Interactions between hydrogen sulphide and nitric oxide regulate two soybean citrate transporters during the alleviation of aluminium toxicity

Abstract

Hydrogen sulphide (H2S) is emerging as an important signalling molecule involved in plant resistance to various stresses. However, the underlying mechanism of H2S in aluminium (Al) resistance and the crosstalk between H2S and nitric oxide (NO) in Al stress signalling remain elusive. Citrate secretion is a wide-spread strategy for plants against Al toxicity. Here, two citrate transporter genes, GmMATE13 and GmMATE47, were identified and characterized in soybean. Functional analysis in Xenopus oocytes and transgenic Arabidopsis showed that GmMATE13 and GmMATE47 mediated citrate exudation and enhanced Al resistance. Al treatment triggered H2S generation and citrate exudation in soybean roots. Pretreatment with an H2S donor significantly elevated Al-induced citrate exudation, reduced Al accumulation in root tips, and alleviated Al-induced inhibition of root elongation, whereas application of an H2S scavenger elicited the opposite effect. Furthermore, H2S and NO mediated Al-induced GmMATE expression and plasma membrane (PM) H+-ATPase activity and expression. Further investigation showed that NO induced H2S production by regulating the key enzymes involved in biosynthesis and degradation of H2S. These findings indicate that H2S acts downstream of NO in mediating Al-induced citrate secretion through the upregulation of PM H+-ATPase-coupled citrate transporter cotransport systems, thereby conferring plant resistance to Al toxicity.