Abstract
Lysigenous aerenchyma, which develops by death and subsequent lysis of the cortical cells in roots, is essential for internal long-distance oxygen transport from shoot base to root tips of plants in waterlogged soil. Although many studies focus on the amounts of aerenchyma in roots, significance of the size of the root cortex in which aerenchyma forms has received less research attention. In the present study, we evaluated the cross-sectional area of each root tissue in adventitious roots of upland crops, wheat (Triticum aestivum) and maize (Zea mays ssp. mays), and the wetland crop, rice (Oryza sativa) under aerated or stagnant deoxygenated conditions; the latter can mimic the changes in gas composition in waterlogged soils. Our analyses revealed that the areas of whole root and cortex of the three species increased under stagnant conditions. In rice roots, cortex to stele ratio (CSR) and aerenchyma to cortex ratio (ACR), which is associated with the areas of gas spaces, were much higher than those in wheat and maize roots, suggesting that these anatomical features are essential for a high capacity for oxygen transport along roots. To test this hypothesis, rates of radial oxygen loss (ROL), which is the diffusive flux of oxygen from within a root to the external medium, from thick and thin adventitious roots of rice were measured using a cylindrical (root-sleeving) oxygen electrode, for plants with shoots in air and roots in an oxygen-free medium. As expected, the rate of ROL from thick roots, which have larger cortex and aerenchyma areas, was higher than that of thin roots. The rate of ROL was highest at the apical part of rice roots, where aerenchyma was hardly detected, but at which cuboidal cell arrangement in the cortex provides tissue porosity. We conclude that high CSR in combination with large root diameter is a feature which promotes oxygen transport from shoot base to root tips of plants. Moreover, we propose that CSR should be a useful quantitative index for the evaluation and improvement of root traits contributing to tolerance of crops to soil waterlogging.
Highlights
Roots are mainly composed of four concentric cell layers: from the outside to inside, these cell layers are the epidermis, cortex, endodermis, and stele (Scheres et al, 2002)
(1) How is cortex to stele ratio (CSR) related with plant adaptation to waterlogging? (2) Does CSR affect the amount of gas space in root? (3) What is the adaptive value of high CSR in terms of root aeration? To this end, we evaluated growth of wheat, maize, and rice seedlings under aerated or stagnant deoxygenated conditions, which can mimic the changes in gas composition in waterlogged soils
aerenchyma to cortex ratio (ACR) in rice roots under stagnant conditions was respectively 1.8-fold and 1.5-fold higher than that in wheat and maize roots (Figure 3A), and CSR in rice roots under stagnant conditions was respectively 2.8-fold and 3.5-fold higher than that in wheat and maize roots (Figure 3B). These results indicate that rice roots have more aerenchyma within cortex when compared with wheat and maize roots, and suggest that higher CSR in rice roots further amplifies the ratio of aerenchyma within whole root
Summary
Roots are mainly composed of four concentric cell layers: from the outside to inside, these cell layers are the epidermis, cortex, endodermis, and stele (Scheres et al, 2002). Aerenchyma consists of longitudinally connected gas spaces which enhances the diffusion of oxygen within plants (Armstrong, 1979; Colmer, 2003b). In addition to the large amount of aerenchyma, rice roots form a barrier impermeable to radial oxygen loss (ROL), and this further enhances longitudinal oxygen diffusion from shoot base to the root tip (Armstrong, 1979; Colmer et al, 1998; Kotula et al, 2009; Shiono et al, 2011). In contrast to the many wetland species, none of the upland crops have ROL barrier in the roots, and its formation is an important mechanism for plants to adapt to waterlogging (Colmer, 2003b)
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