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Title: Xyloglucan Endotransglucosylase-Hydrolase30 negatively affects salt tolerance in Arabidopsis

Abstract

Plants have evolved various strategies to sense and respond to saline environments that severely reduce plant growth and limit agricultural productivity. Alteration to the cell wall is one strategy that helps plants adapt to salt stress. However, we do not fully understand the physiological significance of how cell wall components respond to salt stress. Here, we show that expression of XTH30, encoding a xyloglucan endotransglucosylase/hydrolase, is strongly up-regulated in response to salt stress in Arabidopsis thaliana. Loss-of-function in XTH30 leads to increased salt tolerance and overexpression of XTH30 results in salt hypersensitivity. XTH30 is located in the plasma membrane and highly expressed in the root, flower, stem, and etiolated hypocotyl. The NaCl-induced increase in XLFG (xyloglucan-derived (XyG) oligosaccharide) of the wild type is partly blocked in xth30 mutants. Loss-of-function in XTH30 slows down the decrease of crystalline cellulose content and the depolymerization of microtubules caused by salt stress. Moreover, less Na+ accumulation in shoot and H2O2 content are found in xth30 mutants in response to salt stress. Taken together, these results indicate that XTH30 modulates XyG side chains with altered abundance of XLFG, the cellulose synthesis and cortical microtubule stability, and then negatively affects salt tolerance.

Authors:
 [1];  [1];  [1];  [1];  [1];  [2];  [3];  [2];  [2];  [2];  [1];  [4];  [5];  [4]
  1. Nanjing Agricultural Univ., Nanjing, Jiangsu (China). College of Life Sciences
  2. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  3. Chinese Academy of Sciences (CAS), Guangzhou (China)
  4. Nanjing Agricultural Univ., Nanjing, Jiangsu (China). College of Life Sciences, and State Key Lab. of Crop Genetics and Germplasm Enhancement
  5. Nanjing Agricultural Univ., Nanjing, Jiangsu (China). State Key Lab. of Crop Genetics and Germplasm Enhancement, and Key Lab. of Biology and Germplasm Enhancement of Horticultural Crops in East China, Ministry of Agriculture
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1542421
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Journal of Experimental Botany
Additional Journal Information:
Journal Volume: 70; Journal Issue: 19; Journal ID: ISSN 0022-0957
Publisher:
Oxford University Press
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Arabidopsis; cellulose; microtubule; salt stress; XLFG; XTH30; xyloglucan

Citation Formats

Yan, Jingwei, Huang, Yun, He, Huan, Han, Tong, Di, Pengcheng, Sechet, Julien, Fang, Lin, Liang, Yan, Scheller, Henrik Vibe, Mortimer, Jenny C., Ni, Lan, Jiang, Mingyi, Hou, Xilin, and Zhang, Aying. Xyloglucan Endotransglucosylase-Hydrolase30 negatively affects salt tolerance in Arabidopsis. United States: N. p., 2019. Web. doi:10.1093/jxb/erz311.
Yan, Jingwei, Huang, Yun, He, Huan, Han, Tong, Di, Pengcheng, Sechet, Julien, Fang, Lin, Liang, Yan, Scheller, Henrik Vibe, Mortimer, Jenny C., Ni, Lan, Jiang, Mingyi, Hou, Xilin, & Zhang, Aying. Xyloglucan Endotransglucosylase-Hydrolase30 negatively affects salt tolerance in Arabidopsis. United States. https://doi.org/10.1093/jxb/erz311
Yan, Jingwei, Huang, Yun, He, Huan, Han, Tong, Di, Pengcheng, Sechet, Julien, Fang, Lin, Liang, Yan, Scheller, Henrik Vibe, Mortimer, Jenny C., Ni, Lan, Jiang, Mingyi, Hou, Xilin, and Zhang, Aying. Sat . "Xyloglucan Endotransglucosylase-Hydrolase30 negatively affects salt tolerance in Arabidopsis". United States. https://doi.org/10.1093/jxb/erz311. https://www.osti.gov/servlets/purl/1542421.
@article{osti_1542421,
title = {Xyloglucan Endotransglucosylase-Hydrolase30 negatively affects salt tolerance in Arabidopsis},
author = {Yan, Jingwei and Huang, Yun and He, Huan and Han, Tong and Di, Pengcheng and Sechet, Julien and Fang, Lin and Liang, Yan and Scheller, Henrik Vibe and Mortimer, Jenny C. and Ni, Lan and Jiang, Mingyi and Hou, Xilin and Zhang, Aying},
abstractNote = {Plants have evolved various strategies to sense and respond to saline environments that severely reduce plant growth and limit agricultural productivity. Alteration to the cell wall is one strategy that helps plants adapt to salt stress. However, we do not fully understand the physiological significance of how cell wall components respond to salt stress. Here, we show that expression of XTH30, encoding a xyloglucan endotransglucosylase/hydrolase, is strongly up-regulated in response to salt stress in Arabidopsis thaliana. Loss-of-function in XTH30 leads to increased salt tolerance and overexpression of XTH30 results in salt hypersensitivity. XTH30 is located in the plasma membrane and highly expressed in the root, flower, stem, and etiolated hypocotyl. The NaCl-induced increase in XLFG (xyloglucan-derived (XyG) oligosaccharide) of the wild type is partly blocked in xth30 mutants. Loss-of-function in XTH30 slows down the decrease of crystalline cellulose content and the depolymerization of microtubules caused by salt stress. Moreover, less Na+ accumulation in shoot and H2O2 content are found in xth30 mutants in response to salt stress. Taken together, these results indicate that XTH30 modulates XyG side chains with altered abundance of XLFG, the cellulose synthesis and cortical microtubule stability, and then negatively affects salt tolerance.},
doi = {10.1093/jxb/erz311},
journal = {Journal of Experimental Botany},
number = 19,
volume = 70,
place = {United States},
year = {Sat Jun 29 00:00:00 EDT 2019},
month = {Sat Jun 29 00:00:00 EDT 2019}
}

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Populus euphratica XTH overexpression enhances salinity tolerance by the development of leaf succulence in transgenic tobacco plants
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Galactose-Depleted Xyloglucan Is Dysfunctional and Leads to Dwarfism in Arabidopsis
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The Rice High-Affinity Potassium Transporter1;1 Is Involved in Salt Tolerance and Regulated by an MYB-Type Transcription Factor
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Xyloglucan Metabolism Differentially Impacts the Cell Wall Characteristics of the Endosperm and Embryo during Arabidopsis Seed Germination
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Xyloglucan Deficiency Disrupts Microtubule Stability and Cellulose Biosynthesis in Arabidopsis, Altering Cell Growth and Morphogenesis
journal, November 2015

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  • Plant Physiology, Vol. 170, Issue 1
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Ethylene Signaling Modulates Cortical Microtubule Reassembly in Response to Salt Stress
journal, February 2018

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  • Plant Physiology, Vol. 176, Issue 3
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KATAMARI1/MURUS3 Is a Novel Golgi Membrane Protein That Is Required for Endomembrane Organization in Arabidopsis
journal, April 2005


Salt Stress–Induced Disassembly of Arabidopsis Cortical Microtubule Arrays Involves 26S Proteasome–Dependent Degradation of SPIRAL1
journal, September 2011

  • Wang, Songhu; Kurepa, Jasmina; Hashimoto, Takashi
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O -Acetylation of Arabidopsis Hemicellulose Xyloglucan Requires AXY4 or AXY4L, Proteins with a TBL and DUF231 Domain
journal, November 2011

  • Gille, Sascha; de Souza, Amancio; Xiong, Guangyan
  • The Plant Cell, Vol. 23, Issue 11
  • DOI: 10.1105/tpc.111.091728

Phosphatidic Acid Regulates Microtubule Organization by Interacting with MAP65-1 in Response to Salt Stress in Arabidopsis
journal, November 2012


Loss of Inositol Phosphorylceramide Sphingolipid Mannosylation Induces Plant Immune Responses and Reduces Cellulose Content in Arabidopsis
journal, November 2016

  • Fang, Lin; Ishikawa, Toshiki; Rennie, Emilie A.
  • The Plant Cell, Vol. 28, Issue 12
  • DOI: 10.1105/tpc.16.00186

Molecular modeling of family GH16 glycoside hydrolases: Potential roles for xyloglucan transglucosylases/hydrolases in cell wall modification in the poaceae
journal, December 2004

  • Strohmeier, Marco; Hrmova, Maria; Fischer, Markus
  • Protein Science, Vol. 13, Issue 12
  • DOI: 10.1110/ps.04828404

Hydrogen peroxide produced by NADPH oxidases increases proline accumulation during salt or mannitol stress in Arabidopsis thaliana
journal, July 2015

  • Ben Rejeb, Kilani; Lefebvre-De Vos, Delphine; Le Disquet, Isabel
  • New Phytologist, Vol. 208, Issue 4
  • DOI: 10.1111/nph.13550

Biosynthesis of the Plant Cell Wall Matrix Polysaccharide Xyloglucan
journal, April 2016


Works referencing / citing this record:

Maintenance of Cell Wall Integrity under High Salinity
journal, March 2021

  • Liu, Jianwei; Zhang, Wei; Long, Shujie
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