Peter M. Beckett

Root adaptation to soil waterlogging

Abstract The structural diversity of roots is emphasised and adaptation to soil waterlogging is reviewed. Results pertinent to the mechanism of aerenchyma development are presented, and a modelling approach is used to explore the implications for aeration and rhizosphere oxidation of the structural and physiological adaptations of adventitious roots and laterals.

Pathways of aeration and the mechanisms and beneficial effects of humidity- and Venturi-induced convections in Phragmites australis (Cav.) Trin. ex Steud.

The pathways of diffusive, humidity- and Venturi-induced convective ventilations in Phragmites australis (Cav.) Trin. ex Steud., and the mechanisms of the convections are described. Experimental evidence, indicating those factors, e.g. low relative humidity (RH), light, large leaf-sheath area, which increase humidity-induced convection, and those which increase Venturi convections, e.g. high wind speed, are reviewed. The superior aerating effects of convective as opposed to diffusive ventilation within the plant and their influence on the rhizosphere are demonstrated experimentally and by mathematical modelling.

MEASUREMENT AND MODELLING OF OXYGEN RELEASE FROM ROOTS OF PHRAGMITES AUSTRALIS

Radial oxygen flux from adventitious and lateral roots of Phragmites australis in stagnant and streaming oxygen-free waters were measured polarographically. The potential for oxygen release to anaerobic sediments was predicted by extrapolating from this data and by mathematical modelling, and the oxidation of sediments demonstrated by indicator dye and redox potential measurements. Oxygen losses from roots were much greater during the day than at night and reflected the substantial day-time throughflow convection of gases from culm to rhizome which occurs in this species. Lateral roots, borne at frequencies of ≤120/cm of adventitious root were identified as potentially the major source of oxygen release. Predictions of sediment oxygenation based on oxygen release from single adventitious roots plus laterals in a streaming oxygen-free water-flow system, yielded values of 5-12 g O2 m-2 d-1, based on 150 shoots m-2, the conservative estimate of 10 roots per shoot, and a mean rhizome oxygen concentration of 17%. Mathematical modelling predictions amounted to 4.6-9.6 g of O2 m-2 d-1 based on the same shoot and root numbers, with 600 laterals/root, soil oxygen demand of 50-500 ng cm-3 s-1, and soil oxygen diffusivities from 0.3(clay)-0.85(sand) x 10-5 cm2 s-1. It was estimated that the respective amounts of oxygen likely to diffuse into the sediment from the soil surface would be be 1.0-7.3 g m-2 d-1. It is emphasised that sediment oxygenation by roots may be enhanced proportionally only by greater root numbers, not greater sediment oxygen demand.

Pressurised ventilation in emergent macrophytes: the mechanism and mathematical modelling of humidity-induced convection

Abstract Humidity-induced diffusion (HID) and convection (HIC: pressure flow) are described for a simple physical model and are mathematically modelled. The physical model comprises a cylindrical chamber, partially filled with water, and capped by a micro-porous partition (membrane); an outflow pipe with a tap vents gases from the header space to the outside. The mathematical model comprises a series of equations which embrace the effects of header space depth and boundary layer thickness, the diffusive- and any Poiseuille-flow resistances of the partition, and the venting path resistance. For membrane pore diameters within (i.e. ≤ 0.1 μm) or outside the Knudsen regime, close correlations are found between experimental values of static and dynamic pressure and convective flows, and those obtained from the mathematical model. The findings suggest that for plants, compromises are necessary between factors such as small pore widths, which can help generate high dynamic pressures, and the need for wider pore widths to support greater flows. It is shown that the fastest flows are generated at pore diameters of ca. 0.2 μm, and it is suggested that the high rates of flow found in Phragmites are achieved because of an optimum leaf sheath stomatal pore width coupled to very low venting resistance through the plant. The benefits of a sustained humidifying source close to the base of the pores is also highlighted, and attention is drawn to thermally enhanced HIC and the continuance of HIC when temperatures within the plant might be lower than outside. The results have important implications for understanding convective gas flow generation in plants and its potential for enhancing ‘greenhouse gas’ emissions from wetlands.

PRESSURISED AERATION IN WETLAND MACROPHYTES: SOME THEORETICAL ASPECTS OF HUMIDITY-INDUCED CONVECTION AND THERMAL TRANSPIRATION

The pressurised gas-flows, humidity-induced convection (HIC) and thermal transpiration (TT), which are important for aeration and for greenhouse gas emissions in some wetland macrophytes, are described and discussed. Results obtained from simple mathematical modelling of the processes are presented to illustrate some of their more relevant features. It is emphasised that both processes require the presence of a micro-porous partition having a significantly greater resistance to pressure flow than to diffusion. In particular it is shown that whilst the potential to pressurise by these processes is inversely related to the pore diameters of the partition, the maximum gas flows are generated where pore diameters range from 0.1 to 0.2 μm. Where partitions are a surface feature (e.g. emergent macrophytes) a dominant role for HIC is predicted; where partitions are an embedded feature (e.g. water-lilies) it is deduced that HIC will still play a significant role, but the contribution of TT could be greater.

Mathematical modelling of methane transport by Phragmites: the potential for diffusion within the roots and rhizosphere

The release of methane into the atmosphere by Phragmites australis (Cav.) Trin. ex Steud. can be considered as a two-stage process. The first, a mainly diffusive movement through the rhizosphere from the anaerobic source regions of the soil and into and along the roots to the root–rhizome junction. The second, the removal of the gas from the root–rhizome junction to the atmosphere through the rhizome–culm system, a process often dominated by convective (pressurised) gas flow. This article addresses the first of these stages and is presented in isolation because of its perceived commonality to wetland plants in general. The model treats the root and its oxygenated rhizosphere as a series of concentric cylinders: two non-(or low) porosity stelar cylinders, a highly porous cortex, a non-porous epidermal/hypodermal cylinder and the rhizosphere itself. The methane source lies at the edge of the oxygenated rhizosphere the dimensions of which are determined by the integrated effects of oxygen consumption in root and rhizosphere (the latter including a methanotrophic element) and the diffusive impedances throughout the system. The results demonstrate something of the complexity of root-methane–oxygen relations. Methane entry from the rhizosphere is shown to vary along the length of any individual root and, as expected, methane oxidation within the rhizosphere is found to reduce the potential for methane loss to the atmosphere. Situations are also revealed: (i) where the methane concentration falls to zero within the rhizosphere because of aerobic microbial consumption supported by radial oxygen loss from the root, and (ii) where methane may enter the root at one point and escape to the rhizosphere at some other. In this latter case, methane concentration minima are possible within the rhizosphere supplied by methane fluxes from both the root and the bulk soil. Predictions of the quantities of methane which might be released via Phragmites roots to the atmosphere accord with examples of those previously reported from field data.

Exploring the Radial and Longitudinal Aeration of Primary Maize Roots by Means of Clark-Type Oxygen Microelectrodes

Clark-type oxygen microelectrodes were used to measure the radial and longitudinal oxygen distribution in aerenchymatous and nonaerenchymatous primary roots of intact maize seedlings. A radial intake of oxygen from the rooting medium was restricted by embedding the roots in 1% agar causing aeration to be largely dependent upon longitudinal internal transport from the shoot. In both root types, oxygen concentrations declined with distance from the base, and were lower in the stele than in the cortex. Also, the bulk of the oxygen demand was met internally by transport from the shoots, but a little oxygen was received by radial inward diffusion from the surrounding agar, and in some positions the hypodermal layers received oxygen from both the agar and the cortex. Near to the base, the oxygen partial pressure difference between the cortex and the center of the stele could be as much as 6–8 kPa. Nearer to the tip, the differences were smaller but equally significant. In the nonaerenchymatous roots, cortical oxygen partial pressures near the apex were becoming very low (< 1 kPa) as root lengths approached 100 mm, and towards the center of the stele values reached 0.1 kPa or lower. However, the data indicated that respiratory activity did not decline until the cortical oxygen pressure was less than 2 kPa. Mathematical modeling based on Michaelis–Menten kinetics supported this and suggested that the respiratory decline would be mostly restricted to the stele until cortical oxygen pressures approached very low values. At a cortical oxygen pressure of 0.75 kPa, it was shown that respiratory activity in the pericycle and phloem might remain as high as 80–100% of maximum even though in the center of the stele it could be less than 1% of maximum. Aerenchyma production resulted in increases in oxygen concentration throughout the roots with cortical partial pressures of ca. 5–6 kPa and stelar values of ca. 3–4 kPa near the tips of 100 mm long roots. In aerenchymatous roots, there was some evidence of a decline in the oxygen permeability of the epidermal–hypodermal cylinder close to the apex; a decline in stelar oxygen permeability near the base was indicated for both root types. There was some evidence that the mesocotyl and coleoptile represented a very significant resistance to oxygen transport to the root.

Experimental and modelling data contradict the idea of respiratory down-regulation in plant tissues at an internal [O2] substantially above the critical oxygen pressure for cytochrome oxidase.

• Some recent data on O(2) scavenging by root segments showed a two-phase reduction in respiration rate starting at/above 21 kPa O(2) in the respirometer medium. The initial decline was attributed to a down-regulation of respiration, involving enzymes other than cytochrome oxidase, and interpreted as a means of conserving O(2). As this appeared to contradict earlier findings, we sought to clarify the position by mathematical modelling of the respirometer system. • The Fortran-based model accommodated the multicylindrical diffusive and respiratory characteristics of roots and the kinetics of the scavenging process. Output included moving images and data files of respiratory activity and [O(2)] from root centre to respirometer medium. • With respiration at any locus following a mitochondrial cytochrome oxidase O(2) dependence curve (the Michaelis-Menten constant K(m) = 0.0108 kPa; critical O(2) pressure, 1-2 kPa), the declining rate of O(2) consumption proved to be biphasic: an initial, long semi-linear part, reflecting the spread of severe hypoxia within the stele, followed by a short curvilinear fall, reflecting its extension through the pericycle and cortex. • We conclude that the initial respiratory decline in root respiration recently noted in respirometry studies is attributable to the spread of severe hypoxia from the root centre, rather than a conservation of O(2) by controlled down-regulation of respiration based on O(2) sensors.

A modelling approach to the analysis of pressure-flow in Phragmites stands

Abstract Field studies have shown that resistance to convective gas-flow within the culm-rhizome gas-space system of Phragmites tends to be higher in ‘die-back’ as opposed to healthy stands. However, the collection of reliable data and its interpretation is complicated by many factors. To help interpret field measurements and further our understanding of convective flows in general, we have developed mathematical models based on the humidity-induced convective-flow generating potential of culms. Among other things, these make it possible to study the effects on pressure flows of increasing flow resistances in rhizomes and between culms, of different pressure-generating potentials of interlinked culms and of different numbers of efflux culms. A multi-culm and rhizome model is described together with some simple examples of the way it can prove helpful in interpreting some of the field observations from healthy and die-back sites. Increased venting resistance reduced flows curvilinearly; increasing the counter pressure to mimic those induced by other interlinked living culms reduced flows linearly. In some of the multi-culm examples shown counter-pressure exerted an effect approximately the same as that of rhizome and venting resistance, but as culm numbers declined it assumed even greater importance. The value of conductivity derived from applying pressures to the stubble of excised culms and measuring the flows induced, proved to be a composite measure of the effective conductivity of the whole rhizome-culm train rather than that of the rhizome plus major vent. The expression 1−(Pd/Ps) — the delivery coefficient — where Pd is the dynamic pressure in the base of the intact culm, and Ps the static pressure developed by the culm with the outflow blocked, was identified as a useful and easily obtained measure of the ability of an individual intact culm to contribute to the convective gas-flow in a stand, and one which should be relatively unaffected by weather conditions. For identical interlinked culms it was shown that the flows from all culms fitted exactly along the same line of declining flow versus dynamic pressure irrespective of the numbers of culms or number and position of outflow vents.