Silicon-phosphorus pathway mitigates heavy metal stress by buffering rhizosphere acidification

Heavy metal pollution threatens food security, and rhizosphere acidification will increase the bioavailability of heavy metals. As a beneficial element in plants, silicon can relieve heavy metal stress. However, less attention has been paid to its effects on plant rhizosphere processes. Here, we show that for Japonica (Nipponbare and Oochikara) and Indica (Jinzao 47) rice cultivars, the degree of root acidification was significantly reduced after silicon uptake, and the total organic carbon, citric acid, and malic acid concentrations in rice root exudates were significantly reduced. We further confirmed the results by q-PCR that the expressions of proton pump and organic acid secretion genes were down-regulated by 35–61 % after silicon treatment. Intriguingly, phosphorus allocation, an intensively studied mechanism of rhizosphere acidification, was altered by silicon treatment. Specifically, among total phosphorus in rice seedlings, the soluble proportion increased from 52.0 % to 61.7 %, while cell wall phosphorus decreased from 48.0 % to 32.3 %. Additionally, silicon-mediated alleviation of rhizosphere acidification has positive effects on relieving heavy metal stress. Simulation revealed that low acidification of the nutrient solution resulted in a decrease in bioavailable heavy metal concentrations, thereby reducing rice uptake. We further confirmed that the impediment of rhizosphere acidification led to free-state Cr3+ in solutions decreasing by 43 % and contributed up to 63 % of silicon's mitigation of Cr(III) stress. Overall, we propose a novel mechanism in which silicon reduces heavy metal absorption by increasing plant soluble phosphorus concentration and buffering rhizosphere acidification. This paper provides a unique insight into the role of silicon in plants and, more importantly, a theoretical reference for the rational application of silicon fertilizer to improve phosphorus utilization efficiency, alleviate heavy metal stress, and balance soil pH. [Display omitted] •The Si-P pathway is a new mechanism for plants to alleviate heavy metal stress.•Si can reduce rhizosphere acidification degree and organic acid secretion of rice.•Si competes with P for adsorption sites in cell walls to increase soluble P in rice.•Increased soluble phosphorus in rice is responsible for decreased root secretion.•Obstruction of rhizosphere acidification reduces the bioavailability of heavy metals.