The LRR receptor-like kinase ALR1 is a plant aluminum ion sensor

被引:25
作者
Ding, Zhong Jie [1 ]
Xu, Chen [1 ,2 ]
Yan, Jing Ying [3 ]
Wang, Yu Xuan [1 ]
Cui, Meng Qi [1 ]
Yuan, Jun Jie [1 ]
Wang, Ya Nan [1 ]
Li, Gui Xin [4 ]
Wu, Jian Xiang [4 ]
Wu, Yun Rong [1 ]
Xu, Ji Ming [1 ]
Li, Chun Xiao [1 ]
Shi, Yuan Zhi [5 ]
Mao, Chuan Zao [1 ]
Guo, Jiang Tao [6 ]
Zhou, Jian Min [7 ,8 ]
Benhamed, Moussa [9 ]
Harberd, Nicholas P. [1 ,10 ]
Zheng, Shao Jian [1 ,2 ,11 ]
机构
[1] Zhejiang Univ, Coll Life Sci, State Key Lab Plant Environm Resilience, Hangzhou, Zhejiang, Peoples R China
[2] South China Agr Univ, Coll Nat Resources & Environm, Guangdong Lab Lingnan Modern Agr, Guangzhou, Guangdong, Peoples R China
[3] Zhejiang Univ, Agr Expt Stn, Hangzhou, Zhejiang, Peoples R China
[4] Zhejiang Univ, Inst Biotechnol, State Key Lab Rice Biol, Hangzhou, Zhejiang, Peoples R China
[5] Chinese Acad Agr Sci, Tea Res Inst, Hangzhou, Zhejiang, Peoples R China
[6] Zhejiang Univ, Med Sch, Hangzhou, Zhejiang, Peoples R China
[7] Chinese Acad Sci, Ctr Genome Biol, Beijing, Peoples R China
[8] Chinese Acad Sci, Inst Genet & Dev Biol, State Key Lab Plant Genom, Beijing, Peoples R China
[9] Univ Paris Saclay, CNRS, INRAE, Univ Evry,Inst Plant Sci Paris Saclay IPS2, Orsay, France
[10] Univ Oxford, Dept Biol, Oxford, England
[11] Zhejiang A&F Univ, Inst Ecol Civilizat, Hangzhou, Zhejiang, Peoples R China
来源
CELL RESEARCH | 2024年 / 34卷 / 04期
基金
中国国家自然科学基金; 国家重点研发计划;
关键词
TRANSCRIPTION FACTOR; HYDROGEN-PEROXIDE; NADPH OXIDASE; ARABIDOPSIS; TOLERANCE; GENE; ROOT; PERCEPTION; ACTIVATION; RESISTANCE;
D O I
10.1038/s41422-023-00915-y
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Plant survival requires an ability to adapt to differing concentrations of nutrient and toxic soil ions, yet ion sensors and associated signaling pathways are mostly unknown. Aluminum (Al) ions are highly phytotoxic, and cause severe crop yield loss and forest decline on acidic soils which represent similar to 30% of land areas worldwide. Here we found an Arabidopsis mutant hypersensitive to Al. The gene encoding a leucine-rich-repeat receptor-like kinase, was named Al Resistance1 (ALR1). Al ions binding to ALR1 cytoplasmic domain recruits BAK1 co-receptor kinase and promotes ALR1-dependent phosphorylation of the NADPH oxidase RbohD, thereby enhancing reactive oxygen species (ROS) generation. ROS in turn oxidatively modify the RAE1 F-box protein to inhibit RAE1-dependent proteolysis of the central regulator STOP1, thus activating organic acid anion secretion to detoxify Al. These findings establish ALR1 as an Al ion receptor that confers resistance through an integrated Al-triggered signaling pathway, providing novel insights into ion-sensing mechanisms in living organisms, and enabling future molecular breeding of acid-soil-tolerant crops and trees, with huge potential for enhancing both global food security and forest restoration.
引用
收藏
页码:281 / 294
页数:14
相关论文
共 60 条
[1]   A semisynthetic epitope for kinase substrates [J].
Allen, Jasmina J. ;
Li, Manqing ;
Brinkworth, Craig S. ;
Paulson, Jennifer L. ;
Wang, Dan ;
Hubner, Anette ;
Chou, Wen-Hai ;
Davis, Roger J. ;
Burlingame, Alma L. ;
Messing, Robert O. ;
Katayama, Carol D. ;
Hedrick, Stephen M. ;
Shokat, Kevan M. .
NATURE METHODS, 2007, 4 (06) :511-516
[2]   Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis [J].
Amano, Yukari ;
Tsubouchi, Hiroko ;
Shinohara, Hidefumi ;
Ogawa, Mari ;
Matsubayashi, Yoshikatsu .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2007, 104 (46) :18333-18338
[3]   Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation [J].
Balzergue, Coline ;
Dartevelle, Thibault ;
Godon, Christian ;
Laugier, Edith ;
Meisrimler, Claudia ;
Teulon, Jean-Marie ;
Creff, Audrey ;
Bissler, Marie ;
Brouchoud, Corinne ;
Hagege, Agnes ;
Muller, Jens ;
Chiarenza, Serge ;
Javot, Helene ;
Becuwe-Linka, Noelle ;
David, Pascale ;
Peret, Benjamin ;
Delannoy, Etienne ;
Thibaud, Marie-Christine ;
Armengaud, Jean ;
Abel, Steffen ;
Pellequer, Jean-Luc ;
Nussaume, Laurent ;
Desnos, Thierry .
NATURE COMMUNICATIONS, 2017, 8
[4]   The cells and peripheral representation of sodium taste in mice [J].
Chandrashekar, Jayaram ;
Kuhn, Christina ;
Oka, Yuki ;
Yarmolinsky, David A. ;
Hummler, Edith ;
Ryba, Nicholas J. P. ;
Zuker, Charles S. .
NATURE, 2010, 464 (7286) :297-U182
[5]   Aluminum tolerance in transgenic plants by alteration of citrate synthesis [J].
delaFuente, JM ;
RamirezRodriguez, V ;
CabreraPonce, JL ;
HerreraEstrella, L .
SCIENCE, 1997, 276 (5318) :1566-1568
[6]   ALUMINUM TOLERANCE IN WHEAT (TRITICUM-AESTIVUM L) .2. ALUMINUM-STIMULATED EXCRETION OF MALIC-ACID FROM ROOT APICES [J].
DELHAIZE, E ;
RYAN, PR ;
RANDALL, PJ .
PLANT PHYSIOLOGY, 1993, 103 (03) :695-702
[7]   Engineering high-level aluminum tolerance in barley with the ALMT1 gene [J].
Delhaize, E ;
Ryan, PR ;
Hebb, DM ;
Yamamoto, Y ;
Sasaki, T ;
Matsumoto, H .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2004, 101 (42) :15249-15254
[8]   Opposite Roles of Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Transcriptional Regulation of Plant Immunity [J].
Ding, Yuli ;
Sun, Tongjun ;
Ao, Kevin ;
Peng, Yujun ;
Zhang, Yaxi ;
Li, Xin ;
Zhang, Yuelin .
CELL, 2018, 173 (06) :1454-+
[9]   WRKY46 functions as a transcriptional repressor of ALMT1, regulating aluminum-induced malate secretion in Arabidopsis [J].
Ding, Zhong Jie ;
Yan, Jing Ying ;
Xu, Xiao Yan ;
Li, Gui Xin ;
Zheng, Shao Jian .
PLANT JOURNAL, 2013, 76 (05) :825-835
[10]   A prion-like protein regulator of seed germination undergoes hydration-dependent phase separation [J].
Dorone, Yanniv ;
Boeynaems, Steven ;
Flores, Eduardo ;
Jin, Benjamin ;
Hateley, Shannon ;
Bossi, Flavia ;
Lazarus, Elena ;
Pennington, Janice G. ;
Michiels, Emiel ;
De Decker, Mathias ;
Vints, Katlijn ;
Baatsen, Pieter ;
Bassel, George W. ;
Otegui, Marisa S. ;
Holehouse, Alex S. ;
Exposito-Alonso, Moises ;
Sukenik, Shahar ;
Gitler, Aaron D. ;
Rhee, Seung Y. .
CELL, 2021, 184 (16) :4284-+