MicroRNAs in metal stress: specific roles or secondary responses?

Abstract

In plants, microRNAs (miRNAs) control various biological processes by negatively regulating the expression of complementary target genes, either (1) post-transcriptionally by cleavage or translational inhibition of target mRNA, or (2) transcriptionally by methylation of target DNA. Besides their role in developmental processes, miRNAs are main players in stress responses, including metal stress responses. Exposure of plants to excess metal concentrations disturbs the cellular redox balance and enhances ROS accumulation, eventually leading to oxidative damage or signaling. Plants modify their gene expression by the activity of miRNAs in response to metal toxicity to regulate (1) complexation of excess metals, (2) defense against oxidative stress and (3) signal transduction for controlling various biological responses. This review focuses on the biogenesis, working mechanisms and functioning of miRNAs in plants. In a final part, our current knowledge on the regulatory roles of miRNAs in plant metal stress responses is highlighted, and whether stress-regulated miRNAs have specific roles or are secondary consequences is discussed.

Figure 1

Model of the biogenesis and working mechanisms of miRNAs. MIR genes are transcribed by Pol II to generate a double stranded stem-loop pri-miRNA that can be further processed in short miRNAs (s-miRNAs) or long miRNAs (l-miRNAs). To produce s-miRNAs, the pri-miRNA is sliced by DCL1 and processed by HYL1 and SE. The s-miRNA/miRNA* duplex is methylated by HEN1 and exported to the cytoplasm by HST, where it associates with AGO1 into the RISC-complex. The miRNA binds with near perfect complementarity to its target mRNA to regulate it post-transcriptionally by cleavage or translational inhibition. On the other hand, to produce l-miRNAs, the pri-miRNA is sliced by DCL3 and methylated by HEN1. However, there is also the possibility that Pol IV and RDR are involved in the biogenesis of l-miRNAs. The mature l-miRNA associates with AGO4, guiding de novo DNA methylation probably catalyzed by DRM2. Abbreviations: miRNA gene (MIR), polymerase (Pol), RNA-dependent RNA polymerase (RDR), dicer-like (DCL), hyponastic leaves 1 (HYL1), serrate (SE), hua enhancer 1 (HEN1), hasty (HST), argonaute (AGO), domains rearranged methyltransferase 2 (DRM2).

Figure 2

Summary of metal-regulated miRNAs in plants and their target families. MicroRNAs are categorized based on the metal they respond to. The effects of excess essential (Cu, Mn, Zn and Fe; blue boxes) and non-essential (Cd, Al, Hg and As; purple boxes) metals on the expression of miRNAs is shown (green: up-regulation; red: down-regulation; orange: up-regulation or down-regulation through contrasting results in various studies.). These metal-regulated miRNAs are obtained from several plant species, like Arabidopsis thaliana (At), Phaseolus vulgaris (Pv), Medicago truncatula (Mt), Brassica napus (Bn), Oryza sativa (Os) and Nicotiana tabacum (Nt) [,,–82].