Nitric oxide mediates aluminum-induced citrate secretion through regulating the metabolism and transport of citrate in soybean roots

Abstract

Citrate secretion is a kind of typical strategy for plant against aluminum (Al) toxicity. However, the signaling process in Al-activated citrate secretion needs to be clarified. Physiological and biochemical methods as well as gene expression analysis were employed to examine the regulatory roles of nitric oxide (NO) in Al-activated citrate secretion in soybean roots. Application of NO donor alleviated root growth inhibition and decreased Al content in Al-treated root apices. Al-induced NO production and citrate secretion were further elevated by NO donor, but inhibited by NO scavenger. Inhibition of citrate synthase (CS) or plasma membrane (PM) H+-ATPase activity significantly decreased Al-induced secretion of citrate, but inhibition of aconitase (ACO) activity enhanced citrate secretion under Al stress. Furthermore, NO mediated Al-stimulated CS and PM H+-ATPase activities, but decreased ACO activity under Al stress. Further investigation showed that NO modulated Al-activated transcriptional expression of CS and PM H+-ATPase as well as GmMATE. Overexpression of GmMATE in soybean hairy roots caused an enhanced Al-induced citrate efflux and Al resistance. Our findings suggest that NO-dependent up-regulation of citrate synthesis and activation of PM H+-ATPase-coupled MATE transporter co-transport system participates in Al-activated citrate exudation, thus conferring plant resistance to Al toxicity.