Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants

Abstract

Small, non-coding RNAs are a distinct class of regulatory RNAs in plants and animals that control a variety of biological processes. In plants, several classes of small RNAs with specific sizes and dedicated functions have evolved through a series of pathways. The major classes of small RNAs include microRNAs (miRNAs) and small interfering RNAs (siRNAs), which differ in their biogenesis. miRNAs control the expression of cognate target genes by binding to reverse complementary sequences, resulting in cleavage or translational inhibition of the target RNAs. siRNAs have a similar structure, function, and biogenesis as miRNAs but are derived from long double-stranded RNAs and can often direct DNA methylation at target sequences. Besides their roles in growth and development and maintenance of genome integrity, small RNAs are also important components in plant stress responses. One way in which plants respond to environmental stress is by modifying their gene expression through the activity of small RNAs. Thus, understanding how small RNAs regulate gene expression will enable researchers to explore the role of small RNAs in biotic and abiotic stress responses. This review focuses on the regulatory roles of plant small RNAs in the adaptive response to stresses. This article is part of a Special Issue entitled: Plant gene regulation in response to abiotic stress.

Fig. 1

Biogenesis and function of miRNAs and siRNAs. (A) MIR genes are initially transcribed by Pol II into a single-stranded RNA that folds back to form a hairpin structure (also called pri-miRNA) thought to be stabilized by the RNA-binding protein DAWDLE (DDL) [138]. Splicing and further processing in nuclear dicing bodies involves the interactive functions of HYL1 and SE and of the cap-binding proteins (CBP) CBP20 and CBP80 [139, 140]. Pri-miRNAs and pre-miRNAs are generally thought to be processed from the free-end opposite to the loop by DCL1 to yield one or several phased miRNA/miRNA* duplexes. These are then methylated by HEN1 and transported to the cytoplasm by HST1. The miRNA guide strand is selected, incorporated, and stabilized in dedicated AGO1 protein. miRNA-guided AGO1-containing RISC directs mRNA cleavage or translation inhibition of the target transcript. miRNA-guided AGO1 functions are promoted by SQUINT (SQN) and HSP90 [22, 141]. (B) Various sources of dsRNA, its processing into siRNAs by one of four DCLs proteins assisted by dsRNA-binding proteins, HEN1-mediated siRNA stabilization, and selected strands of siRNA duplexes guide AGO-containing RISC to target RNAs for endonucleolytic cleavage and for translation repression, or these siRNAs can then guide AGO4 or AGO6 to function in RNA-directed DNA Methylation (RdDM) pathway involving Pol IV and Pol V. Cytosine methylation at these specific sites involves different effectors like the de novo methyltransferase DOMAINS REARRANGED METHYLTRANSFERASE 2 (DRM2); DEFECTIVE IN RNADIRECTED DNA METHYLATION 1 (DRD1), a member of the SWI2-SNF2 chromatin remodeling protein family; and DEFECTIVE IN MERISTEM SILENCING 3 (DMS3), a structural maintenance of chromosomes (SMC) protein.

Fig. 2

Summary of stress-regulated small RNAs and their target families. Small RNAs are categorized based on the stress that they respond to. Grey box: abiotic stress, dark grey: biotic stress, green boxes: up-regulated small RNA, light green boxes: slightly up-regulated small RNA, and red boxes: down-regulated small RNA. At (Arabidopsis thaliana), Bd (Brachypodium distachyon), Bn (Brassica napus), Br (Brassica rapa), Gm (Glycine max), Mt (Medicago truncatula), Nt (Nicotiana tabacum), Os (Oryza sativa), Pt (Populus trichocarpa), Pta (Pinus taeda), Ptr (Populus tremula), Pp (Physcomitrella patens), Pv (Phaseolus vulgaris), Ta (Triticum aestivum), Zm (Zea mays). See the text for references.

Fig. 3

Regulatory network of stress-responsive miRNAs in Arabidopsis. A network is proposed that describes the molecular mechanisms underlying the response of Arabidopsis plants to different biotic and abiotic stresses. The network is based on the changes in expression profiles of miRNA and subsequent target transcripts in plants under stress. Green boxes: up-regulated RNAs; red boxes: down-regulated RNAs.