The Xyloglucan Endotransglucosylase/Hydrolase Gene XTH22/TCH4 Regulates Plant Growth by Disrupting the Cell Wall Homeostasis in Arabidopsis under Boron Deficiency.

Cheng Zhang,Sheliang Wang,Wenjun Zhang,Lan Liu,Junbao Pu,Zhexuan Jiang,Mingliang He,Fangsen Xu

doi:10.3390/ijms23031250

Cheng Zhang, Sheliang Wang + Show 6 more

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https://doi.org/10.3390/ijms23031250

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Abstract

TCH4 is a xyloglucan endotransglucosylase/hydrolase (XTH) family member. Extensive studies have shown that XTHs are very important in cell wall homeostasis for plant growth and development. Boron (B), as an essential micronutrient for plants, plays an essential role in the cross-linking of cell wall pectin. However, the effect of B on cell wall organization is unclear. This study aimed to explore the mechanism of plant adaption to B stress by investigating the role of TCH4 in cell wall homeostasis. We conducted both plate and hydroponic cultures of wild-type Col-0 and overexpression and gene knockout lines of XTH22/TCH4 to analyze the phenotype, components, and characteristics of the cell wall using immunofluorescence, atomic force microscopy (AFM), and transmission electron microscopy (TEM). B deficiency induces the expression of TCH4. The overexpression lines of TCH4 presented more sensitivity to B deficiency than the wild-type Col-0, while the knockout lines of TCH4 were more resistant to low B stress. Up-regulation of TCH4 influenced the ratio of chelator-soluble pectin to alkali-soluble pectin and decreased the degree of methylesterification of pectin under B-deficient conditions. Moreover, we found that B deficiency disturbed the arrangement of cellulose, enlarged the gap between cellulose microfibrils, and decreased the mechanical strength of the cell wall, leading to the formation of a thickened and deformed triangular region of the cell wall. These symptoms were more profound in the TCH4 overexpression lines. Consistently, compared with Col-0, the O2− and MDA contents in the TCH4 overexpression lines increased under B-deficient conditions. This study identified the B-deficiency-induced TCH4 gene, which regulates cell wall homeostasis to influence plant growth under B-deficient conditions.

Highlights

IntroductionBoron (B) is an essential micronutrient for plant growth
The results suggest that the distinct phenotype of TCH4 overexpression (TCH4-OX) lines under B deficiency might be attributed to its function in cell wall modification
We found that B deficiency increased the pectin methylesterase (PME) enzyme activities in both the roots and shoots, and PME enzyme activities in the TCH4-OX plants were higher than those in the wild-type Col-0 plants (Figure 7a)

Summary

Introduction

Boron (B) is an essential micronutrient for plant growth. B deficiency causes some physiological changes, such as increased ROS and anthocyanin accumulation [1]. B deficiency leads to many morphological defects, such as inhibition of leaf expansion, root elongation, and a reduction in fertility and crop yield [2,3,4]. B deficiency is a severe agricultural problem worldwide [5]. Many studies have indicated that the apparent function of B is its participation in the formation of the primary cell wall via cross-linking two monomeric rhamnogalacturonan II (RG-II) of the pectin to form dimeric RG-II [6,7]

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