Arabinosylation of cell wall extensin is required for the directional response to salinity in roots

Yutao Zou; Nora Gigli-Bisceglia; Eva van Zelm; Pinelopi Kokkinopoulou; Magdalena M Julkowska; Maarten Besten; Thu-Phuong Nguyen; Hongfei Li; Jasper Lamers; Thijs de Zeeuw; Joram A Dongus; Yuxiao Zeng; Yu Cheng; Iko T Koevoets; Bodil Jørgensen; Marcel Giesbers; Jelmer Vroom; Tijs Ketelaar; Bent Larsen Petersen; Timo Engelsdorf; Joris Sprakel; Yanxia Zhang; Christa Testerink

doi:10.1093/plcell/koae135

Arabinosylation of cell wall extensin is required for the directional response to salinity in roots

Yutao Zou
, Nora Gigli-Bisceglia
, Eva van Zelm
, Pinelopi Kokkinopoulou
, Magdalena M Julkowska
, Maarten Besten
, Thu-Phuong Nguyen
, Hongfei Li
, Jasper Lamers
, Thijs de Zeeuw
, Joram A Dongus
, Yuxiao Zeng
, Yu Cheng
, Iko T Koevoets
, Bodil Jørgensen
, Marcel Giesbers
, Jelmer Vroom
, Tijs Ketelaar
, Bent Larsen Petersen
, Timo Engelsdorf

Joris Sprakel, Yanxia Zhang^*, Christa Testerink^*

^*Corresponding author for this work

Wageningen University & Research
Boyce Thompson Institute
University of Copenhagen
Max Planck Institute of Molecular Plant Physiology

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Soil salinity is a major contributor to crop yield losses. To improve our understanding of root responses to salinity, we developed and exploited a real-time salt-induced tilting assay. This assay follows root growth upon both gravitropic and salt challenges, revealing that root bending upon tilting is modulated by Na+ ions, but not by osmotic stress. Next, we measured this salt-specific response in 345 natural Arabidopsis (Arabidopsis thaliana) accessions and discovered a genetic locus, encoding the cell wall-modifying enzyme EXTENSIN ARABINOSE DEFICIENT TRANSFERASE (ExAD) that is associated with root bending in the presence of NaCl (hereafter salt). Extensins are a class of structural cell wall glycoproteins known as hydroxyproline (Hyp)-rich glycoproteins, which are posttranslationally modified by O-glycosylation, mostly involving Hyp-arabinosylation. We show that salt-induced ExAD-dependent Hyp-arabinosylation influences root bending responses and cell wall thickness. Roots of exad1 mutant seedlings, which lack Hyp-arabinosylation of extensin, displayed increased thickness of root epidermal cell walls and greater cell wall porosity. They also showed altered gravitropic root bending in salt conditions and a reduced salt-avoidance response. Our results suggest that extensin modification via Hyp-arabinosylation is a unique salt-specific cellular process required for the directional response of roots exposed to salinity.

Original language	English
Pages (from-to)	3328-3343
Number of pages	16
Journal	The Plant Cell
Volume	36
Issue number	9
Early online date	1 May 2024
DOIs	https://doi.org/10.1093/plcell/koae135
Publication status	Published - Sept 2024

Bibliographical note

Funding

We thank Leonie Bentsink and Leo Willems of the Seed Lab, Laboratory of Plant Physiology, Wageningen University & Research for providing HapMap seeds for the GWAS screen. We also thank David E. Salt and Paulina Flis from Future Food Beacon of Excellence and School of Biosciences, University of Nottingham, United Kingdom, for ion measurements. Yut.Z. was sponsored by the China Scholarship Council (CSC), J.S. and M.B. are supported by ERC-CoG grant CATCH grant number: 101000981 and C.T. acknowledges support from the European Research Council (ERC) through the European Union's Horizon 2020 Research and Innovation program (ERC Consolidator Grant agreement 724321) and the Dutch Research Council (NWO) (Vici grant VI.C.192.033 and OCENW.KLEIN.421).

Funders	Funder number
China Scholarship Council (CSC)
ERC-CoG grant CATCH	101000981
European Research Council (ERC)	724321
Dutch Research Council (NWO)	VI.C.192.033, OCENW.KLEIN.421

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koae135Final published version, 29.1 MBLicence: CC BY

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Zou, Y., Gigli-Bisceglia, N., van Zelm, E., Kokkinopoulou, P., Julkowska, M. M., Besten, M., Nguyen, T.-P., Li, H., Lamers, J., de Zeeuw, T., Dongus, J. A., Zeng, Y., Cheng, Y., Koevoets, I. T., Jørgensen, B., Giesbers, M., Vroom, J., Ketelaar, T., Petersen, B. L., ... Testerink, C. (2024). Arabinosylation of cell wall extensin is required for the directional response to salinity in roots. The Plant Cell, 36(9), 3328-3343. https://doi.org/10.1093/plcell/koae135

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title = "Arabinosylation of cell wall extensin is required for the directional response to salinity in roots",

abstract = "Soil salinity is a major contributor to crop yield losses. To improve our understanding of root responses to salinity, we developed and exploited a real-time salt-induced tilting assay. This assay follows root growth upon both gravitropic and salt challenges, revealing that root bending upon tilting is modulated by Na+ ions, but not by osmotic stress. Next, we measured this salt-specific response in 345 natural Arabidopsis (Arabidopsis thaliana) accessions and discovered a genetic locus, encoding the cell wall-modifying enzyme EXTENSIN ARABINOSE DEFICIENT TRANSFERASE (ExAD) that is associated with root bending in the presence of NaCl (hereafter salt). Extensins are a class of structural cell wall glycoproteins known as hydroxyproline (Hyp)-rich glycoproteins, which are posttranslationally modified by O-glycosylation, mostly involving Hyp-arabinosylation. We show that salt-induced ExAD-dependent Hyp-arabinosylation influences root bending responses and cell wall thickness. Roots of exad1 mutant seedlings, which lack Hyp-arabinosylation of extensin, displayed increased thickness of root epidermal cell walls and greater cell wall porosity. They also showed altered gravitropic root bending in salt conditions and a reduced salt-avoidance response. Our results suggest that extensin modification via Hyp-arabinosylation is a unique salt-specific cellular process required for the directional response of roots exposed to salinity.",

author = "Yutao Zou and Nora Gigli-Bisceglia and \{van Zelm\}, Eva and Pinelopi Kokkinopoulou and Julkowska, \{Magdalena M\} and Maarten Besten and Thu-Phuong Nguyen and Hongfei Li and Jasper Lamers and \{de Zeeuw\}, Thijs and Dongus, \{Joram A\} and Yuxiao Zeng and Yu Cheng and Koevoets, \{Iko T\} and Bodil J{\o}rgensen and Marcel Giesbers and Jelmer Vroom and Tijs Ketelaar and Petersen, \{Bent Larsen\} and Timo Engelsdorf and Joris Sprakel and Yanxia Zhang and Christa Testerink",

note = "{\textcopyright} The Author(s) 2024. Published by Oxford University Press on behalf of American Society of Plant Biologists.",

year = "2024",

month = sep,

doi = "10.1093/plcell/koae135",

language = "English",

volume = "36",

pages = "3328--3343",

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Zou, Y, Gigli-Bisceglia, N , van Zelm, E, Kokkinopoulou, P, Julkowska, MM, Besten, M, Nguyen, T-P, Li, H, Lamers, J, de Zeeuw, T, Dongus, JA, Zeng, Y, Cheng, Y, Koevoets, IT, Jørgensen, B, Giesbers, M, Vroom, J, Ketelaar, T, Petersen, BL, Engelsdorf, T, Sprakel, J, Zhang, Y & Testerink, C 2024, 'Arabinosylation of cell wall extensin is required for the directional response to salinity in roots', The Plant Cell, vol. 36, no. 9, pp. 3328-3343. https://doi.org/10.1093/plcell/koae135

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T1 - Arabinosylation of cell wall extensin is required for the directional response to salinity in roots

AU - Zou, Yutao

AU - Gigli-Bisceglia, Nora

AU - van Zelm, Eva

AU - Kokkinopoulou, Pinelopi

AU - Julkowska, Magdalena M

AU - Besten, Maarten

AU - Nguyen, Thu-Phuong

AU - Li, Hongfei

AU - Lamers, Jasper

AU - de Zeeuw, Thijs

AU - Dongus, Joram A

AU - Zeng, Yuxiao

AU - Cheng, Yu

AU - Koevoets, Iko T

AU - Jørgensen, Bodil

AU - Giesbers, Marcel

AU - Vroom, Jelmer

AU - Ketelaar, Tijs

AU - Petersen, Bent Larsen

AU - Engelsdorf, Timo

AU - Sprakel, Joris

AU - Zhang, Yanxia

AU - Testerink, Christa

PY - 2024/9

Y1 - 2024/9

N2 - Soil salinity is a major contributor to crop yield losses. To improve our understanding of root responses to salinity, we developed and exploited a real-time salt-induced tilting assay. This assay follows root growth upon both gravitropic and salt challenges, revealing that root bending upon tilting is modulated by Na+ ions, but not by osmotic stress. Next, we measured this salt-specific response in 345 natural Arabidopsis (Arabidopsis thaliana) accessions and discovered a genetic locus, encoding the cell wall-modifying enzyme EXTENSIN ARABINOSE DEFICIENT TRANSFERASE (ExAD) that is associated with root bending in the presence of NaCl (hereafter salt). Extensins are a class of structural cell wall glycoproteins known as hydroxyproline (Hyp)-rich glycoproteins, which are posttranslationally modified by O-glycosylation, mostly involving Hyp-arabinosylation. We show that salt-induced ExAD-dependent Hyp-arabinosylation influences root bending responses and cell wall thickness. Roots of exad1 mutant seedlings, which lack Hyp-arabinosylation of extensin, displayed increased thickness of root epidermal cell walls and greater cell wall porosity. They also showed altered gravitropic root bending in salt conditions and a reduced salt-avoidance response. Our results suggest that extensin modification via Hyp-arabinosylation is a unique salt-specific cellular process required for the directional response of roots exposed to salinity.

AB - Soil salinity is a major contributor to crop yield losses. To improve our understanding of root responses to salinity, we developed and exploited a real-time salt-induced tilting assay. This assay follows root growth upon both gravitropic and salt challenges, revealing that root bending upon tilting is modulated by Na+ ions, but not by osmotic stress. Next, we measured this salt-specific response in 345 natural Arabidopsis (Arabidopsis thaliana) accessions and discovered a genetic locus, encoding the cell wall-modifying enzyme EXTENSIN ARABINOSE DEFICIENT TRANSFERASE (ExAD) that is associated with root bending in the presence of NaCl (hereafter salt). Extensins are a class of structural cell wall glycoproteins known as hydroxyproline (Hyp)-rich glycoproteins, which are posttranslationally modified by O-glycosylation, mostly involving Hyp-arabinosylation. We show that salt-induced ExAD-dependent Hyp-arabinosylation influences root bending responses and cell wall thickness. Roots of exad1 mutant seedlings, which lack Hyp-arabinosylation of extensin, displayed increased thickness of root epidermal cell walls and greater cell wall porosity. They also showed altered gravitropic root bending in salt conditions and a reduced salt-avoidance response. Our results suggest that extensin modification via Hyp-arabinosylation is a unique salt-specific cellular process required for the directional response of roots exposed to salinity.

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DO - 10.1093/plcell/koae135

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SN - 1040-4651

VL - 36

SP - 3328

EP - 3343

JO - The Plant Cell

JF - The Plant Cell

IS - 9

ER -

Arabinosylation of cell wall extensin is required for the directional response to salinity in roots

Abstract

Bibliographical note

Funding

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