Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Chen C

PROVIDER: S-EPMC10315306 | biostudies-literature | 2023 Jul

REPOSITORIES: biostudies-literature

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

Chen Chaofan C Zhang Yi Y Cai Jianfa J Qiu Yuting Y Li Lihong L Gao Chengxu C Gao Yiqun Y Ke Meiyu M Wu Shengwei S Wei Chuan C Chen Jiaomei J Xu Tongda T Friml Jiří J Wang Junqi J Li Ruixi R Chao Daiyin D Zhang Baocai B Chen Xu X Gao Zhen Z

Plant physiology 20230701 3

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 (Arabidop ...[more]

PMID: 37010107

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Project description:Understanding plant adaptation mechanisms to prolonged water immersion provides options for genetic modification of existing crops to create cultivars more tolerant of periodic flooding. An important advancement in understanding flooding adaptation would be to elucidate mechanisms, such as aerenchyma air-space formation induced by hypoxic conditions, consistent with prolonged immersion. Lysigenous aerenchyma formation occurs through programmed cell death (PCD), which may entail the chemical modification of polysaccharides in root tissue cell walls. We investigated if a relationship exists between modification of pectic polysaccharides through de-methyl esterification (DME) and the formation of root aerenchyma in select Fabaceae species. To test this hypothesis, we first characterized the progression of aerenchyma formation within the vascular stele of three different legumes-Pisum sativum, Cicer arietinum, and Phaseolus coccineus-through traditional light microscopy histological staining and scanning electron microscopy. We assessed alterations in stele morphology, cavity dimensions, and cell wall chemistry. Then we conducted an immunolabeling protocol to detect specific degrees of DME among species during a 48-hour flooding time series. Additionally, we performed an enzymatic pretreatment to remove select cell wall polymers prior to immunolabeling for DME pectins. We were able to determine that all species possessed similar aerenchyma formation mechanisms that begin with degradation of root vascular stele metaxylem cells. Immunolabeling results demonstrated DME occurs prior to aerenchyma formation and prepares vascular tissues for the beginning of cavity formation in flooded roots. Furthermore, enzymatic pretreatment demonstrated that removal of cellulose and select hemicellulosic carbohydrates unmasks additional antigen binding sites for DME pectin antibodies. These results suggest that additional carbohydrate modification may be required to permit DME and subsequent enzyme activity to form aerenchyma. By providing a greater understanding of cell wall pectin remodeling among legume species, we encourage further investigation into the mechanism of carbohydrate modifications during aerenchyma formation and possible avenues for flood-tolerance improvement of legume crops.

Dataset Information

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

Publications

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

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