H₂ S improves salt-stress recovery via organic acid turn-over in apple seedlings

Signalling roles of hydrogen sulphide (H₂ S) in stress biology are widely reported but not sufficiently established to urge its use in agronomic practice. Our lack of quantitative understanding of the metabolic rewiring in H₂ S signalling makes it difficult to elucidate its functions in stress tolerance on the biochemical level. Here, Malus hupehensis Rehd. var. pingyiensis seedlings were first treated with salt stress for 2 weeks and then treated with four different concentrations of NaHS. Through vigorous investigations, including phenotypic analysis, ¹³ C transient labelling and targeted metabolic and transcriptomic analysis, for the first time in the seedlings of a woody fruit crop, we found out that H₂ S recycles fixed carbons through glycolysis and tricarboxylic acid cycle to inhibit the futile accumulation of carbohydrates, to maintain an efficient CO₂ assimilation, to keep a balanced starch metabolism, to produce sufficient H₂ O₂ , to maintain malate/γ-aminobutyric acid homeostasis via an H₂ O₂ -induced anion channel (aluminium-activated malate transporter) and eventually to improve salt-stress recovery. Our results systematically demonstrate the vital roles of central carbon metabolism in H₂ S signalling and clarify the mode of action of H₂ S in apple seedlings. We conclude that H₂ S signalling interacts with central carbon metabolism in a bottom-up manner to recover plant growth after salt stress.