4.1 ǀ Root-induced change in the rhizosphere
The following root-induced changes in the soil occur in the region of the root tip and along the length of fine laterals where the bulk of nutrient uptake happens (Figure 2c).
Ferrous iron oxidation. Oxygen diffusing down through a root’s aerenchyma leaks out into the soil, which has a much lower O2 concentration. Mobile inorganic reductants in the soil are oxidized, particularly Fe2+ which is precipitated as Fe(OH)3 on or near the root. As a result the concentration of Fe2+ near the root falls and more Fe2+ moves in from the bulk soil by diffusion and mass flow in the transpiration stream. This is then oxidized resulting in a zone of Fe(OH)3 accumulation near the root (Begg, Kirk, Mackenzie & Neue, 1994). Each mol of Fe2+ oxidized generates 2 mol of H+ (Figure 2c), so the pH in the oxidation zone tends to fall. Away from the root tip, in zones where there is no release of O2 from the roots, Fe(OH)3 may be re-reduced to Fe2+ in anaerobic respiration fuelled by organic substrates released from the roots (Benckiser, Santiago, Neue, Watanabe & Ottow, 1984). This effect may be greater under nutrient deficiencies as a result of leaky root membranes, resulting in exacerbated Fe toxicity.
CO2 uptake into roots. Large dissolved CO2 concentrations develop in submerged rice soils (equivalent partial pressures 5–70 kPa – Greenway, Armstrong & Colmer, 2006; Kirk et al., 2019; Ponnamperuma, 1972) because CO2 formed in root and soil respiration escapes only slowly by diffusion through the water-filled soil pores. There is therefore a large CO2 gradient between the soil and the aerenchyma inside the root. Hence CO2 will enter the roots and be vented to the shoots and atmosphere by diffusion through the aerenchyma. Kirk et al. (2019) showed that CO2venting through rice roots can be equivalent to a third of the daily CO2 fixation in photosynthesis. Net removal of CO2 decreases the concentration of the acid H2CO3 near the root, and this may offset the acidity produced in Fe2+ oxidation and excess cation uptake (Affholder, Weiss, Wissuwa, Johnson-Beebout & Kirk, 2017; Begg et al., 1994).
Proton release due to excess cation over anion intake. Because the main form of plant-available N in anaerobic soil is NH4+, the root absorbs an excess of nutrient cations (NH4+, K+, Na+, Ca2+, Mg2+, Fe2+) over anions (H2PO4-, Cl-, SO42-). Consequently H+ is released by the root to maintain electrical neutrality, tending to further decrease the pH. Note that if any N is taken up as NO3- as a result of nitrification of NH4+ in the rhizosphere (see below), the net acid-base change is the same because, although the root exports 2 mol less H+ for each mol of NO3- replacing a mol of NH4+, 2 mol of H+are formed in the nitrification of each mol of NH4+. Note also that Si, which is taken up in large quantities by rice plants, crosses the root as the uncharged H4SiO4 molecule (pK 1 = 9.46 at 25oC).
Net changes. The net effects of these processes will depend on their rates versus rates of buffering processes in the soil. In typical, acidic Fe toxic soils, the dominant effect is likely to be a decrease in pH at the root surface due to the large amount of H+produced in Fe2+ oxidation. Begg et al. (1994) found the rhizosphere of rice in an Fe toxic soil was acidified by two pH units from 6.5 in the soil bulk to 4.5 at the root surface. The pH profile across the rhizosphere will depend on the net rate of H+ generation near the root versus the rate at which the pH change is propagated away through the soil by acid-base transfer. Generally, the main acid-base pairs involved are H3O+–H2O and H2CO3–HCO3-: H3O+ ions move away from the acidification zone to the soil bulk which has a higher pH, and HCO3- towards it. The resulting pH change will be greatest in the pH range in which H3O+ and HCO3- concentrations are both low (typically pH 4.5–6.0, depending on the soil CO2pressure), as shown in the model calculations in Figure 2d,e. Hence the pH decrease will be greater in Fe toxic soils with already low pH and relatively low dissolved CO2.
Although Fe plaque on root surfaces is generally focused on in the literature, most of the Fe(OH)3 is precipitated in the rhizosphere over a mm or two from the root surface (Kirk, Ahmad & Nye, 1990). The profile of Fe(OH)3 may be banded in ‘Liesegang’ rings centred on the root axis. This happens because sorption of Fe2+ on the soil solid – and hence its mobility and rate of oxidation – is pH dependent, decreasing as the pH decreases. Therefore some of the Fe2+ locally diffuses ahead of the oxidation front towards the higher pH zone, where it is more-strongly sorbed. The total Fe profile is therefore banded.
ǀ Effects of root-induced changes on nutrient ions in the rhizosphere
The sharp gradients in redox and pH across the rhizosphere resulting from the above changes will greatly affect its chemistry and biology, and hence nutrient and toxin uptake by roots.
Ammonium and nitrate. In some circumstances, a significant part of the N taken by rice in submerged soils is as NO3- formed by nitrification of NH4+ in the rhizosphere (Kirk & Kronzucker, 2005). Studies on the kinetics of N uptake and assimilation show that lowland rice is exceptionally efficient in absorbing and assimilating NO3- compared with other plant species (Kronzucker, Siddiqi, Glass & Kirk, 2000). This is important because plant growth and yield are generally improved when plants absorb their N as a mixture of NO3- and NH4+ compared with growth on either N source on its own. In Fe toxic soils, rates of nitrification in the rhizosphere are likely to be impeded both by competition for root-released O2 with Fe2+ oxidation, and because the rhizosphere is acidified. The proportion of N absorbed as NO3- will be correspondingly lowered.
There may be a further effect on N nutrition through an interaction with CO2 venting through the roots (Kirk et al., 2019). Concentrations of dissolved CO2 tend to be smaller in Fe toxic soils because of lower rates of microbial respiration (Section 2). But in submerged soils with high dissolved CO2concentrations, enhanced availability of CO2 in the roots may have a growth stimulating effect by facilitating anaplerotic production of organic acids for amino acid synthesis (Balkos, Britto & Kronzucker, 2010; Britto & Kronzucker, 2005). This is potentially important because all the NH4+ taken up by rice is assimilated into amino acids in the roots before being transported to the shoots, requiring carbon skeletons (Kronzucker et al., 2000). Rice in Fe toxic soil with lower dissolved CO2 concentrations would not benefit from this.
Exchangeable cations. An unexplored consequence of the changes in the rhizosphere, likely to be important in Fe toxic soils, is the effect on nutrient cations such as K+, Ca2+ and Mg2+. The following factors will tend to decrease the concentration of nutrient cations in the soil solution where they are available for uptake by roots.
  1. The overall concentration of the solution in a submerged soil is generally controlled by the concentration of bicarbonate anions (HCO3-), formed from dissolved CO2 (Kirk 2004). If the pH decreases below about 6.0, the concentration of HCO3- in solution will decrease and so the concentration of cations in solution balanced by the anions must also decrease.
  2. A decrease in pH will also mean the negative charge on soil surfaces and therefore the cation exchange capacity will tend to decrease.
  3. However, removal of exchangeable Fe2+ as it is oxidised will mean a greater proportion of surface exchange sites is occupied by non-Fe cations.
Hence the need to exclude toxic Fe2+ from the root by oxidizing it in the rhizosphere may impair the absorption of nutrient cations by the root. Genotypes with greater Fe oxidizing power may make things worse for themselves in Fe toxic soils deficient in nutrient cations.
Phosphate and other ions. Phosphate anions may be immobilised on iron plaque and freshly precipitated Fe(OH)3 in the rhizosphere. On the other hand, in P-deficient soils, acid-soluble forms of P in the soil may be solubilized by acidification of the rhizosphere, resulting in increased uptake into roots (Jianguo & Shuman, 1991; Saleque & Kirk, 1995). Likewise acid-soluble forms of Zn may be solubilized in Zn-deficient soils (Kirk & Bajita, 1995). Possibly uptake of micro-nutrients is enhanced at low levels of Fe plaque as a result of a concentrating effect close to absorbing root surfaces (Kirk & Bajita, 1995; Zhang, Zhang & Mao, 1996, 1999).