Multi-copper oxidases SKU5 and SKS1 coordinate cell wall formation using apoplastic redox-based reactions in roots

Chen，Chaofan1,2; Zhang，Yi1,2; Cai，Jianfa2; Qiu，Yuting2; Li，Lihong2; Gao，Chengxu3; Gao，Yiqun4; Ke，Meiyu1,2; Wu，Shengwei1,2; Wei，Chuan1; Chen，Jiaomei2; Xu，Tongda2; Friml，Jiří5; Wang，Junqi6; Li，Ruixi6; Chao，Daiyin4; Zhang，Baocai3; Chen，Xu2; Gao，Zhen2

2023-07-01

10.1093/plphys/kiad207

Plant Physiology   Impact Factor & Quartile

0032-0889

1532-2548

The primary cell wall is a fundamental plant constituent that is flexible but sufficiently rigid to support the plant cell shape. Although many studies have demonstrated that reactive oxygen species (ROS) serve as important signaling messengers to modify the cell wall structure and affect cellular growth, the regulatory mechanism underlying the spatial-temporal regulation of ROS activity for cell wall maintenance remains largely unclear. Here, we demonstrate the role of the Arabidopsis (Arabidopsis thaliana) multicopper oxidase-like protein skewed 5 (SKU5) and its homolog SKU5-similar 1 (SKS1) in root cell wall formation through modulating ROS homeostasis. Loss of SKU5 and SKS1 function resulted in aberrant division planes, protruding cell walls, ectopic deposition of iron, and reduced nicotinamide adeninedinucleotide phosphate (NADPH) oxidase-dependent ROS overproduction in the root epidermis-cortex and cortex-endodermis junctions. A decrease in ROS level or inhibition of NADPH oxidase activity rescued the cell wall defects of sku5 sks1 double mutants. SKU5 and SKS1 proteins were activated by iron treatment, and iron over-accumulated in the walls between the root epidermis and cortex cell layers of sku5 sks1. The glycosylphosphatidylinositol-anchored motif was crucial for membrane association and functionality of SKU5 and SKS1. Overall, our results identified SKU5 and SKS1 as regulators of ROS at the cell surface for regulation of cell wall structure and root cell growth.

SCI

English

Others

National Natural Science Foundation of China["31870170","31701168"] ; Distinguished Young Scholar Program of Fujian Agriculture and Forestry University[xjq201921] ; Scientific Research Foundation of Graduate School of Fujian Agriculture and Forestry University[324-1122yb082]

Plant Sciences

Plant Sciences

WOS:000971795800001

OXFORD UNIV PRESS INC

PLANT & ANIMAL SCIENCE

2-s2.0-85164209546

Scopus

1.College of Life Science,Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology,Fujian Agriculture and Forestry University,Fujian,Fuzhou,350002,China
2.FAFU-UCR Joint Center for Horticultural Biology and Metabolomics,Haixia Institute of Science and Technology,Fujian Agriculture and Forestry University,Fujian,Fuzhou,350002,China
3.State Key Laboratory of Plant Genomics,Institute of Genetics and Developmental Biology,The Innovative Academy of Seed Design,Chinese Academy of Sciences,Beijing,100101,China
4.National Key Laboratory of Plant Molecular Genetics,CAS Center for Excellence in Molecular Plant Sciences,Shanghai Institute of Plant Physiology and Ecology,Chinese Academy of Sciences,Shanghai,200032,China
5.Faculty of Cell Biology,Institute of Science and Technology Austria (IST Austria),Klosterneuburg,3400,Austria
6.Department of Biology,Institute of Plant and Food Science,Southern University of Science and Technology,Guangdong,Shenzhen,518055,China

Chen，Chaofan,Zhang，Yi,Cai，Jianfa,et al. Multi-copper oxidases SKU5 and SKS1 coordinate cell wall formation using apoplastic redox-based reactions in roots[J]. Plant Physiology,2023,192(3):2243-2260.

Chen，Chaofan.,Zhang，Yi.,Cai，Jianfa.,Qiu，Yuting.,Li，Lihong.,...&Gao，Zhen.(2023).Multi-copper oxidases SKU5 and SKS1 coordinate cell wall formation using apoplastic redox-based reactions in roots.Plant Physiology,192(3),2243-2260.

Chen，Chaofan,et al."Multi-copper oxidases SKU5 and SKS1 coordinate cell wall formation using apoplastic redox-based reactions in roots".Plant Physiology 192.3(2023):2243-2260.