3.2 ǀ Root morphology and Fe2+ exclusion
Iron exclusion by oxygenation of the rhizosphere is a principal adaptation to Fe toxic soils. Because of the very slow diffusion of respiratory gases through water and submerged soil, rice roots must develop an efficient internal aeration system to deliver O2 to submerged tissues and vent respiratory CO2 in the opposite direction. As a root elongates, the cortex degrades forming a network of interconnected gas channels – aerenchyma – connected to lacunae at the shoot base (Yamauchi, Colmer, Pederson & Nakazono, 2018). Oxygen enters from the atmosphere above and diffuses through the aerenchyma to root tissues. In addition, the roots contain a barrier to radial O2 loss in the basal zones. The barrier restricts O2 loss, and thereby permits a greater length of root to be aerated. However, particularly in Fe toxic soils, some degree of O2 loss to the rhizosphere is permitted to exclude Fe2+ by oxidizing it to Fe(III), and possibly for other aerobic processes in the rhizosphere.
Rice genotypes differ in their Fe excluding powers, due to differences in aerenchyma formation, barriers to radial O2 loss, and enzymatic Fe oxidation power (Ando, Yoshida & Nishiyama, 1983; Engel, Asch & Becker, 2012; Mongon, Konnerup, Colmer & Rerkasem, 2014; Yamauchi et al., 2018). Aerenchyma formation is ‘constitutive’. Ethylene signalling has been implicated in the flood-induced enhancement of aerenchyma formation, with involvement also of H2O2 in the programmed cell death that forms the lacunae in shoots (Yamauchi et al., 2018). Wu et al. (2014) reported a QTL for Fe toxicity tolerance on Chromosome 3 associated with Fe exclusion via greater aerenchyma formation.
There is potentially a conflict between the rooting characteristics required for internal aeration and those for Fe2+exclusion and efficient nutrient acquisition. Efficient nutrient uptake and Fe2+ exclusion are favoured by a large external root surface area (but see Section 4.2 for potential negative effects of root exclusion on nutrient uptake), whereas efficient internal aeration requires the opposite. Kirk (2003) developed a model for exploring this, based on steady-state diffusion of O2 through a crown root and its laterals and the simultaneous consumption of O2 in root respiration and loss to the soil. This showed, for a realistic set of parameter values, including rates of O2 loss to the soil at typical rates of Fe2+ oxidation in the rhizosphere, a system of coarse, aerenchmymatous, crown roots with gas-impermeable walls conducting O2 to short, fine, gas-permeable laterals provided the greatest absorbing surface per unit aerated root mass. This is the basic architecture of current rice genotypes.