Exogenous hydrogen sulfide modulates metabolic responses of sugar and phenolic acid in naked oat leaves under saline-alkali stress

In order to clarify the regulatory effect of hydrogen sulfide signaling on the plant metabolome under saline-alkali stress and to reveal its mechanism of enhancing plant saline-alkali tolerance, a pot experiment was conducted with naked oat (Avena nude) as the material. Four treatments were applied to potted naked oat plants in a 2 × 2 factorial combination, including 0 or 3.00 g·kg⁻¹ saline-alkali (molar ratio of NaCl∶Na₂SO₄∶Na₂CO₃∶NaHCO₃ at 12∶8∶1∶9) added to the potting soil and spraying with distilled water or 50 µmol·L⁻¹ sodium hydrosulfide (a hydrogen sulfide donor) on leaves at the heading stage. The effects of exogenous hydrogen sulfide on glycolytic metabolite levels, redox balance, and phenolic acid content in leaves and on the yield traits of naked oats under the four treatments were investigated using ultra-performance liquid chromatography-tandem mass spectrometry technology combined with orthogonal partial least squares discriminant analysis. Under non-saline-alkali conditions, sodium hydrosulfide application did not have a significant effect on the ratios of (reduced glutathione)/(oxidized glutathione) and (reduced coenzyme Ⅱ)/(oxidized coenzyme Ⅱ), adenosine triphosphate content in leaves, and yield traits of naked oats; however, the levels of citrate, succinate, and 6-phosphogluconolactone were significantly upregulated and those of glucose-6-phosphate, pyruvate, lactate, α-ketoglutaric acid, glutamate, asparagine, erythrose-4-phosphate, and sedoheptulose-7-phosphate were significantly downregulated in the leaves. Saline-alkali stress significantly reduced the levels of glucose, glucose-6-phosphate, fructose-6-phosphate, fructose-1,6-diphosphate, 3-phosphate glyceraldehydes, 3-phosphoglyceric acid, pyruvate, lactate, α-ketoglutaric acid, glutamate, glutamine, asparagine, erythrose-4-phosphate, sedoheptulose-7-phosphate, ribose-5-phosphate, reduced glutathione, oxidized glutathione, reduced coenzyme Ⅱ, and oxidized coenzyme Ⅱ in the leaves of naked oats; whereas the ratio of reduced glutathione to oxidized glutathione was increased significantly. Spraying with sodium hydrosulfide significantly increased the levels of glucose, fructose-6-phosphate, 3-phosphoglyceric acid, lactate, α-ketoglutaric acid, fumarate, malate, glutamine, 6-phosphogluconolactone, and sedoheptulose-7-phosphate in the leaves of naked oats under saline-alkali stress, and significantly decreased the asparagine content. The levels of trans-cinnamic acid and syringaldehyde in the leaves of naked oats under non-saline-alkali conditions were significantly decreased by spraying with sodium hydrosulfide. Saline-alkali stress significantly reduced the content of trans-cinnamic acid in the leaves of naked oats, and markedly increased the levels of benzoic acid, p-hydroxycinnamic acid, and trans-ferulic acid. Spraying with sodium hydrosulfide significantly increased the levels of 4-hydroxybenzoic acid and vanillin in the leaves of naked oats under saline-alkali stress, and remarkably decreased the levels of salicylic acid and 4-hydroxy-3,5-dimethoxycinnamic acid.There was no significant increase in spike number, spike boll number, thousand-grain weight, and biological yield of naked oats under saline-alkali stress as a result of spraying with sodium hydrosulfide; however, sodium hydrosulfide significantly alleviated the decrease in spike grain number and grain yield induced by saline-alkali stress. These results indicate that exogenous hydrogen sulfide participates in the regulation of sugar catabolism and phenolic acid levels in naked oats, which can enhance the saline-alkali tolerance of naked oats. The increasing effect of exogenous hydrogen sulfide on organic acid levels in the sugar decomposition pathway and the unique regulatory effect on phenolic acids may play an important role in enhancing the saline-alkali tolerance of naked oats.