Integrated Analysis of the Transcriptome and Metabolome Revealed the Molecular Mechanisms Underlying the Enhanced Salt Tolerance of Rice Due to the Application of Exogenous Melatonin

Abstract

High salinity is one of the major abiotic stresses limiting rice production. Melatonin has been implicated in the salt tolerance of rice. However, the molecular basis of melatonin-mediated salt tolerance in rice remains unclear. In the present study, we performed an integrated transcriptome and metabolome profiling of rice seedlings treated with salt, melatonin, or salt + melatonin. The application of exogenous melatonin increased the salt tolerance of rice plants by decreasing the sodium content to maintain Na+/K+ homeostasis, alleviating membrane lipid oxidation, and enhancing chlorophyll contention. A comparative transcriptome analysis revealed that complex molecular pathways contribute to melatonin-mediated salt tolerance. More specifically, the AP2/EREBP–HB–WRKY transcriptional cascade and phytohormone (e.g., auxin and abscisic acid) signaling pathways were activated by an exogenous melatonin treatment. On the basis of metabolome profiles, 64 metabolites, such as amino acids, organic acids, nucleotides, and secondary metabolites, were identified with increased abundances only in plants treated with salt + melatonin. Several of these metabolites including endogenous melatonin and its intermediates (5-hydroxy-L-tryptophan, N1-acetyl-N2-formyl-5-methoxykynuramine), gallic acid, diosmetin, and cyanidin 3-O-galactoside had antioxidant functions, suggesting melatonin activates multiple antioxidant pathways to alleviate the detrimental effects of salt stress. Combined transcriptome and metabolome analyses revealed a few gene–metabolite networks related to various pathways, including linoleic acid metabolism and amino acid metabolism that are important for melatonin-mediated salt tolerance. The data presented herein may be useful for further elucidating the multiple regulatory roles of melatonin in plant responses to abiotic stresses.