Stefan C, Manford A, Emr S . ER-PM connections: sites of information transfer and inter-organelle communication. Curr Opin Cell Biol. 2013; 25(4):434-42. PMC: 4074705. DOI: 10.1016/j.ceb.2013.02.020. View

Stefan C, Manford A, Baird D, Yamada-Hanff J, Mao Y, Emr S . Osh proteins regulate phosphoinositide metabolism at ER-plasma membrane contact sites. Cell. 2011; 144(3):389-401. DOI: 10.1016/j.cell.2010.12.034. View

van Vliet A, Giordano F, Gerlo S, Segura I, Van Eygen S, Molenberghs G . The ER Stress Sensor PERK Coordinates ER-Plasma Membrane Contact Site Formation through Interaction with Filamin-A and F-Actin Remodeling. Mol Cell. 2017; 65(5):885-899.e6. DOI: 10.1016/j.molcel.2017.01.020. View

Kamauchi S, Nakatani H, Nakano C, Urade R . Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J. 2005; 272(13):3461-76. DOI: 10.1111/j.1742-4658.2005.04770.x. View

Wang X, Li X, Deng X, Luu D, Maurel C, Lin J . Single-molecule fluorescence imaging to quantify membrane protein dynamics and oligomerization in living plant cells. Nat Protoc. 2015; 10(12):2054-63. DOI: 10.1038/nprot.2015.132. View

10.

Stefano G, Brandizzi F . Advances in Plant ER Architecture and Dynamics. Plant Physiol. 2017; 176(1):178-186. PMC: 5761816. DOI: 10.1104/pp.17.01261. View

11.

Liu J, Howell S . bZIP28 and NF-Y transcription factors are activated by ER stress and assemble into a transcriptional complex to regulate stress response genes in Arabidopsis. Plant Cell. 2010; 22(3):782-96. PMC: 2861475. DOI: 10.1105/tpc.109.072173. View

12.

Dong Q, Wallrad L, Almutairi B, Kudla J . Ca signaling in plant responses to abiotic stresses. J Integr Plant Biol. 2022; 64(2):287-300. DOI: 10.1111/jipb.13228. View

13.

Ma L, Ye J, Yang Y, Lin H, Yue L, Luo J . The SOS2-SCaBP8 Complex Generates and Fine-Tunes an AtANN4-Dependent Calcium Signature under Salt Stress. Dev Cell. 2019; 48(5):697-709.e5. DOI: 10.1016/j.devcel.2019.02.010. View

14.

Cui Y, Li X, Yu M, Li R, Fan L, Zhu Y . Sterols regulate endocytic pathways during flg22-induced defense responses in . Development. 2018; 145(19). DOI: 10.1242/dev.165688. View

15.

Alpy F, Rousseau A, Schwab Y, Legueux F, Stoll I, Wendling C . STARD3 or STARD3NL and VAP form a novel molecular tether between late endosomes and the ER. J Cell Sci. 2013; 126(Pt 23):5500-12. DOI: 10.1242/jcs.139295. View

16.

Su W, Liu Y, Xia Y, Hong Z, Li J . Conserved endoplasmic reticulum-associated degradation system to eliminate mutated receptor-like kinases in Arabidopsis. Proc Natl Acad Sci U S A. 2010; 108(2):870-5. PMC: 3021050. DOI: 10.1073/pnas.1013251108. View

17.

Zhu J . Abiotic Stress Signaling and Responses in Plants. Cell. 2016; 167(2):313-324. PMC: 5104190. DOI: 10.1016/j.cell.2016.08.029. View

18.

Lev S, Ben Halevy D, Peretti D, Dahan N . The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol. 2008; 18(6):282-90. DOI: 10.1016/j.tcb.2008.03.006. View

19.

Martiniere A, Lavagi I, Nageswaran G, Rolfe D, Maneta-Peyret L, Luu D . Cell wall constrains lateral diffusion of plant plasma-membrane proteins. Proc Natl Acad Sci U S A. 2012; 109(31):12805-10. PMC: 3411962. DOI: 10.1073/pnas.1202040109. View

20.

Schott A, Ravaud S, Keller S, Radzimanowski J, Viotti C, Hillmer S . Arabidopsis stromal-derived Factor2 (SDF2) is a crucial target of the unfolded protein response in the endoplasmic reticulum. J Biol Chem. 2010; 285(23):18113-21. PMC: 2878572. DOI: 10.1074/jbc.M110.117176. View