Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants

Peng Wang, Monica Calvo-Polanco, Guilhem Reyt, Marie Barberon, Chloe Champeyroux, Véronique Santoni, Christophe Maurel, Rochus B Franke, Karin Ljung, Ondrej Novak, Niko Geldner, Yann Boursiac, David E Salt (Corresponding Author)

Research output: Contribution to journalArticle

3 Citations (Scopus)
4 Downloads (Pure)

Abstract

The endodermis is a key cell layer in plant roots that contributes to the controlled uptake of water and mineral nutrients into plants. In order to provide such functionality the endodermal cell wall has specific chemical modifications consisting of lignin bands (Casparian strips) that encircle each cell, and deposition of a waxy-like substance (suberin) between the wall and the plasma membrane. These two extracellular deposits provide control of diffusion enabling the endodermis to direct the movement of water and solutes into and out of the vascular system in roots. Loss of integrity of the Casparian strip-based apoplastic barrier is sensed by the leakage of a small peptide from the stele into the cortex. Here, we report that such sensing of barrier integrity leads to the rebalancing of water and mineral nutrient uptake, compensating for breakage of Casparian strips. This rebalancing involves both a reduction in root hydraulic conductivity driven by deactivation of aquaporins, and downstream limitation of ion leakage through deposition of suberin. These responses in the root are also coupled to a reduction in water demand in the shoot mediated by ABA-dependent stomatal closure.

Original languageEnglish
Article number4227
JournalScientific Reports
Volume9
DOIs
Publication statusPublished - 12 Mar 2019

Fingerprint

Mineral Waters
Cell Wall
Water Movements
Aquaporins
Plant Roots
Water
Lignin
Blood Vessels
Cell Membrane
Ions
Food
Peptides
suberin

Keywords

  • AQUAPORINS
  • ARABIDOPSIS
  • CASPARIAN STRIP
  • ORGANIZATION
  • ROOTS
  • STRESS
  • TARGET

ASJC Scopus subject areas

  • General

Cite this

Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants. / Wang, Peng; Calvo-Polanco, Monica; Reyt, Guilhem; Barberon, Marie; Champeyroux, Chloe; Santoni, Véronique; Maurel, Christophe; Franke, Rochus B; Ljung, Karin; Novak, Ondrej; Geldner, Niko; Boursiac, Yann; Salt, David E (Corresponding Author).

In: Scientific Reports, Vol. 9, 4227, 12.03.2019.

Research output: Contribution to journalArticle

Wang, P, Calvo-Polanco, M, Reyt, G, Barberon, M, Champeyroux, C, Santoni, V, Maurel, C, Franke, RB, Ljung, K, Novak, O, Geldner, N, Boursiac, Y & Salt, DE 2019, 'Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants', Scientific Reports, vol. 9, 4227. https://doi.org/10.1038/s41598-019-40588-5
Wang, Peng ; Calvo-Polanco, Monica ; Reyt, Guilhem ; Barberon, Marie ; Champeyroux, Chloe ; Santoni, Véronique ; Maurel, Christophe ; Franke, Rochus B ; Ljung, Karin ; Novak, Ondrej ; Geldner, Niko ; Boursiac, Yann ; Salt, David E. / Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants. In: Scientific Reports. 2019 ; Vol. 9.
@article{7f8a4c831eb946528b4770a33a6fa9a5,
title = "Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants",
abstract = "The endodermis is a key cell layer in plant roots that contributes to the controlled uptake of water and mineral nutrients into plants. In order to provide such functionality the endodermal cell wall has specific chemical modifications consisting of lignin bands (Casparian strips) that encircle each cell, and deposition of a waxy-like substance (suberin) between the wall and the plasma membrane. These two extracellular deposits provide control of diffusion enabling the endodermis to direct the movement of water and solutes into and out of the vascular system in roots. Loss of integrity of the Casparian strip-based apoplastic barrier is sensed by the leakage of a small peptide from the stele into the cortex. Here, we report that such sensing of barrier integrity leads to the rebalancing of water and mineral nutrient uptake, compensating for breakage of Casparian strips. This rebalancing involves both a reduction in root hydraulic conductivity driven by deactivation of aquaporins, and downstream limitation of ion leakage through deposition of suberin. These responses in the root are also coupled to a reduction in water demand in the shoot mediated by ABA-dependent stomatal closure.",
keywords = "AQUAPORINS, ARABIDOPSIS, CASPARIAN STRIP, ORGANIZATION, ROOTS, STRESS, TARGET",
author = "Peng Wang and Monica Calvo-Polanco and Guilhem Reyt and Marie Barberon and Chloe Champeyroux and V{\'e}ronique Santoni and Christophe Maurel and Franke, {Rochus B} and Karin Ljung and Ondrej Novak and Niko Geldner and Yann Boursiac and Salt, {David E}",
note = "We acknowledge support from the ERA-NET Coordinating Action in Plant Sciences program project ERACAPS13.089_RootBarriers, with support from Biotechnology and Biological Sciences Research Council (grant no. BB/N023927/1 to D.E.S.), the German Research Foundation (DFG; grant no. FR 1721/2-1 to R.B.F. and the AgreenSkills+ fellowship programme to MC-P which has received funding from the EU’s Seventh Framework Programme under grant agreement N° FP7-609398 (AgreenSkills+ contract). This work was also funded by the Ministry of Education, Youth and Sports of the Czech Republic (National Program for Sustainability I, grant no. LO1204), the Swedish Governmental Agency for Innovation Systems (Vinnova) and the Swedish Research Council (VR). We thank Kevin Mackenzie (University of Aberdeen–Microscopy Histology Facility) and Carine Alcon (BPMP-PHIV microscopy platform) for assistance using the confocal microscope and stereo microscope for observing the root samples, and the Swedish Metabolomics Centre (http://www.swedishmetabolomicscentre.se/) for access to instrumentation.",
year = "2019",
month = "3",
day = "12",
doi = "10.1038/s41598-019-40588-5",
language = "English",
volume = "9",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",

}

TY - JOUR

T1 - Surveillance of cell wall diffusion barrier integrity modulates water and solute transport in plants

AU - Wang, Peng

AU - Calvo-Polanco, Monica

AU - Reyt, Guilhem

AU - Barberon, Marie

AU - Champeyroux, Chloe

AU - Santoni, Véronique

AU - Maurel, Christophe

AU - Franke, Rochus B

AU - Ljung, Karin

AU - Novak, Ondrej

AU - Geldner, Niko

AU - Boursiac, Yann

AU - Salt, David E

N1 - We acknowledge support from the ERA-NET Coordinating Action in Plant Sciences program project ERACAPS13.089_RootBarriers, with support from Biotechnology and Biological Sciences Research Council (grant no. BB/N023927/1 to D.E.S.), the German Research Foundation (DFG; grant no. FR 1721/2-1 to R.B.F. and the AgreenSkills+ fellowship programme to MC-P which has received funding from the EU’s Seventh Framework Programme under grant agreement N° FP7-609398 (AgreenSkills+ contract). This work was also funded by the Ministry of Education, Youth and Sports of the Czech Republic (National Program for Sustainability I, grant no. LO1204), the Swedish Governmental Agency for Innovation Systems (Vinnova) and the Swedish Research Council (VR). We thank Kevin Mackenzie (University of Aberdeen–Microscopy Histology Facility) and Carine Alcon (BPMP-PHIV microscopy platform) for assistance using the confocal microscope and stereo microscope for observing the root samples, and the Swedish Metabolomics Centre (http://www.swedishmetabolomicscentre.se/) for access to instrumentation.

PY - 2019/3/12

Y1 - 2019/3/12

N2 - The endodermis is a key cell layer in plant roots that contributes to the controlled uptake of water and mineral nutrients into plants. In order to provide such functionality the endodermal cell wall has specific chemical modifications consisting of lignin bands (Casparian strips) that encircle each cell, and deposition of a waxy-like substance (suberin) between the wall and the plasma membrane. These two extracellular deposits provide control of diffusion enabling the endodermis to direct the movement of water and solutes into and out of the vascular system in roots. Loss of integrity of the Casparian strip-based apoplastic barrier is sensed by the leakage of a small peptide from the stele into the cortex. Here, we report that such sensing of barrier integrity leads to the rebalancing of water and mineral nutrient uptake, compensating for breakage of Casparian strips. This rebalancing involves both a reduction in root hydraulic conductivity driven by deactivation of aquaporins, and downstream limitation of ion leakage through deposition of suberin. These responses in the root are also coupled to a reduction in water demand in the shoot mediated by ABA-dependent stomatal closure.

AB - The endodermis is a key cell layer in plant roots that contributes to the controlled uptake of water and mineral nutrients into plants. In order to provide such functionality the endodermal cell wall has specific chemical modifications consisting of lignin bands (Casparian strips) that encircle each cell, and deposition of a waxy-like substance (suberin) between the wall and the plasma membrane. These two extracellular deposits provide control of diffusion enabling the endodermis to direct the movement of water and solutes into and out of the vascular system in roots. Loss of integrity of the Casparian strip-based apoplastic barrier is sensed by the leakage of a small peptide from the stele into the cortex. Here, we report that such sensing of barrier integrity leads to the rebalancing of water and mineral nutrient uptake, compensating for breakage of Casparian strips. This rebalancing involves both a reduction in root hydraulic conductivity driven by deactivation of aquaporins, and downstream limitation of ion leakage through deposition of suberin. These responses in the root are also coupled to a reduction in water demand in the shoot mediated by ABA-dependent stomatal closure.

KW - AQUAPORINS

KW - ARABIDOPSIS

KW - CASPARIAN STRIP

KW - ORGANIZATION

KW - ROOTS

KW - STRESS

KW - TARGET

UR - http://www.scopus.com/inward/record.url?scp=85062834292&partnerID=8YFLogxK

UR - http://www.mendeley.com/research/surveillance-cell-wall-diffusion-barrier-integrity-modulates-water-solute-transport-plants

U2 - 10.1038/s41598-019-40588-5

DO - 10.1038/s41598-019-40588-5

M3 - Article

VL - 9

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

M1 - 4227

ER -