From promoting aggregation to enhancing obstruction: A negative feedback regulatory mechanism of alleviation of trivalent chromium toxicity by silicon in rice

Abstract

Trivalent chromium [Cr(III)] is a threat to the environment and crop production. Silicon (Si) has been shown to be effective in mitigating Cr(III) toxicity in rice. However, the mechanisms by which Si reduces Cr(III) uptake in rice are unclear. Herein, we hypothesized that the ability of Si to obstruct Cr(III) diffusion via apoplastic bypass is related to silicic acid polymerization, which may be affected by Cr(III) in rice roots. To test this hypothesis, we employed hydroponics experiments on rice (Oryza sativa L.) and utilized apoplastic bypass tracer techniques, as well as model simulations, to investigate 1) the effect of Si on Cr(III) toxicity and its obstruction capacity via apoplastic bypass, 2) the effect of Cr(III) on silicic acid polymerization, and 3) the relationship between the degree of silicic acid polymerization and its Cr(III) obstruction capacity. We found that Si reversed the damage caused by Cr(III) stress in rice. Si exerted an obstruction effect in the apoplast, significantly decreasing the share of Cr(III) uptake via the apoplastic bypass from 18% to 11%. Moreover, Cr(III) reduced silica particles' radii and increased Si concentration in roots. Modeling revealed that a 5-fold reduction in their radii decreased the diffusion of Cr(III) in apoplast by approximately 17%. We revealed that Cr(III) promoted silicic acid polymerization, resulting in the formation of a higher number of Si particles with a smaller radius in roots, which in turn increased the ability of Si to obstruct Cr(III) diffusion. This negative feedback regulatory mechanism is novel and crucially important for maintaining homeostasis in rice, unveiling the unique role of Si under Cr(III) ion stress and providing a theoretical basis for promoting the use of Si fertilizer in the field.