Interaction between the signaling molecules hydrogen sulfide and hydrogen peroxide and their role in vacuolar H⁺‐ATPase regulation in cadmium‐stressed cucumber roots

Abstract

Vacuolar H -ATPase (V-ATPase; EC 3.6.3.14) is the main enzyme responsible for generating a proton gradient across the tonoplast. Under cadmium (Cd) stress conditions, V-ATPase activity is inhibited. In the present work, hydrogen sulfide (H S) and hydrogen peroxide (H O ) cross-talk was analyzed in cucumber (Cucumis sativus L.) seedlings exposed to Cd to explain the role of both signaling molecules in the control of V-ATPase. V-ATPase activity and gene expression as well as H S and H O content and endogenous production were determined in roots of plants treated with 100 μM CdCl and different inhibitors or scavengers. It was found that H S donor improved photosynthetic parameters in Cd-stressed cucumber seedlings. Cd-induced stimulation of H S level was correlated with the increased activities of the H S-generating desulfhydrases. Increased H O and lowered H S contents in roots were able to reduce V-ATPase activities similar to Cd. H O and H S-induced modulations in V-ATPase activities were not closely related to the transcript level of encoding genes, suggesting posttranslational modifications of enzyme protein. On the other hand, exogenous H O raised H S content in root tissues independently from the desulfhydrase activity. Although treatment of control plants with H S significantly stimulated NADPH oxidase activity and gene expression, H S did not affect H O accumulation in roots exposed to Cd. The results suggest the existence of two pathways of H S generation in Cd-stressed cucumber roots. One involves desulfhydrase activity, as was previously demonstrated in different plant species. The other, the desulfhydrase-independent pathway induced by H O /NADPH oxidase, may protect V-ATPase from inhibition by Cd.

The endogenous L-cysteine desulfhydrase and hydrogen sulfide participate in supplemented phosphorus-induced tolerance to salinity stress in maize (Zeamays) plants

“…However, application of HT or PAG reversed the increase in LDES activity and endogenous H 2 S, and eliminated an increase in chlorophyll content and Fv/Fm, suggesting that LDES activity and H 2 S might play vital roles in SP-enhanced chlorophyll content and Fv/Fm. It has been reported that exogenously applied H 2 S improved chlorophyll content in pepper plants subjected to zinc toxicity stress (Kaya et al, 2018), in cucumber stressed with cadmium (Kabała et al, 2018) and strawberry plants subjected to iron deficiency (Kaya and Ashraf, 2019). Salinity stress affects both water status (Gandonou et al, 2018) and nutrient uptake of plants (Rahneshan et al, 2018), as shown in our experiment.…”

Glutathione and hydrogen sulfide are required for sulfur‐mediated mitigation of Cr(VI) toxicity in tomato, pea and brinjal seedlings

“…In the Cr(VI) + S + BSO combination, endogenous H 2 S and cysteine contents and DES activity were not significantly affected while growth was suppressed more than Cr(VI) treatment alone (Table , Figs and ), whereas in Cr(VI) + S + BSO + GSH combination growth was much better than Cr(VI) treatment alone suggesting that H 2 S signaling preceded GSH biosynthesis and also essential for additional S‐mediated mitigation of Cr(VI) toxicity in tomato, pea and brinjal seedlings. Although H 2 S‐mediated mitigation of abiotic stress such as toxic metals in plants is now increasingly being known (Singh et al , Zhu et al , Kabała et al , Valivand et al ), its implication in essential element such as S‐mediated mitigation of Cr(VI) toxicity in plants was not known.…”

“…whereas in Cr(VI) + S + BSO + GSH combination growth was much better than Cr(VI) treatment alone suggesting that H 2 S signaling preceded GSH biosynthesis and also essential for additional S-mediated mitigation of Cr(VI) toxicity in tomato, pea and brinjal seedlings. Although H 2 S-mediated mitigation of abiotic stress such as toxic metals in plants is now increasingly being known (Singh et al 2015, Zhu et al 2018, Kabała et al 2019, Valivand et al 2019, its implication in essential element such as S-mediated mitigation of Cr(VI) toxicity in plants was not known. Toxic metals such as Cr(VI) has the capability of inducing generation of ROS which damage macromolecules (Kováčik et al 2013, Eleftheriou et al 2015, Singh et al 2015, Singh and Prasad 2019 and this tendency of Cr(VI) may indirectly be linked with sacrificed growth of studied vegetables (Table 1, Figs 5-10).…”

“…Besides this, in recent years, hydrogen sulfide (H 2 S), a colorless gaseous signaling molecule, has gained much attention because of its implication in regulating wide ranges of plant physiological processes (Hancock and Whiteman 2016, Corpas et al 2019, Kabała et al 2019. Reports of the metal toxicity alleviatory role of H 2 S under abiotic stress have increased (Singh et al 2015, Zhu et al 2018, Kabała et al 2019, Valivand et al 2019. However, implication of H 2 S signaling in regulating essential elements like S-mediated mitigation of Cr(VI) toxicity in plants, to our knowledge, is still not known.…”

Hydrogen Sulfide: From a Toxic Molecule to a Key Molecule of Cell Life

“…This observation was also described in white clover, where H 2 S acts as a downstream signal of H 2 O 2 and NO in response to dehydration [155]. A recent study showed a newly discovered crosstalk between H 2 S and H 2 O 2 in another abiotic stress response, in which H 2 S can act as a positive regulator of Vacuolar H + -ATPase, while H 2 O 2 acts as a negative regulator during cadmium stress in cucumber roots [156]. In mammalian cells, H 2 O 2 is a key signal in redox regulation, and as it occurs in plants, these regulatory pathways may also be influenced by H 2 S. H 2 O 2 is produced by NAPDH oxidases in the plasma membrane and is transported to the cytosol through protein channels named aquaporins (AQP3, AQP8, and AQP9).…”