Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots

By Timothy D. Colmer. 2003

1,157 citations recorded by the source corpus.

Internal transport of gases is crucial for vascular plants inhabiting aquatic, wetland or flood-prone environments. Diffusivity of gases in water is approximately 10 000 times slower than in air; thus direct exchange of gases between submerged tissues and the environment is strongly impeded. Aerenchyma provides a low-resistance internal pathway for gas transport between shoot and root extremities. By this pathway, O2 is supplied to the roots and rhizosphere, while CO2, ethylene, and methane move from the soil to the shoots and atmosphere. Diffusion is the mechanism by which gases move within roots of all plant species, but significant pressurized through-flow occurs in stems and rhizomes of several emergent and floating-leaved wetland plants. Through-flows can raise O2 concentrations in the rhizomes close to ambient levels. In general, rates of flow are determined by plant characteristics such as capacity to generate positive pressures in shoot tissues, and resistance to flow in the aerenchyma, as well as environmental conditions affecting leaf-to-air gradients in humidity and temperature. O2 diffusion in roots is influenced by anatomical, morphological and physiological characteristics, and environmental conditions. Roots of many (but not all) wetland species contain large volumes of aerenchyma (e.g. root porosity can reach 55%), while a barrier impermeable to radial O2 loss (ROL) often occurs in basal zones. These traits act synergistically to enhance the amount of O2 diffusing to the root apex and enable the development of an aerobic rhizosphere around the root tip, which enhances root penetration into anaerobic substrates. The barrier to ROL in roots of some species is induced by growth in stagnant conditions, whereas it is constitutive in others. An inducible change in the resistance to O2 across the hypodermis/exodermis is hypothesized to be of adaptive significance to plants inhabiting transiently waterlogged soils. Knowledge on the anatomical basis of the barrier to ROL in various species is scant. Nevertheless, it has been suggested that the barrier may also impede influx of: (i) soil-derived gases, such as CO2, methane, and ethylene; (ii) potentially toxic substances (e.g. reduced metal ions) often present in waterlogged soils; and (iii) nutrients and water. Lateral roots, that remain permeable to O2, may be the main surface for exchange of substances between the roots and rhizosphere in wetland species. Further work is required to determine whether diversity in structure and function in roots of wetland species can be related to various niche habitats.

Subfields: Ecology, Plant Science

View Paper: https://www.semanticscholar.org/paper/1cb6b91795c48325f978abbcd6a8c03278c77b58

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Citations in the corpus

Root cortex : structural and functional variability and responses to environmental stress (2004, background): “However, they were covered by gas-impermeable peripheral cortical layers (Morita and Nemoto, 1995; Colmer, 2003; Fig. 1B).”
An integrated perspective to explain nitrogen mineralization in grazed ecosystems (2013, background): “…soil moisture, thereby selecting for plant species olerant to waterlogging, such as species that possess specific root raits (e.g. the formation of aerenchyma or radial oxygen loss) that llow them to cope with reduced oxygen availability in the soil Justin and Armstrong, 1987; Colmer, 2003).”
Suberin lamella development in maize seedling roots grown in aerated and stagnant conditions (2005, background): “There have been a number of studies on roots of wetland plants growing under oxygen-deficient conditions that provide both indirect and direct evidence that hypoxia stimulates exodermal development (see review by Colmer 2003 and references therein).”
Flooding Stress on Plants: Anatomical, Morphological and Physiological Responses (2012, background): “Suberin is the most likely candidate to function as barrier to oxygen leakage (Colmer, 2003a,b; Colmer et al., 2006; Kotula et al., 2009; Shiono et al., 2011; Ranathunge et al., 2011).”
An overview of plant responses to soil waterlogging (2008, background): “Indeed, there is clear evidence that in flooded soils, an O2 gradient exists between the stele, which may be under anoxic conditions, and the cortical cells which may only be under hypoxic conditions (Thomson and Greenway 1991; Colmer 2003).”
Acclimation of a terrestrial plant to submergence facilitates gas exchange under water (2004, background): “Another common response of floodplain species is the increase of the amount of air spaces (aerenchyma) within the shoot and the roots to optimize within-plant gas transport (Colmer 2003).”
Mechanisms of waterlogging tolerance in wheat: Morphological and metabolic adaptations under hypoxia or anoxia (2011, background): “…and results in a small zone of oxygenated soil around the roots providing an aerobic environment for microorganisms that can prevent the influx of potentially toxic soil components (Visser et al., 1997; Armstrong and Armstrong 1988; Colmer, 2003) such as nitrites and sulphides of Fe, Cu and Mn.”
Sulphide intrusion in eelgrass (Zostera marina L.) (2004, background): “ Colmer 2003 ). It seems puzzling, however, that, when measuring sulphide concentrations in different parts of the same rhizome, there were considerable time lags in the appearance of the sulphide signals.”
Growth Control by Ethylene: Adjusting Phenotypes to the Environment (2007, background): “These would include the formation of longitudinal air channels (aerenchyma; He and others 1992), which allow gases, notably O2, to diffuse from the emerging shoot into the root system ( Colmer 2003 ).”
Oxygen Movement in Seagrasses (2007, background): “The formation of air-spaces within below-ground tissues seems to be stimulated by ethylene produced under conditions with low internal oxygen contents (Drew et al., 2000; Colmer, 2003), and lacunal development in eelgrass has been shown to increase with higher sediment organic content and lower redo”
Biochemical cycling in the rhizosphere having an impact on global change (2009, neutral): “Transport is linked to root porosity (intercellular gas spaces and aerenchyma), which differ substantially among plants (Colmer 2003) but also within genus (e.”
Root anatomy and soil resource capture (2021, background): “The exodermis, hypodermis, and endodermis are often embedded with suberin and/or lignin which regulate the movement of water and ions, primarily though reducing apoplastic transport (Steu-dle 2000; Colmer 2003; Enstone et al. 2003; Schreiber et al. 2005).”