Gasotransmitter H2S accelerates seed germination via activating AOX mediated cyanide-resistant respiration pathway

Plant Physiol Biochem. 2022 Nov 1:190:193-202. doi: 10.1016/j.plaphy.2022.09.003. Epub 2022 Sep 9.

Abstract

Hydrogen sulfide (H2S) has been witnessed as a crucial gasotransmitter involving in various physiological processes in plants. H2S signaling has been reported to involve in regulating seed germination, but the underlying mechanism remains poorly understood. Here, we found that endogenous H2S production was activated in germinating Arabidopsis seeds, correlating with upregulated both the transcription and the activity of L-cysteine desulfhydrase (EC 4.4.1.28, LCD and DES1) responsible for H2S production. Moreover, seed germination could be significantly accelerated by exogenous NaHS (the H2S donor) fumigation and over-expressing DES1, while H2S-generation defective (lcd/des1) seeds exhibited decreased germination speed. We also confirmed that the alternative oxidase (AOX), a cyanide-insensitive terminal oxidase, can be stimulated by imbibition. Furthermore, exogenous H2S fumigation and over-expressing DES1 could significantly reinforced imbibition induced increase of both the AOX1A expression and AOX protein abundance, while this increase could be obviously weakened in lcd/des1. Additionally, exogenous H2S fumigation mediated post-translational modification to keep AOX in its reduced and active state, which might involve H2S induced improvement of the reduced GSH content and the cell reducing power. The promotive effect of H2S on germination was clearly impaired by inducing aox1a mutation, indicating that AOX acts downstream of H2S signaling to accelerate seed germination. Consequently, H2S signaling was activated during germination then acted as a trigger to induce AOX mediated cyanide-resistant respiration to accelerate seed germination. Our study correlates H2S signaling to cyanide-resistant respiration, providing evidence for more extensive studies of H2S signaling.

Keywords: Alternative oxidase; Hydrogen sulfide; Post-translational activation; Seed germination; Transcriptional regulation.

MeSH terms

  • Arabidopsis Proteins* / genetics
  • Arabidopsis Proteins* / metabolism
  • Arabidopsis* / genetics
  • Cyanides / metabolism
  • Cyanides / pharmacology
  • Cystathionine gamma-Lyase / genetics
  • Cystathionine gamma-Lyase / metabolism
  • Cystathionine gamma-Lyase / pharmacology
  • Gasotransmitters* / metabolism
  • Germination
  • Hydrogen Sulfide* / metabolism
  • Hydrogen Sulfide* / pharmacology
  • Mitochondrial Proteins
  • Oxidoreductases / metabolism
  • Plant Proteins
  • Respiration
  • Seeds / metabolism

Substances

  • Arabidopsis Proteins
  • Cyanides
  • Gasotransmitters
  • Mitochondrial Proteins
  • Plant Proteins
  • Oxidoreductases
  • alternative oxidase
  • Cystathionine gamma-Lyase
  • DES1 protein, Arabidopsis
  • Hydrogen Sulfide