A barrier to radial oxygen loss helps the root system cope with waterlogging-induced hypoxia

Abstract

Internal aeration is crucial for root growth under waterlogged conditions. Many wetland plants have a structural barrier that impedes oxygen leakage from the basal part of roots called a radial oxygen loss (ROL) barrier. ROL barriers reduce the loss of oxygen transported via the aerenchyma to the root tips, enabling long-distance oxygen transport for cell respiration at the root tip. Because the root tip does not have an ROL barrier, some of the transferred oxygen is released into the waterlogged soil, where it oxidizes and detoxifies toxic substances (e.g., sulfate and Fe²⁺) around the root tip. ROL barriers are located at the outer part of roots (OPRs). Their main component is thought to be suberin. Suberin deposits may block the entry of potentially toxic compounds in highly reduced soils. The amount of ROL from the roots depends on the strength of the ROL barrier, the length of the roots, and environmental conditions, which causes spatiotemporal changes in the root system's oxidization pattern. We summarize recent achievements in understanding how ROL barrier formation is regulated and discuss opportunities for breeding waterlogging-tolerant crops.

Keywords: aerenchyma; apoplastic barrier; flooding; planar O2 optode; rhizosphere oxidation; root system; suberin.

Fig. 1.

Adaptive significance of an ROL barrier for roots in waterlogged soil. (A) Oxygen molecules diffusing longitudinally through aerenchyma toward the root apex may either be consumed by respiration of root cells or diffuse radially to the rhizosphere (called radial oxygen loss, ROL). Although ROL aerates the rhizosphere, it also reduces the supply of oxygen to the root apex. (B) Many wetland species form an ROL barrier in the basal parts of roots. ROL barrier promotes longitudinal oxygen diffusion by preventing losses to anaerobic soils. (i) In anaerobic soils, enhanced movement of oxygen toward the apex enables active respiration of the cells at the root tips. Because the root tip does not have an ROL barrier, (ii) the ROL around the root tip detoxifies toxic reduced substances in the waterlogged soil. (iii) The barrier also blocks the entry of potentially toxic compounds in highly reduced soils.

Fig. 2.

Predicted locations of oxidized rhizosphere and ROL barrier formation along short and long roots. (A) Predicted locations of oxidized soil (blue) in the rhizosphere. (B, C) Radial oxygen loss (green arrows) in very short (<50 mm) roots (B) and long roots (>100 mm) (C).

Fig. 3.

An oxygen-permeable window site in the adventitious roots of Echinochloa colona. Cross-section of an adventitious root showing the location of a window (white arrow) at a site in the exodermis where a lateral root is expected to emerge. The window is composed of passage cells that lack suberin lamellae. Suberin lamellae are indicated as yellow-green fluorescence with Fluorol Yellow 088 (yellow arrowhead). Red arrowhead indicates the pericycle from which lateral root primordia are predicted to emerge. Blue fluorescence indicates autofluorescence. Fluorol Yellow 088 staining was conducted as described in Ejiri and Shiono (2019). The plants were grown in an aerated nutrient solution for ten days and then transferred into a deoxygenated stagnant nutrient solution for 14 days. Abbreviations: CP, cortical parenchyma; end, endodermis; epi, epidermis; exo, exodermis; LP, lateral root primordia; scl, sclerenchyma; ste, stele. Scale bars: 100 μm.