The carbon cost of protecting the root apex from soil acidity: A theoretical framework

There is an assumption in much recent literature that secreted organic anions (OAs) protect the root meristem from Al toxicity by complexation of Al ions. In fact, several possible mechanisms exist by which common OA might afford some degree of protection. Plants can excrete OA which undergo chemical association with protons (hereafter referred to as protonation) in the soil and increase rhizosphere pH. The cost in reduced carbon relative to protons consumed, C:H+, ranges from 2'6. The efficiency of this mechanism can be enhanced in the presence of soil organisms which can oxidise the OA that remain dissociated at soil pH to CO2 and H2O, thereby consuming protons which associate with lower pK functional groups (pK 1.2 to ~ 4). For fully dissociated organic acids the C:H+ ratio decreases to the range 1'3. The C cost to plants is further minimised if MnO2 is the terminal electron acceptor rather than O2, resulting in C:H+<1. OA might also complex or chelate Al. Complexes of Al3+ with oxalate appear to be effective, with some C:H+'1. However, citrate complexation appears to be more stable in pure solutions and might offer the additional benefit of enhanced P acquisition. Our assessment is that the most efficient strategy for a plant to employ to protect itself from Al toxicity is to increase pH near the root apex by secreting OA into soil where the microbial oxidation of reduced C could be coupled with the reduction of MnO2. This would consume 0.2'0.67 mole of C per H+, which is the order of magnitude better than the C:H+ ratio of 2'6 that would occur if only protonation of OA was to be relied upon. These mechanisms have implications for the effectiveness of programs aimed at selecting cultivars for resistance to acidic soils.