The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling

被引:380
作者
Bi, Guozhi [1 ]
Su, Min [2 ]
Li, Nan [2 ]
Liang, Yu [2 ]
Dang, Song [2 ]
Xu, Jiachao [2 ]
Hu, Meijuan [1 ]
Wang, Jizong [4 ]
Zou, Minxia [5 ,6 ]
Deng, Yanan [2 ]
Li, Qiyu [2 ]
Huang, Shijia [7 ]
Li, Jiejie [5 ,6 ]
Chai, Jijie [7 ,8 ,9 ]
He, Kangmin [2 ,3 ,10 ]
Chen, Yu-hang [2 ,3 ,10 ]
Zhou, Jian-Min [1 ,10 ,11 ]
机构
[1] Chinese Acad Sci, Inst Genet & Dev Biol, State Key Lab Plant Genom, Beijing 100101, Peoples R China
[2] Chinese Acad Sci, Inst Genet & Dev Biol, State Key Lab Mol Dev Biol, Beijing 100101, Peoples R China
[3] Univ Chinese Acad Sci, Beijing 100049, Peoples R China
[4] Peking Univ, Sch Adv Agr Sci, State Key Lab Prot & Plant Gene Res, Beijing 100871, Peoples R China
[5] Beijing Normal Univ, Coll Life Sci, Beijing Key Lab Gene Resource & Mol Dev, Beijing 100875, Peoples R China
[6] Beijing Normal Univ, Coll Life Sci, Key Lab Cell Proliferat & Regulat, Minist Educ, Beijing 100875, Peoples R China
[7] Tsinghua Univ, Beijing Adv Innovat Ctr Struct Biol, Tsinghua Peking Joint Ctr Life Sci, Ctr Plant Biol,Sch Life Sci, Beijing 100084, Peoples R China
[8] Max Planck Inst Plant Breeding Res, Cologne, Germany
[9] Univ Cologne, Inst Biochem, Zuelpicher Str 47, D-50674 Cologne, Germany
[10] Chinese Acad Sci, Innovat Acad Seed Design, Beijing 100101, Peoples R China
[11] Univ Chinese Acad Sci, CAS Ctr Excellence Biot Interact, Beijing 100049, Peoples R China
基金
中国国家自然科学基金;
关键词
SINGLE-MOLECULE ANALYSIS; DISEASE RESISTANCE GENE; PLASMA-MEMBRANE; OXIDATIVE BURST; ARABIDOPSIS; EFFECTOR; DYNAMICS; PROTEIN; PSEUDOKINASE; RECOGNITION;
D O I
10.1016/j.cell.2021.05.003
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
Nucleotide-binding, leucine-rich repeat receptors (NLRs) are major immune receptors in plants and animals. Upon activation, the Arabidopsis NLR protein ZAR1 forms a pentameric resistosome in vitro and triggers immune responses and cell death in plants. In this study, we employed single-molecule imaging to show that the activated ZAR1 protein can form pentameric complexes in the plasma membrane, The ZAR1 resistosome displayed ion channel activity in Xenopus oocytes in a manner dependent on a conserved acidic residue Glu11 situated in the channel pore. Pre-assembled ZAR1 resistosome was readily incorporated into planar lipid-bilayers and displayed calcium-permeable cation-selective channel activity. Furthermore, we show that activation of ZAR1 in the plant cell led to Glu11 -dependent Ca2+ influx, perturbation of subcellular structures, production of reactive oxygen species, and cell death. The results thus support that the ZAR1 resisto-some acts as a calcium-permeable cation channel to trigger immunity and cell death.
引用
收藏
页码:3528 / +
页数:26
相关论文
共 76 条
[1]   An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species [J].
Adachi, Hiroaki ;
Contreras, Mauricio P. ;
Harant, Adeline ;
Wu, Chih-hang ;
Derevnina, Lida ;
Sakai, Toshiyuki ;
Duggan, Cian ;
Moratto, Eleonora ;
Bozkurt, Tolga O. ;
Maqbool, Abbas ;
Win, Joe ;
Kamoun, Sophien .
ELIFE, 2019, 8
[2]   Advances in Analysis of Low Signal-to-Noise Images Link Dynamin and AP2 to the Functions of an Endocytic Checkpoint [J].
Aguet, Francois ;
Antonescu, Costin N. ;
Mettlen, Marcel ;
Schmid, Sandra L. ;
Danuser, Gaudenz .
DEVELOPMENTAL CELL, 2013, 26 (03) :279-291
[3]   Uncoiling CNLs: Structure/Function Approaches to Understanding CC Domain Function in Plant NLRs [J].
Bentham, Adam R. ;
Zdrzalek, Rafal ;
De la Concepcion, Juan Carlos ;
Banfield, Mark J. .
PLANT AND CELL PHYSIOLOGY, 2018, 59 (12) :2398-2408
[4]   The Plant "Resistosome": Structural Insights into Immune Signaling [J].
Burdett, Hayden ;
Bentham, Adam R. ;
Williams, Simon J. ;
Dodds, Peter N. ;
Anderson, Peter A. ;
Banfield, Mark J. ;
Kobe, Bostjan .
CELL HOST & MICROBE, 2019, 26 (02) :193-201
[5]   Single-molecule analysis of fluorescently labeled G-protein-coupled receptors reveals complexes with distinct dynamics and organization [J].
Calebiro, Davide ;
Rieken, Finn ;
Wagner, Julia ;
Sungkaworn, Titiwat ;
Zabel, Ulrike ;
Borzi, Alfio ;
Cocucci, Emanuele ;
Zuern, Alexander ;
Lohse, Martin J. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2013, 110 (02) :743-748
[6]   Pyroptosis is driven by non-selective gasdermin-D pore and its morphology is different from MLKL channel-mediated necroptosis [J].
Chen, Xin ;
He, Wan-ting ;
Hu, Lichen ;
Li, Jingxian ;
Fang, Yuan ;
Wang, Xin ;
Xu, Xiaozheng ;
Wang, Zhuo ;
Huang, Kai ;
Han, Jiahuai .
CELL RESEARCH, 2016, 26 (09) :1007-1020
[7]   Homologue structure of the SLAC1 anion channel for closing stomata in leaves [J].
Chen, Yu-hang ;
Hu, Lei ;
Punta, Marco ;
Bruni, Renato ;
Hillerich, Brandan ;
Kloss, Brian ;
Rost, Burkhard ;
Love, James ;
Siegelbaum, Steven A. ;
Hendrickson, Wayne A. .
NATURE, 2010, 467 (7319) :1074-U157
[8]   The First Five Seconds in the Life of a Clathrin-Coated Pit [J].
Cocucci, Emanuele ;
Aguet, Francois ;
Boulant, Steeve ;
Kirchhausen, Tom .
CELL, 2012, 150 (03) :495-507
[9]   The Inflammasome NLRs in Immunity, Inflammation, and Associated Diseases [J].
Davis, Beckley K. ;
Wen, Haitao ;
Ting, Jenny P. -Y. .
ANNUAL REVIEW OF IMMUNOLOGY, VOL 29, 2011, 29 :707-735
[10]   Calcium transport across plant membranes: mechanisms and functions [J].
Demidchik, Vadim ;
Shabala, Sergey ;
Isayenkov, Stanislav ;
Cuin, Tracey A. ;
Pottosin, Igor .
NEW PHYTOLOGIST, 2018, 220 (01) :49-69