TaMIR1139: a wheat miRNA responsive to Pi-starvation, acts a critical mediator in modulating plant tolerance to Pi deprivation.

KEY MESSAGE: Wheat miRNA member TaMIR1139 targets genes functional in various families and plays crucial roles in regulating plant Pi starvation tolerance. Through regulating target genes at posttranscriptional or translational level, plant miRNAs are involved in mediating diverse biological processes associated with growth, development, and responses to adverse stresses. In this study, we characterized the expression pattern and function of TaMIR1139, a miRNA member of wheat (T. aestivum) under Pi deprivation. TaMIR1139 precursor is also present in N. tabucum, suggesting the conserved nature of miR1139 across monocots and eudicots. TaMIR1139 targets seven genes within different families. The transcripts abundance of TaMIR1139 was induced upon Pi deprivation and the upregulated expression under Pi starvation was downregulated by the Pi recovery treatment, In contrast, the genes targeted by TaMIR1139 exhibited reduced transcripts upon Pi starvation and their downregulated expression was recovered by Pi-recovery condition, suggesting the regulation of them under TaMIR1139 through a cleavage mechanism. TaMIR1139 overexpression conferred the Pi-deprived plants improved phenotype, biomass, photosynthesis, and Pi acquisition. Transcriptome analysis identified numerous genes involving biological process, cellular components, and molecular function were differentially expressed in the TaMIR1139 overexpression lines, which suggests the TaMIR1139-mediated plant Pi starvation tolerance to be associated with the role of miRNA in extensively modulating the transcript profiling. A phosphate transporter (PT) gene NtPT showed significantly upregulated expression in TaMIR1139 overexpression lines; overexpression of it conferred plants improved Pi acquisition upon Pi starvation, suggesting its contribution to the TaMIR1139-mediated plant low-Pi stress resistance. Our investigation indicates that TaMIR1139 is critical in plant Pi starvation tolerance through transcriptionally regulating the target genes and modulating the Pi stress-defensiveness processes.