The Crosstalk of Melatonin and Hydrogen Sulfide Determines Photosynthetic Performance by Regulation of Carbohydrate Metabolism in Wheat under Heat Stress

Abstract

Photosynthesis is a pivotal process that determines the synthesis of carbohydrates required for sustaining growth under normal or stress situation. Stress exposure reduces the photosynthetic potential owing to the excess synthesis of reactive oxygen species that disturb the proper functioning of photosynthetic apparatus. This decreased photosynthesis is associated with disturbances in carbohydrate metabolism resulting in reduced growth under stress. We evaluated the importance of melatonin in reducing heat stress-induced severity in wheat (Triticum aestivum L.) plants. The plants were subjected to 25 °C (optimum temperature) or 40 °C (heat stress) for 15 days at 6 h time duration and then developed the plants for 30 days. Heat stress led to oxidative stress with increased production of thiobarbituric acid reactive substances (TBARS) and hydrogen peroxide (H2O2) content and reduced accrual of total soluble sugars, starch and carbohydrate metabolism enzymes which were reflected in reduced photosynthesis. Application of melatonin not only reduced oxidative stress through lowering TBARS and H2O2 content,augmenting the activity of antioxidative enzymes but also increased the photosynthesis in plant and carbohydrate metabolism that was needed to provide energy and carbon skeleton to the developing plant under stress. However, the increase in these parameters with melatonin was mediated via hydrogen sulfide (H2S), as the inhibition of H2S by hypotaurine (HT; H2S scavenger) reversed the ameliorative effect of melatonin. This suggests a crosstalk of melatonin and H2S in protecting heat stress-induced photosynthetic inhibition via regulation of carbohydrate metabolism.

Melatonin and Carbohydrate Metabolism in Plant Cells

“…The result is an activation of the metabolic turnover such that it is adequate and conditioned to the physiological situation of the moment. In summary, melatonin has multiple regulation actions; for example, it influences photosynthesis, improving the efficiency of Rubisco and other Calvin cycle-related enzymes, Photosystem I and II, chlorophyll and carotenoid content and stomatal complex, with the result of a higher net photosynthesis, and, in specific carbohydrate metabolism, melatonin mobilizes some key pathways such as starch and sucrose biosynthesis, through SPS, SuS, and invertases upregulation, mainly (see Figure 3), increasing biosynthesis sugar rate to cope with stressful situations [99].…”

Melatonin Confers Plant Cadmium Tolerance: An Update

“…Synergistic effects of melatonin and H 2 S regulated K + /Na + homeostasis, and reduced excessive accumulation of ROS by enhancing the activity of antioxidant enzymes. Inhibition of H 2 S by HT reversed the melatonin-modulated heat tolerance by inhibiting photosynthesis, carbohydrate metabolism, and the activity of antioxidant enzymes in wheat [36]. Recent investigation has revealed that melatonin-induced pepper tolerance to iron deficiency and salt stress was dependent on H 2 S and NO [118].…”

“…Various pharmacological, enzyme activity, and gene expression investigations revealed the crosstalk of H 2 S-melatonin in response to salt and heat stress in tomato and cucumber [34][35][36]. Exogenous melatonin induced the H 2 S generation by activating the L-cysteine desulfhydrase (L-CDes) activity, which was encoded by LCD, DCD, and DES1 [31,35].…”

“…Moreover, H 2 S homeostasis and L-cysteine desulfhydrase activity were involved in melatonin-modulated salt stress tolerance in tomato and cucumber seedlings [31,34,35]. Crosstalk of melatonin and H 2 S in alleviating heat stress was also suggested in wheat [36]. However, the involvement of H 2 S action in melatonin-mediated abiotic stress tolerance is still largely unknown, especially in Cd stress.…”

Melatonin in Plant Defense against Abiotic Stress

“…Exogenous melatonin also induces the production of endogenous NO which antagonizes ethylene biosynthesis and, henceforth, delays senescence [194]. Melatonin, along with H 2 S, helps in mitigating high temperature stress by improving photosynthetic attributes and carbohydrate metabolism [64]. Besides reducing accumulation of indole-3-acetic acid, melatonin (20 µM) application in Oryza sativa grown under fluoride stress hinders fluoride uptake and alters the phytohormone homeostasis [72].…”