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

Plant Cell Environ. 2019 Aug;42(8):2340-2356. doi: 10.1111/pce.13555. Epub 2019 May 26.

Abstract

Hydrogen sulphide (H2 S) is emerging as an important signalling molecule involved in plant resistance to various stresses. However, the underlying mechanism of H2 S in aluminium (Al) resistance and the crosstalk between H2 S 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 H2 S generation and citrate exudation in soybean roots. Pretreatment with an H2 S 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 H2 S scavenger elicited the opposite effect. Furthermore, H2 S and NO mediated Al-induced GmMATE expression and plasma membrane (PM) H+ -ATPase activity and expression. Further investigation showed that NO induced H2 S production by regulating the key enzymes involved in biosynthesis and degradation of H2 S. These findings indicate that H2 S 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.

Keywords: GmMATE; aluminium resistance; citrate exudation; hydrogen sulphide; nitric oxide; plasma membrane H+-ATPase; soybean.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aluminum / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism
  • Carrier Proteins / metabolism*
  • Glycine max / growth & development
  • Glycine max / metabolism*
  • Hydrogen Sulfide / metabolism*
  • Nitric Oxide / metabolism*
  • Plant Proteins / metabolism*
  • Plant Roots / growth & development
  • Plant Roots / metabolism
  • Soil Pollutants / metabolism*
  • Stress, Physiological

Substances

  • Carrier Proteins
  • Plant Proteins
  • Soil Pollutants
  • citrate-binding transport protein
  • Nitric Oxide
  • Aluminum
  • Hydrogen Sulfide