Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis

W. Armstrong, D. Cousins, J. Armstrong, David Turner, P.M. Beckett

    Research output: Contribution to journalArticle

    230 Citations (Scopus)

    Abstract

    Adventitious roots of intact Phragmites plantlets were secured horizontally 2-3 mm below the surface of an oxygen-depleted fluid agar across which oxygen-free nitrogen was gently streamed to create a constant oxygen sink; the leafy shoot was fully exposed to air. Radial oxygen profiles through rhizosphere and root at different distances from the apex were obtained polarographically using Clark-type bevelled microelectrodes servo-driven in steps of 10 mu m (root) or 10-50 mu m (rhizosphere). The pattern of radial oxygen loss (ROL) typical of wetland plants, viz. high at the apex and declining sharply sub-apically, was related to synergism between ROL, and oxygen consumption and increasing impedance to diffusion within the epidermal/hypodermal cylinder rather than to a surface resistance. The smallest oxygen deficit (2 kPa) to develop across the 80 mu m thick epidermal/hypodermal cylinder was within the apical 10 mm and was consistent with tissue oxygen diffusivities similar to water. At 100 mm from the apex, consumption and impedance had increased the deficit to about 15 kPa and reduced ROL almost to zero. The developing impedance within the epidermal/hypodermal cylinder was least in cell layers immediately adjoining the cortex and increased most in the hypodermal cell layer abutting the epidermis. The sub-apical decline in ROL appeared to coincide with the appearance of aerenchyma in the cortex but thin walled 'passage areas' (windows) in the hypodermal/epidermal cylinder persisted locally and remained leaky to oxygen to some degree. It is through these windows that lateral roots emerge and the cortex in line with the windows remains non-aerenchymatous. The radial and longitudinal oxygen profiles were consistent with modelling predictions. The shapes of the stelar oxygen profiles were consistent with a higher oxygen demand in the outer region (viz. pericycle, phloem, protoxylem and early metaxylem cylinder) than in the inner core (late metaxylem cylinder and medulla), but the deficits were relatively small (less than or equal to 3 kPa) and consistent with minimal wall thickening in the endodermis and narrowness of stele. The possible relevance of the results to entry of methane and other products from the rhizosphere into root and to the mechanism of aerenchyma formation are discussed. (C) 2000 Annals of Botany Company.
    Original languageEnglish
    Pages (from-to)687-703
    JournalAnnals of Botany
    Volume86
    DOIs
    Publication statusPublished - 2000

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    wetland plants
    Phragmites australis
    gas exchange
    rhizosphere
    permeability
    oxygen
    impedance
    cortex
    Phragmites
    endodermis
    stele
    adventitious roots
    synergism
    epidermis (plant)
    diffusivity
    phloem
    oxygen consumption
    methane
    plantlets

    Cite this

    @article{85758495065941dd9be0d71f562bbc47,
    title = "Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis",
    abstract = "Adventitious roots of intact Phragmites plantlets were secured horizontally 2-3 mm below the surface of an oxygen-depleted fluid agar across which oxygen-free nitrogen was gently streamed to create a constant oxygen sink; the leafy shoot was fully exposed to air. Radial oxygen profiles through rhizosphere and root at different distances from the apex were obtained polarographically using Clark-type bevelled microelectrodes servo-driven in steps of 10 mu m (root) or 10-50 mu m (rhizosphere). The pattern of radial oxygen loss (ROL) typical of wetland plants, viz. high at the apex and declining sharply sub-apically, was related to synergism between ROL, and oxygen consumption and increasing impedance to diffusion within the epidermal/hypodermal cylinder rather than to a surface resistance. The smallest oxygen deficit (2 kPa) to develop across the 80 mu m thick epidermal/hypodermal cylinder was within the apical 10 mm and was consistent with tissue oxygen diffusivities similar to water. At 100 mm from the apex, consumption and impedance had increased the deficit to about 15 kPa and reduced ROL almost to zero. The developing impedance within the epidermal/hypodermal cylinder was least in cell layers immediately adjoining the cortex and increased most in the hypodermal cell layer abutting the epidermis. The sub-apical decline in ROL appeared to coincide with the appearance of aerenchyma in the cortex but thin walled 'passage areas' (windows) in the hypodermal/epidermal cylinder persisted locally and remained leaky to oxygen to some degree. It is through these windows that lateral roots emerge and the cortex in line with the windows remains non-aerenchymatous. The radial and longitudinal oxygen profiles were consistent with modelling predictions. The shapes of the stelar oxygen profiles were consistent with a higher oxygen demand in the outer region (viz. pericycle, phloem, protoxylem and early metaxylem cylinder) than in the inner core (late metaxylem cylinder and medulla), but the deficits were relatively small (less than or equal to 3 kPa) and consistent with minimal wall thickening in the endodermis and narrowness of stele. The possible relevance of the results to entry of methane and other products from the rhizosphere into root and to the mechanism of aerenchyma formation are discussed. (C) 2000 Annals of Botany Company.",
    author = "W. Armstrong and D. Cousins and J. Armstrong and David Turner and P.M. Beckett",
    year = "2000",
    doi = "10.1006/anbo.2000.1236",
    language = "English",
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    pages = "687--703",
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    Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis. / Armstrong, W.; Cousins, D.; Armstrong, J.; Turner, David; Beckett, P.M.

    In: Annals of Botany, Vol. 86, 2000, p. 687-703.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere: a microelectrode and modelling study with Phragmites australis

    AU - Armstrong, W.

    AU - Cousins, D.

    AU - Armstrong, J.

    AU - Turner, David

    AU - Beckett, P.M.

    PY - 2000

    Y1 - 2000

    N2 - Adventitious roots of intact Phragmites plantlets were secured horizontally 2-3 mm below the surface of an oxygen-depleted fluid agar across which oxygen-free nitrogen was gently streamed to create a constant oxygen sink; the leafy shoot was fully exposed to air. Radial oxygen profiles through rhizosphere and root at different distances from the apex were obtained polarographically using Clark-type bevelled microelectrodes servo-driven in steps of 10 mu m (root) or 10-50 mu m (rhizosphere). The pattern of radial oxygen loss (ROL) typical of wetland plants, viz. high at the apex and declining sharply sub-apically, was related to synergism between ROL, and oxygen consumption and increasing impedance to diffusion within the epidermal/hypodermal cylinder rather than to a surface resistance. The smallest oxygen deficit (2 kPa) to develop across the 80 mu m thick epidermal/hypodermal cylinder was within the apical 10 mm and was consistent with tissue oxygen diffusivities similar to water. At 100 mm from the apex, consumption and impedance had increased the deficit to about 15 kPa and reduced ROL almost to zero. The developing impedance within the epidermal/hypodermal cylinder was least in cell layers immediately adjoining the cortex and increased most in the hypodermal cell layer abutting the epidermis. The sub-apical decline in ROL appeared to coincide with the appearance of aerenchyma in the cortex but thin walled 'passage areas' (windows) in the hypodermal/epidermal cylinder persisted locally and remained leaky to oxygen to some degree. It is through these windows that lateral roots emerge and the cortex in line with the windows remains non-aerenchymatous. The radial and longitudinal oxygen profiles were consistent with modelling predictions. The shapes of the stelar oxygen profiles were consistent with a higher oxygen demand in the outer region (viz. pericycle, phloem, protoxylem and early metaxylem cylinder) than in the inner core (late metaxylem cylinder and medulla), but the deficits were relatively small (less than or equal to 3 kPa) and consistent with minimal wall thickening in the endodermis and narrowness of stele. The possible relevance of the results to entry of methane and other products from the rhizosphere into root and to the mechanism of aerenchyma formation are discussed. (C) 2000 Annals of Botany Company.

    AB - Adventitious roots of intact Phragmites plantlets were secured horizontally 2-3 mm below the surface of an oxygen-depleted fluid agar across which oxygen-free nitrogen was gently streamed to create a constant oxygen sink; the leafy shoot was fully exposed to air. Radial oxygen profiles through rhizosphere and root at different distances from the apex were obtained polarographically using Clark-type bevelled microelectrodes servo-driven in steps of 10 mu m (root) or 10-50 mu m (rhizosphere). The pattern of radial oxygen loss (ROL) typical of wetland plants, viz. high at the apex and declining sharply sub-apically, was related to synergism between ROL, and oxygen consumption and increasing impedance to diffusion within the epidermal/hypodermal cylinder rather than to a surface resistance. The smallest oxygen deficit (2 kPa) to develop across the 80 mu m thick epidermal/hypodermal cylinder was within the apical 10 mm and was consistent with tissue oxygen diffusivities similar to water. At 100 mm from the apex, consumption and impedance had increased the deficit to about 15 kPa and reduced ROL almost to zero. The developing impedance within the epidermal/hypodermal cylinder was least in cell layers immediately adjoining the cortex and increased most in the hypodermal cell layer abutting the epidermis. The sub-apical decline in ROL appeared to coincide with the appearance of aerenchyma in the cortex but thin walled 'passage areas' (windows) in the hypodermal/epidermal cylinder persisted locally and remained leaky to oxygen to some degree. It is through these windows that lateral roots emerge and the cortex in line with the windows remains non-aerenchymatous. The radial and longitudinal oxygen profiles were consistent with modelling predictions. The shapes of the stelar oxygen profiles were consistent with a higher oxygen demand in the outer region (viz. pericycle, phloem, protoxylem and early metaxylem cylinder) than in the inner core (late metaxylem cylinder and medulla), but the deficits were relatively small (less than or equal to 3 kPa) and consistent with minimal wall thickening in the endodermis and narrowness of stele. The possible relevance of the results to entry of methane and other products from the rhizosphere into root and to the mechanism of aerenchyma formation are discussed. (C) 2000 Annals of Botany Company.

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    M3 - Article

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    JO - Annals of Botany

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