The Regulatory Activities of Plant MicroRNAs: A More Dynamic Perspective

Abstract

Twenty years have elapsed since the discovery of a microRNA (miRNA) gene in Caenorhabditis elegans. Based on growing research progress, we are approaching the nature of this small RNA species, which seemed to be mysterious before. The regulatory activities of miRNAs have been extensively studied through target identification and physiological and phenotypic assays by using bioinformatic, genetic, and biochemical approaches. However, recent evidence points to the fact that the effective levels of miRNAs are determined by transcription, processing, miRNAinduced silencing complex loading, action, turnover use, and decay. Each process is affected by certain factors, such as genomic modifications, RNA editing, miRNA-induced silencing complex loading competition, target abundance and complementarity, and spatiotemporal effects, thus conferring a highly dynamic feature to miRNA activities. To maintain steady-state levels of the functional miRNAs, thus ensuring a normal physiological and biochemical status, plants employ several exquisite strategies, such as feedback regulation and a buffering system, to minimize the influence of external signal fluctuations. In this review, we raise the notion that a more dynamic picture of miRNA activities should be drawn to construct comprehensive miRNA-mediated networks in plants.MicroRNAs (miRNAs), approximately 21 nucleotides in length, were identified as a small RNA (sRNA) species with essential regulatory roles in various biological processes (Carrington and Ambros, 2003). The transcription of most miRNA genes is guided by RNA polymerase II Xie et al., 2005). Following transcription, the single-stranded RNAs with internal stem-loop structures are then recognized by Drosha and Dicer in animals (Kim et al., 2009a) or Dicer-Like1 (DCL1) in plants (Voinnet, 2009) for sequential cleavage, converting the primary microRNAs (pri-miRNAs) to the precursor microRNAs (pre-miRNAs) and finally to the miRNA/miRNA* duplexes. After dissociation from the duplexes, the miRNAs are incorporated into Argonaute (AGO)-associated micro-RNA-induced silencing complexes (miRISCs; preferentially AGO1-associated miRISCs). Although the sophisticated model of miRNA biogenesis is seemingly settled for each step, there exist many key nodes that influence the final activity of a miRNA gene. The transcription of miRNA genes is under the rigorous surveillance of many cis-and trans-factors, such as chromatin marks and specific transcription factors (TFs). The processing efficiency of the miRNA precursors is basically determined by their own sequences and structures and is regulated in a spatiotemporal manner (Davis and Hata, 2009;Cuperus et al., 2011;Zhu et al., 2011). Furthermore, the sorting of miRNAs into specific AGO complexes should not be oversimplified, since not all the miRNAs are uniformly loaded into AGO1-associated miRISCs. Additionally, loading competition between miRNAs and other sRNAs occurs in planta.In plants, miRNAs guide the miRISCs to target transcripts containing highly complementary recognition ...

Salt Stress Reveals a New Role for ARGONAUTE1 in miRNA Biogenesis at the Transcriptional and Posttranscriptional Levels

“…The final accumulation of miRNA molecules and consequently the final levels of their mRNA targets result from a combined effect of the regulation of MIR genes transcription as well as the processing of miRNA precursors (Kai and Pasquinelli, 2010;Barciszewska-Pacak et al, 2015). The final levels of mature miRNAs can also be regulated by miRNA degradation or stabilization (Meng et al, 2011). The 10-member Arabidopsis (Arabidopsis thaliana) family of ARGONAUTE proteins is involved in such miRNA stabilization (Kai and Pasquinelli, 2010).…”

“…This regulation of miRNA expression can be achieved at several levels. It also includes the control of the level of DCL1 and AGO1 mRNA by specific miRNAs (Meng et al, 2011) in a distinctive feedback mechanism. The final accumulation of miRNA molecules and consequently the final levels of their mRNA targets result from a combined effect of the regulation of MIR genes transcription as well as the processing of miRNA precursors (Kai and Pasquinelli, 2010;Barciszewska-Pacak et al, 2015).…”

The Role of Long Non-coding RNAs in Abiotic Stress Tolerance in Plants

“…A number of studies have identifi ed and established the role of other small ncRNAs such as miRNAs and siRNAs in mediating abiotic stress tolerance in plants through sequence-dependent gene silencing at transcriptional and post-transcriptional level (Voinnet 2009 ;Sunkar et al 2012 ;Meng et al 2013 ). In contrast to small ncRNAs, only a few lncRNAs have been identifi ed and functionally characterized further to implicate their involvement in abiotic stress response in plants (Ben Amor et al 2009 ;Contreras-Cubas et al 2012 ).…”

The use of high-throughput sequencing methods for plant microRNA research

“…However, recent studies revealed some important biological functions of miRNA*s in both plants and animals. 44,58,[111][112][113][114] Here, based on the results obtained from our sRNA-seq-based bioinformatics analysis, we proposed that certain miRNA*s or isomiR*s could act as anti-miRs to inhibit the cognate miRNAs from binding the target transcripts, thus reducing the activities of the miRNAs. It is based on the following evidences: (1) According to the biogenesis model of the plant miRNAs, after DCL1-mediated 2-step processing, miRNA and its miRNA*, forming as a short RNA duplex, were exported to the cytoplasm for loading into the AGO1 complex.…”