Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores

Kosala Ranathunge, Lukasz Kotula, Ernst Steudle, Renee Lafitte

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74 Citations (Scopus)

Abstract

The relative contribution of the apoplastic and cell- to-cell paths to the overall hydraulic conductivity of the outer part of rice roots (Lp OPR) was estimated using a pressure perfusion technique for 30-d-old rice plants (lowland cultivar, IR64, and upland cultivar, Azucena). The technique was based on the perfusion of aerenchyma of root segments from two different zones (20-50 mm and 50-100 mm from the root apex) with aerated nutrient solution using precise pump rates. The outer part of roots (OPR) comprised an outermost rhizodermis, an exodermis, sclerenchyma fibre cells, and the innermost unmodified cortical cell layer. No root anatomical differences were observed for the two cultivars used. Development of apoplastic barriers such as Casparian bands and suberin lamellae in the exodermis were highly variable. On average, matured apoplastic barriers were observed at around 50-70 mm from the root apex. Lignification of the exodermis was completed earlier than that of sclerenchyma cells. Radial water flow across the OPR was impeded either by partially blocking off the porous apoplast with China ink particles (diameter 50 nm) or by closing water channels (aquaporins) in cell membranes with 50 μM HgCl2. The reduction of LpOPR was relatively larger in the presence of an apoplastic blockage with ink (≈30%) than in the presence of the water channel blocker (≈10%) suggesting a relatively larger apoplastic water flow. The reflection coefficient of the OPR (σsOPR) for mannitol significantly increased during both treatments. It was larger when pores of the apoplast were closed, but absolute values were low (overall range of σsOPR=0.1-0.4), which also suggested a large contribution of the non-selective, apoplastic path to overall water flow. The strongest evidence in favour of a predominantly apoplastic water transport came from the comparison between diffusional (PdOPR, measured with heavy water, HDO) and osmotic water permeability (P fOPR) or hydraulic conductivity (LpOPR). PfOPR was larger by a factor of 600-1400 compared with PdOPR. The development of OPR along roots resulted in a decrease of PdOPR by a factor of three (segments taken at 20-50 and 50-100 mm from root apex, respectively). Heat-killing of living cells resulted in an increase of P dOPR for both immature (20-50 mm) and mature (50-100 mm) root segments by a factor of two. Even though both pathways (apoplast and cell-to-cell) contributed to the overall water flow, the findings indicate predominantly apoplastic water flow across the OPR, even In the presence of apoplastic barriers. Low diffusional water permeabilities may suggest a low rate of oxygen diffusion across the OPR from aerenchyma to the outer anaerobic soil medium (low PO2OPR). To date, there are no data on P O2OPR. Provisional data of radial oxygen losses (ROL) across the OPR suggest that, unlike water, rice roots efficiently retain oxygen within the aerenchyma. This ability strongly increases as roots/OPR develop.

Original languageEnglish
Pages (from-to)433-447
Number of pages15
JournalJournal of Experimental Botany
Volume55
Issue number396
DOIs
Publication statusPublished - 1 Feb 2004
Externally publishedYes

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Aquaporins
aquaporins
Permeability
permeability
rice
Water
water
Ink
water flow
Oxygen
apoplast
Perfusion
Deuterium Oxide
Oryza
Mercuric Chloride
sclerenchyma
cells
Mannitol
oxygen
hydraulic conductivity

Cite this

@article{02a786fab7464e19b1eca21c9870af1b,
title = "Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores",
abstract = "The relative contribution of the apoplastic and cell- to-cell paths to the overall hydraulic conductivity of the outer part of rice roots (Lp OPR) was estimated using a pressure perfusion technique for 30-d-old rice plants (lowland cultivar, IR64, and upland cultivar, Azucena). The technique was based on the perfusion of aerenchyma of root segments from two different zones (20-50 mm and 50-100 mm from the root apex) with aerated nutrient solution using precise pump rates. The outer part of roots (OPR) comprised an outermost rhizodermis, an exodermis, sclerenchyma fibre cells, and the innermost unmodified cortical cell layer. No root anatomical differences were observed for the two cultivars used. Development of apoplastic barriers such as Casparian bands and suberin lamellae in the exodermis were highly variable. On average, matured apoplastic barriers were observed at around 50-70 mm from the root apex. Lignification of the exodermis was completed earlier than that of sclerenchyma cells. Radial water flow across the OPR was impeded either by partially blocking off the porous apoplast with China ink particles (diameter 50 nm) or by closing water channels (aquaporins) in cell membranes with 50 μM HgCl2. The reduction of LpOPR was relatively larger in the presence of an apoplastic blockage with ink (≈30{\%}) than in the presence of the water channel blocker (≈10{\%}) suggesting a relatively larger apoplastic water flow. The reflection coefficient of the OPR (σsOPR) for mannitol significantly increased during both treatments. It was larger when pores of the apoplast were closed, but absolute values were low (overall range of σsOPR=0.1-0.4), which also suggested a large contribution of the non-selective, apoplastic path to overall water flow. The strongest evidence in favour of a predominantly apoplastic water transport came from the comparison between diffusional (PdOPR, measured with heavy water, HDO) and osmotic water permeability (P fOPR) or hydraulic conductivity (LpOPR). PfOPR was larger by a factor of 600-1400 compared with PdOPR. The development of OPR along roots resulted in a decrease of PdOPR by a factor of three (segments taken at 20-50 and 50-100 mm from root apex, respectively). Heat-killing of living cells resulted in an increase of P dOPR for both immature (20-50 mm) and mature (50-100 mm) root segments by a factor of two. Even though both pathways (apoplast and cell-to-cell) contributed to the overall water flow, the findings indicate predominantly apoplastic water flow across the OPR, even In the presence of apoplastic barriers. Low diffusional water permeabilities may suggest a low rate of oxygen diffusion across the OPR from aerenchyma to the outer anaerobic soil medium (low PO2OPR). To date, there are no data on P O2OPR. Provisional data of radial oxygen losses (ROL) across the OPR suggest that, unlike water, rice roots efficiently retain oxygen within the aerenchyma. This ability strongly increases as roots/OPR develop.",
keywords = "Aerenchyma, Apoplastic transport, Bulk flow, Diffusional water permeabilty, Exodermis, Hydraulic conductivity, Rice root, Water channels",
author = "Kosala Ranathunge and Lukasz Kotula and Ernst Steudle and Renee Lafitte",
year = "2004",
month = "2",
day = "1",
doi = "10.1093/jxb/erh041",
language = "English",
volume = "55",
pages = "433--447",
journal = "Journal of Experimental Botany",
issn = "0022-0957",
publisher = "OXFORD UNIV PRESS UNITED KINGDOM",
number = "396",

}

TY - JOUR

T1 - Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores

AU - Ranathunge, Kosala

AU - Kotula, Lukasz

AU - Steudle, Ernst

AU - Lafitte, Renee

PY - 2004/2/1

Y1 - 2004/2/1

N2 - The relative contribution of the apoplastic and cell- to-cell paths to the overall hydraulic conductivity of the outer part of rice roots (Lp OPR) was estimated using a pressure perfusion technique for 30-d-old rice plants (lowland cultivar, IR64, and upland cultivar, Azucena). The technique was based on the perfusion of aerenchyma of root segments from two different zones (20-50 mm and 50-100 mm from the root apex) with aerated nutrient solution using precise pump rates. The outer part of roots (OPR) comprised an outermost rhizodermis, an exodermis, sclerenchyma fibre cells, and the innermost unmodified cortical cell layer. No root anatomical differences were observed for the two cultivars used. Development of apoplastic barriers such as Casparian bands and suberin lamellae in the exodermis were highly variable. On average, matured apoplastic barriers were observed at around 50-70 mm from the root apex. Lignification of the exodermis was completed earlier than that of sclerenchyma cells. Radial water flow across the OPR was impeded either by partially blocking off the porous apoplast with China ink particles (diameter 50 nm) or by closing water channels (aquaporins) in cell membranes with 50 μM HgCl2. The reduction of LpOPR was relatively larger in the presence of an apoplastic blockage with ink (≈30%) than in the presence of the water channel blocker (≈10%) suggesting a relatively larger apoplastic water flow. The reflection coefficient of the OPR (σsOPR) for mannitol significantly increased during both treatments. It was larger when pores of the apoplast were closed, but absolute values were low (overall range of σsOPR=0.1-0.4), which also suggested a large contribution of the non-selective, apoplastic path to overall water flow. The strongest evidence in favour of a predominantly apoplastic water transport came from the comparison between diffusional (PdOPR, measured with heavy water, HDO) and osmotic water permeability (P fOPR) or hydraulic conductivity (LpOPR). PfOPR was larger by a factor of 600-1400 compared with PdOPR. The development of OPR along roots resulted in a decrease of PdOPR by a factor of three (segments taken at 20-50 and 50-100 mm from root apex, respectively). Heat-killing of living cells resulted in an increase of P dOPR for both immature (20-50 mm) and mature (50-100 mm) root segments by a factor of two. Even though both pathways (apoplast and cell-to-cell) contributed to the overall water flow, the findings indicate predominantly apoplastic water flow across the OPR, even In the presence of apoplastic barriers. Low diffusional water permeabilities may suggest a low rate of oxygen diffusion across the OPR from aerenchyma to the outer anaerobic soil medium (low PO2OPR). To date, there are no data on P O2OPR. Provisional data of radial oxygen losses (ROL) across the OPR suggest that, unlike water, rice roots efficiently retain oxygen within the aerenchyma. This ability strongly increases as roots/OPR develop.

AB - The relative contribution of the apoplastic and cell- to-cell paths to the overall hydraulic conductivity of the outer part of rice roots (Lp OPR) was estimated using a pressure perfusion technique for 30-d-old rice plants (lowland cultivar, IR64, and upland cultivar, Azucena). The technique was based on the perfusion of aerenchyma of root segments from two different zones (20-50 mm and 50-100 mm from the root apex) with aerated nutrient solution using precise pump rates. The outer part of roots (OPR) comprised an outermost rhizodermis, an exodermis, sclerenchyma fibre cells, and the innermost unmodified cortical cell layer. No root anatomical differences were observed for the two cultivars used. Development of apoplastic barriers such as Casparian bands and suberin lamellae in the exodermis were highly variable. On average, matured apoplastic barriers were observed at around 50-70 mm from the root apex. Lignification of the exodermis was completed earlier than that of sclerenchyma cells. Radial water flow across the OPR was impeded either by partially blocking off the porous apoplast with China ink particles (diameter 50 nm) or by closing water channels (aquaporins) in cell membranes with 50 μM HgCl2. The reduction of LpOPR was relatively larger in the presence of an apoplastic blockage with ink (≈30%) than in the presence of the water channel blocker (≈10%) suggesting a relatively larger apoplastic water flow. The reflection coefficient of the OPR (σsOPR) for mannitol significantly increased during both treatments. It was larger when pores of the apoplast were closed, but absolute values were low (overall range of σsOPR=0.1-0.4), which also suggested a large contribution of the non-selective, apoplastic path to overall water flow. The strongest evidence in favour of a predominantly apoplastic water transport came from the comparison between diffusional (PdOPR, measured with heavy water, HDO) and osmotic water permeability (P fOPR) or hydraulic conductivity (LpOPR). PfOPR was larger by a factor of 600-1400 compared with PdOPR. The development of OPR along roots resulted in a decrease of PdOPR by a factor of three (segments taken at 20-50 and 50-100 mm from root apex, respectively). Heat-killing of living cells resulted in an increase of P dOPR for both immature (20-50 mm) and mature (50-100 mm) root segments by a factor of two. Even though both pathways (apoplast and cell-to-cell) contributed to the overall water flow, the findings indicate predominantly apoplastic water flow across the OPR, even In the presence of apoplastic barriers. Low diffusional water permeabilities may suggest a low rate of oxygen diffusion across the OPR from aerenchyma to the outer anaerobic soil medium (low PO2OPR). To date, there are no data on P O2OPR. Provisional data of radial oxygen losses (ROL) across the OPR suggest that, unlike water, rice roots efficiently retain oxygen within the aerenchyma. This ability strongly increases as roots/OPR develop.

KW - Aerenchyma

KW - Apoplastic transport

KW - Bulk flow

KW - Diffusional water permeabilty

KW - Exodermis

KW - Hydraulic conductivity

KW - Rice root

KW - Water channels

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U2 - 10.1093/jxb/erh041

DO - 10.1093/jxb/erh041

M3 - Article

VL - 55

SP - 433

EP - 447

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

SN - 0022-0957

IS - 396

ER -