MicroRNA Member TaMIR5062 in T. Aestivum Involves Plant Drought and Salt Acclimation via Regulating Physiological Processes Associated with Water Retention and ROS Homeostasis

microRNA members negatively regulate target genes via posttranscriptional cleavage or translation repression mechanisms, impacting on plant growth, development, and stress response. In this study, we characterized TaMIR5062, a miRNA member in T. aestivum, in mediating drought and salt responses. TaMIR5062 interacts with six target genes, including two encoding calmodulins, three coding for 4-oxalocrotonate tautomerases, and one for pumilio-family RNA binding domain protein. The TaMIR5062 transcripts were gradually upregulated in plants upon 27-h drought and salt treatments, whose induced expression under stress treatments was restored following the normal recovery condition. Tobacco (N. tabacum) lines transformed with TaMIR5062 modified growth traits under drought and salt treatments; the lines overexpressing miRNA (i.e., Sen 1 and Sen 2) improved growth traits (i.e., biomass, leaf area, and root length) whereas those with knockdown (Anti 1) alleviated growth features compared with wild type. These results suggested the critical role of TaMIR5062 in improving plant drought and salt tolerance. In line with growth traits in stress-challenged lines, improved leaf water retention (i.e., promoted stomata closing, water losing rate, and osmolytes) and ROS-associated parameters (higher SOD, CAT, and POD activities, etc.) were shown in Sen 1 and Sen 2 under stress conditions. Antioxidant enzyme (AE) genes NtMnSOD1, NtCAT, and NtPOD9 encoding SOD, CAT, and POD, respectively, enhanced transcription in Sen 1 and downregulated expression in Anti 1 challenged with drought and salt stress. These results suggested the improved ROS homeostasis mediated by TaMIR5062 associates modified expression of distinct AE genes. Quantities of genes functional into categories “biological process”, “cellular component”, and “molecular function” contribute to TaMIR5062-mediated osmotic stress adaptation by regulating distinct biological pathways (i.e., protein folding) and metabolisms (i.e., photosynthesis and isoprenoid biosynthesis), which impact on plant osmotic-regulation, ROS homeostasis, and stress defensiveness underlying miRNA regulation. TaMIR5062 is a valuable target for molecular breeding of drought-tolerant crop cultivars.