Plant Non-Coding RNAs: Origin, Biogenesis, Mode of Action and Their Roles in Abiotic Stress

Abstract

As sessile species, plants have to deal with the rapidly changing environment. In response to these environmental conditions, plants employ a plethora of response mechanisms that provide broad phenotypic plasticity to allow the fine-tuning of the external cues related reactions. Molecular biology has been transformed by the major breakthroughs in high-throughput transcriptome sequencing and expression analysis using next-generation sequencing (NGS) technologies. These innovations have provided substantial progress in the identification of genomic regions as well as underlying basis influencing transcriptional and post-transcriptional regulation of abiotic stress response. Non-coding RNAs (ncRNAs), particularly microRNAs (miRNAs), short interfering RNAs (siRNAs), and long non-coding RNAs (lncRNAs), have emerged as essential regulators of plants abiotic stress response. However, shared traits in the biogenesis of ncRNAs and the coordinated cross-talk among ncRNAs mechanisms contribute to the complexity of these molecules and might play an essential part in regulating stress responses. Herein, we highlight the current knowledge of plant microRNAs, siRNAs, and lncRNAs, focusing on their origin, biogenesis, modes of action, and fundamental roles in plant response to abiotic stresses.

Keywords: abiotic stress; biogenesis; long non-coding RNA; non-coding RNA; transcriptional.

Figure 1

Classification of non-coding RNAs (ncRNAs). Housekeeping ncRNAs include; tRNAs- transfer RNAs, snRNAs-small nuclear RNAs, rRNAs-ribosomal RNAs, snoRNAs-small nucleolar RNAs. The regulatory ncRNAs consist of miRNAs-microRNAs, siRNAs-short interfering RNAs, piRNAs-piwi-interacting RNAs, and lncRNAs-long non-coding RNAs.

Figure 2

Biogenesis of plant miRNAs. In the nucleus, MIR genes are processed to miRNA/miRNA* duplexes through the action of Pol II, DCL1, SE, HYL1, HEN1, and HASTY. In the cytoplasm, the duplex is incorporated with RISC-AGO complex to which guides it towards the target, resulting in suppression of the translation and cleavage of mRNAs.

Figure 3

Biogenesis of siRNAs. The double stranded RNA (dsRNAs) is transformed into siRNAs by DCL, HEN1, and DRB. The RISC-AGO complex then guides the selected strands of siRNA duplexes to post transcription gene silencing (PTGS) or transcription gene silencing (TGS).

Figure 4

The biogenesis of long-non-coding RNAs (lncRNAs) and their gene regulation mechanisms in plants. (i) The transcripts of lncRNA (red box) are classified on the basis of their genomic location and in relation to the nearest gene (blue box): (A) sense lncRNAs are transcribed on the same strand as an exon; (B) antisense lncRNAs are transcribed on the opposite strand of an exon; (C) intronic lncRNAs are transcribed on the intron; (D) intergenic lncRNAs are located between two distinct genes; (E) enhancer lncRNAs emerge from an enhancer region of protein-coding genes. (ii) The gene regulation pathways induced in plants by lncRNAs. LncRNAs regulate gene expression either by: (1) interacting with transcriptional activator leading to gene activation; (2) interacting with transcriptional repressor thereby suppressing transcription; (3) controlling RNA splicing by interacting with splicing factor or binding premRNA splicing junction; (4) recruiting chromatin remodeling complex such as PRC to regulate gene expression in the promoter region; (5) LncRNA mimics miRNAs by occupying their target sites on the mRNA.

Figure 5

The miRNAs-guided target gene regulations under drought stress in maize. miRNAs that are positively regulated by drought stress (black arrow and blue rectangle) target negative regulators (top gray rectangle) of stress tolerance for enhanced suppression (red blunt arrow) of target gene products. By contrast, miRNAs that are suppressed by drought stress (red blunt arrow and gold rectangle) likely target positive regulators (bottom gray rectangle) of stress tolerance resulting in the accumulation of gene products (orange rectangle) which regulate drought stress response. SPL, sporocyteless; ARF, auxin response factor; DCL1, dicer like protein; NAC1, no apical meristem; SCL, scarecrow-like 3; APS, ATP sulfurylase; UBC24/PHO2, ubiquitin-conjugating Enzyme E2/phosphate 2; NLA, nitrogen limitation adaptation; MYB, myeloblastosis; HD-ZIP III, homeodomain-leucine zipper 3; HAP2, heme activator protein 2; AP2, apetala 2; CSD, copper/zinc superoxide dismutase.

Figure 6

Differential expression of commonly expressed miRNAs in maize and Arabidopsis during the drought stress response. Expression of miR168, miR397, and miR188 is down-regulated in maize but up-regulated in Arabidopsis. A red blunt arrow indicates a decrease while the black arrow represents an increase in the expression of the corresponding miRNA.

Figure 7

Regulatory network of miRNAs in Arabidopsis under abiotic stress. The proposed network describes the molecular mechanisms underlying the response of Arabidopsis plants to various abiotic stresses. The network is solely based on alterations in miRNA expression patterns and subsequent target transcripts in stressed plants.