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Melatonin alleviates low-sulfur stress by promoting sulfur homeostasis in tomato plants.

ABSTRACT: Despite involvement of melatonin (MT) in plant growth and stress tolerance, its role in sulfur (S) acquisition and assimilation remains unclear. Here we report that low-S conditions cause serious growth inhibition by reducing chlorophyll content, photosynthesis and biomass accumulation. S deficiency evoked oxidative stress leading to the cell structural alterations and DNA damage. In contrast, MT supplementation to the S-deprived plants resulted in a significant diminution in reactive oxygen species (ROS) accumulation, thereby mitigating S deficiency-induced damages to cellular macromolecules and ultrastructures. Moreover, MT promoted S uptake and assimilation by regulating the expression of genes encoding enzymes involved in S transport and metabolism. MT also protected cells from ROS-induced damage by regulating 2-cysteine peroxiredoxin and biosynthesis of S-compounds. These results provide strong evidence that MT can enhance plant tolerance to low-S-induced stress by improving S uptake, metabolism and redox homeostasis, and thus advocating beneficial effects of MT on increasing the sulfur utilization efficiency.

SUBMITTER: Hasan MK

PROVIDER: S-EPMC6033901 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Melatonin alleviates low-sulfur stress by promoting sulfur homeostasis in tomato plants.

Hasan Md Kamrul MK Liu Chen-Xu CX Pan Yan-Ting YT Ahammed Golam Jalal GJ Qi Zhen-Yu ZY Zhou Jie J

Scientific reports 20180705 1

Despite involvement of melatonin (MT) in plant growth and stress tolerance, its role in sulfur (S) acquisition and assimilation remains unclear. Here we report that low-S conditions cause serious growth inhibition by reducing chlorophyll content, photosynthesis and biomass accumulation. S deficiency evoked oxidative stress leading to the cell structural alterations and DNA damage. In contrast, MT supplementation to the S-deprived plants resulted in a significant diminution in reactive oxygen spe ...[more]

PMID: 29976982

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Project description:Trehalose (Tre), which was an osmoprotective or stabilizing molecule, played a protective role against different abiotic stresses in plants and showed remarkable perspectives in salt stress. In this study, the potential role of Tre in improving the resistance to salt stress in tomato plants was investigated. Tomato plants (Micro Tom) were treated with Hoagland nutrient solution (CK), 10 mM Tre (T), 150 mM sodium chloride (NaCl, S), and 10 mM Tre+150 mM NaCl (S+T) for 5 days. Our results showed that foliar application of Tre alleviated the inhibition of tomato plant growth under salt stress. In addition, salt stress decreased the values of net photosynthetic rate (Pn, 85.99%), stomata conductance (gs, 57.3%), and transpiration rate (Tr, 47.97%), but increased that of intercellular carbon dioxide concentration (Ci, 26.25%). However, exogenous application of Tre significantly increased photosynthetic efficiency, increased the activity of Calvin cycle enzymes [ribulose diphosphate carboxylase/oxygenase (Rubisco), fructose-1,6-bisphosphate aldolase (FBA), fructose-1, 6-bisphosphatase (FBPase), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), and transketolase (TK)], up-regulated the expression of genes encoding enzymes, induced stomatal opening, and alleviated salt-induced damage to the chloroplast membrane and structure. In the saline environment, photosynthetic electron transport was restricted, resulting the J-I-P phase to decrease. At the same time, the absorption, capture, and transport energies per excited cross-section and per active reaction center decreased, and the dissipation energy increased. Conversely, Tre reversed these values and enhanced the photosystem response to salt stress by protecting the photosynthetic electron transport system. In addition, foliage application with Tre significantly increased the potassium to sodium transport selectivity ratio (S K-Na ) by 16.08%, and increased the levels of other ions to varying degrees. Principal component analysis (PCA) analysis showed that exogenous Tre could change the distribution of elements in different organs and affect the expressions of SlSOS1, SlNHX, SlHKT1.1, SlVHA, and SlHA-A at the transcriptional level under salt stress, thereby maintaining ion homeostasis. This study demonstrated that Tre was involved in the process of mitigating salt stress toxicity in tomato plants and provided specific insights into the effectiveness of Tre in mediating salt tolerance.

Project description:BackgroundMelatonin is a pleiotropic signaling molecule that plays multifarious roles in plants stress tolerance. The polyamine (PAs) metabolic pathway has been suggested to eliminate the effects of environmental stresses. However, the underlying mechanism of how melatonin and PAs function together under heat stress largely remains unknown. In this study, we investigated the potential role of melatonin in regulating PAs and nitric oxide (NO) biosynthesis, and counterbalancing oxidative damage induced by heat stress in tomato seedlings.ResultsHeat stress enhanced the overproduction of reactive oxygen species (ROS) and damaged inherent defense system, thus reduced plant growth. However, pretreatment with 100??M melatonin (7?days) followed by exposure to heat stress (24?h) effectively reduced the oxidative stress by controlling the overaccumulation of superoxide (O2•-) and hydrogen peroxide (H2O2), lowering the lipid peroxidation content (as inferred based on malondialdehyde content) and less membrane injury index (MII). This was associated with increased the enzymatic and non-enzymatic antioxidants activities by regulating their related gene expression and modulating the ascorbate-glutathione cycle. The presence of melatonin induced respiratory burst oxidase (RBOH), heat shock transcription factors A2 (HsfA2), heat shock protein 90 (HSP90), and delta 1-pyrroline-5-carboxylate synthetase (P5CS) gene expression, which helped detoxify excess ROS via the hydrogen peroxide-mediated signaling pathway. In addition, heat stress boosted the endogenous levels of putrescine, spermidine and spermine, and increased the PAs contents, indicating higher metabolic gene expression. Moreover, melatonin-pretreated seedlings had further increased PAs levels and upregulated transcript abundance, which coincided with suppression of catabolic-related genes expression. Under heat stress, exogenous melatonin increased endogenous NO content along with nitrate reductase- and NO synthase-related activities, and expression of their related genes were also elevated.ConclusionsMelatonin pretreatment positively increased the heat tolerance of tomato seedlings by improving their antioxidant defense mechanism, inducing ascorbate-glutathione cycle, and reprogramming the PAs metabolic and NO biosynthesis pathways. These attributes facilitated the scavenging of excess ROS and increased stability of the cellular membrane, which mitigated heat-induced oxidative stress.

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Dataset Information

Melatonin alleviates low-sulfur stress by promoting sulfur homeostasis in tomato plants.

Publications

Melatonin alleviates low-sulfur stress by promoting sulfur homeostasis in tomato plants.

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