Melatonin Increases the Chilling Tolerance of Chloroplast in Cucumber Seedlings by Regulating Photosynthetic Electron Flux and the Ascorbate-Glutathione Cycle

Abstract

The aim of the study was to monitor the effects of exogenous melatonin on cucumber (Cucumis sativus L.) chloroplasts and explore the mechanisms through which it mitigates chilling stress. Under chilling stress, chloroplast structure was seriously damaged as a result of over-accumulation of reactive oxygen species (ROS), as evidenced by the high levels of superoxide anion (O2−) and hydrogen peroxide (H2O2). However, pretreatment with 200 μM melatonin effectively mitigated this by suppressing the levels of ROS in chloroplasts. On the one hand, melatonin enhanced the scavenging ability of ROS by stimulating the ascorbate–glutathione (AsA–GSH) cycle in chloroplasts. The application of melatonin led to high levels of AsA and GSH, and increased the activity of total superoxide dismutase (SOD, EC 1.15.1.1), ascorbate peroxidase (APX, EC 1.11.1.11), monodehydroascorbate reductase (MDHAR, EC 1.6.5.4) dehydroascorbate reductase (DHAR, EC 1.5.5.1), glutathione reductase (GR, EC1.6.4.2) in the AsA–GSH cycle. On the other hand, melatonin lessened the production of ROS in chloroplasts by balancing the distribution of photosynthetic electron flux. Melatonin helped maintain a high level of electron flux in the PCR cycle [Je(PCR)] and in the PCO cycle [Je(PCO)], and suppressed the O2-dependent alternative electron flux Ja(O2-dependent) which is one important ROS source. Results indicate that melatonin increased the chilling tolerance of chloroplast in cucumber seedlings by accelerating the AsA–GSH cycle to enhance ROS scavenging ability and by balancing the distribution of photosynthetic electron flux so as to suppress ROS production.

Melatonin induction and its role in high light stress tolerance in Arabidopsis thaliana

“…Conversely, melatonin synthesis in plants has been shown to be significantly induced in response to many abiotic and biotic stresses, including heavy metals, drought, cold, and pathogens, among others . These stressors commonly induce ROS and/or NO production in plants.…”

“…In accordance with our speculations as mentioned above, several recent publications have revealed that plants produce melatonin at concentrations far lower than nanogram per gram weight in healthy tissues during their normal growth and development. 16,60,61 Conversely, melatonin synthesis in plants has been shown to be significantly induced in response to many abiotic and biotic stresses, including heavy metals, 20,25 drought, 17 cold, 10 and pathogens, 28,59 among others. 30 These stressors commonly induce ROS and/or NO production in plants.…”

“…Recently, melatonin has drawn attention as a potent antioxidant in both animals and plants. [6][7][8] An increasing number of reports have shown that exogenous melatonin treatment ameliorates damage resulting from various biotic and abiotic stresses by increasing levels of glutathione [9][10][11][12] and other enzymatic antioxidants [13][14][15][16] in a number of plant species. Moreover, melatonin exhibits direct ROS-scavenging activity, conferring stress tolerance in response to drought, 17 salt, 18,19 aluminum, 20 cadmium, 21,22 and ROS-generating herbicides 23,24 by reducing ROS levels.…”

Uniconazole confers chilling stress tolerance in soybean (Glycine max L.) by modulating photosynthesis, photoinhibition, and activating oxygen metabolism system

“…Chilling stress is one of the destructive abiotic stresses that restricts photosynthesis and eventually limits agricultural production and quality of tropical and subtropical plants (Allen and Ort 2001, Ikeda et al 2009, Liu et al 2012, Nahar et al 2015. Reduction in electron transport (Zhao et al 2016) and photosynthetic efficiency, and changes in protein structure and enzyme activities are some of the most common and primary chilling injury symptoms within plants. Inhibition of the carbon reduction cycle (Allen and Ort 2001), PSII activity (Strauss et al 2006), and photosynthesis (Savitch et al 1997, Allen andOrt 2001) under chilling stress increases generation of reactive oxygen species (ROS) (Gill andTuteja 2010, Zhao et al 2016).…”

“…Various strategies are being employed to alleviate the adverse effects of chilling stress in plants. Foliage spray of plant growth regulators (PGRs) is an effective, facile, and practical technique to enhance tolerance of plants, which has been used widely in recent years (Zhang et al 2007, Manafi et al 2015, Zhao et al 2016.…”