Abstract
Al³⁺ and H⁺ toxicities predicted to occur at moderately acidic conditions (pH [water] = 5-5.5) in low-Ca soils were characterized by the combined approaches of computational modeling of electrostatic interactions of ions at the root plasma membrane (PM) surface and molecular/physiological analyses in Arabidopsis (Arabidopsis thaliana). Root growth inhibition in known hypersensitive mutants was correlated with computed {Al³⁺} at the PM surface ({Al³⁺}(PM)); inhibition was alleviated by increased Ca, which also reduced {Al³⁺}(PM) and correlated with cellular Al responses based on expression analysis of genes that are markers for Al stress. The Al-inducible Al tolerance genes ALUMINUM-ACTIVATED MALATE TRANSPORTER1 and ALUMINUM SENSITIVE3 were induced by levels of {Al³⁺}(PM) too low to inhibit root growth in tolerant genotypes, indicating that protective responses are triggered when {Al³⁺}(PM) was below levels that can initiate injury. Modeling of the H⁺ sensitivity of the SENSITIVE TO PROTON RHIZOTOXICITY1 knockout mutant identified a Ca alleviation mechanism of H⁺ rhizotoxicity, possibly involving stabilization of the cell wall. The phosphatidate phosphohydrolase1 (pah1) pah2 double mutant showed enhanced Al susceptibility under low-P conditions, where greater levels of negatively charged phospholipids in the PM occur, which increases {Al³⁺}(PM) through increased PM surface negativity compared with wild-type plants. Finally, we found that the nonalkalinizing Ca fertilizer gypsum improved the tolerance of the sensitive genotypes in moderately acidic soils. These findings fit our modeling predictions that root toxicity to Al³⁺ and H⁺ in moderately acidic soils involves interactions between both toxic ions in relation to Ca alleviation.
Highlights
Al3+ and H+ toxicities predicted to occur at moderately acidic conditions in low-Ca soils were characterized by the combined approaches of computational modeling of electrostatic interactions of ions at the root plasma membrane (PM)
To validate the predictions obtained from the SGCS modeling studies in wheat, where {Al3+}PM determines Al rhizotoxicity at moderately acidic conditions, we were required to use a sensitive phenotype at pH greater than 5 that could provide sufficient data sets
We found that accurate speciation is critical to simulate Al rhizotoxicity in the complex nutrient solution used to grow Arabidopsis (Supplemental Fig. S1), whereas the previous speciation program in the SGCS program was based on more simple nutrient solutions (e.g. CaCl2 plus AlCl3)
Summary
Al3+ and H+ toxicities predicted to occur at moderately acidic conditions (pH [water] = 5–5.5) in low-Ca soils were characterized by the combined approaches of computational modeling of electrostatic interactions of ions at the root plasma membrane (PM). We found that the nonalkalinizing Ca fertilizer gypsum improved the tolerance of the sensitive genotypes in moderately acidic soils. These findings fit our modeling predictions that root toxicity to Al3+ and H+ in moderately acidic soils involves interactions between both toxic ions in relation to Ca alleviation. The complex rhizotoxicities at moderately acidic conditions that can be alleviated by Ca have been predicted by modeling studies in wheat (Triticum aestivum; Kinraide, 2003).
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