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Review
. 2017 Dec;216(4):1002-1017.
doi: 10.1111/nph.14834. Epub 2017 Oct 19.

The 'how' and 'where' of plant microRNAs

Yu Yu  1 , Tianran Jia  1 , Xuemei Chen  1   2
Affiliations
Review

The 'how' and 'where' of plant microRNAs

Yu Yu et al. New Phytol. 2017 Dec.

Abstract

Contents 1002 I. 1002 II. 1007 III. 1010 IV. 1013 1013 References 1013 SUMMARY: MicroRNAs (miRNAs) are small non-coding RNAs, of typically 20-24 nt, that regulate gene expression post-transcriptionally through sequence complementarity. Since the identification of the first miRNA, lin-4, in the nematode Caenorhabditis elegans in 1993, thousands of miRNAs have been discovered in animals and plants, and their regulatory roles in numerous biological processes have been uncovered. In plants, research efforts have established the major molecular framework of miRNA biogenesis and modes of action, and are beginning to elucidate the mechanisms of miRNA degradation. Studies have implicated restricted and surprising subcellular locations in which miRNA biogenesis or activity takes place. In this article, we summarize the current knowledge on how plant miRNAs are made and degraded, and how they repress target gene expression. We discuss not only the players involved in these processes, but also the subcellular sites in which these processes are known or implicated to take place. We hope to raise awareness that the cell biology of miRNAs holds the key to a full understanding of these enigmatic molecules.

Keywords: ARGONAUTE1; DICER-LIKE1; HYPONASTIC LEAVES 1; dicing body; endoplasmic reticulum (ER); membrane-bound polysome; microRNA; phased small interfering RNA.

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Figures

Fig. 1
Fig. 1
Illustrations of major steps in microRNA (miRNA) biogenesis. RNA polymerase II (Pol II)-mediated miRNA gene (MIR) transcription is regulated by multiple transcription factors (TFs). Pol II activity itself is also subjected to phospho-regulation at its C-terminal domain (CTD). miRNA precursors are processed at the dicing bodies by the dicing complex, which is mainly composed of DICER-LIKE 1 (DCL1), HYPONASTIC LEAVES 1 (HYL1) and SERRATE (SE). Many other protein factors contribute to miRNA precursor processing through phospho-regulation, RNA splicing and other unknown molecular mechanisms. It remains unclear whether the dicing complex interacts with HUA ENHANCER 1 (HEN1) (question mark) and contributes to miRNA/miRNA* duplex export and RNA-induced silencing complex (RISC) assembly. During RISC loading, one strand of the small RNA duplex is selected as the guide strand (red) and incorporated into ARGONAUTE 1 (AGO1) to form a functional RISC, whereas the other strand (the passenger strand) is removed and degraded. Proteins are color-coded according to their known molecular functions in phospho-regulation of Pol II (red), MIR transcription (pink), phospho-regulation of HYL1 (orange), splicing/RNA-binding(dark blue)and potentially splicing/RNA-binding (light blue), and RISC assembly (brown). The core dicing complex components are colored green and protein with unknown molecular functions is colored purple. m7G,7-methylguanylate cap at the 5′ end of primary miRNAs; CDKF;1, CYCLIN-DEPENDENT KINASE F;1; CDKDs, CYCLIN-DEPENDENT KINASE D; NOT2, NEGATIVE ON TATA LESS 2; CDC5, CELL DIVISION CYCLE 5; CPL, C-TERMINAL DOMAIN PHOSPHATASE-LIKE; RCF3, REGULATOR OF CBF GENE EXPRESSION 3; PP4, Protein Phosphatase 4 complex; MPK3, MITOGEN-ACTIVATED PROTEIN KINASE 3; SnRK2s,SNF1-related protein kinase subfamily 2; CBC, Cap Binding Complex; AtGRP7, GLYCINE-RICH RNA-BINDING PROTEIN 7; STA1, STABILIZED 1; PRL1, PROTEIN PLEIOTROPIC REGULATORY LOCUS 1; MAC, MOS4-associated Complex; MOS2, MODIFIER OF SNC1, 2; THO/TREX, suppressor of the Transcription defects of Hpr1 mutants by Overexpression/TRanscription-EXport complex; PINP1, PSR1-INTERACTING PROTEIN 1; DBR1, LARIAT DEBRANCHING ENZYME 1; DDL, DAWDLE; HST, HASTY; HSP90, HEAT SHOCK PROTEIN 90; EMA1, ENHANCED MIRNA ACTIVITY 1; TRN1, TRANSPORTIN 1.
Fig. 2
Fig. 2
Overview of microRNA (miRNA) modes of action in plants. Mature miRNAs are incorporated into ARGONAUTE proteins to direct post-transcriptional gene silencing (PTGS) via transcript cleavage and translation repression or trigger the biogenesis of secondary small interfering RNAs(siRNAs). ARGONAUTE 1 (AGO1) mediates miRNA target cleavage followed by degradation of the cleavage fragments. The cytoplasmic location of this event is unclear, but the uridylation and turnover of 5′ cleavage fragments occur on AGO1. Translation repression takes place on membrane-bound polysomes (MBPs), and requires endoplasmic reticulum (ER)-localized ALTERED MERISTEM PROGRAM 1 (AMP1). Components of Processing body (P-body) are also involved in this process, although the function of these factors and their connection to ER remain mysterious. ARGONAUTE 7 (AGO7) cleaves miR390 targets that are associated with MBPs, and forms siRNA bodies together with SUPPRESSOR OF GENE SILENCING 3 (SGS3) and RNA-DEPENDENT RNA POLYMERASE 6 (RDR6) that are adjacent to the cis-Golgi. Other TAS transcripts that generate phased secondary siRNAs (phasiRNAs) in response to AGO1-mediated cleavage also associate with MBPs. Events are classified with colored lines according to miRNA-mediated actions (dark lines) and subsequent processing (light purple lines) of their targets. DCL4 DICER-LIKE4; HESO1, HEN1 SUPPRESSOR 1; URT1, UTP:RNA URIDYLYLTRANSFERASE 1; XRN4, EXORIBONUCLEASE4; SUO, a GW-repeat protein; VCS, VARICOSE; DCP1, DECAPPING 1; DCP2, DECAPPING 2; RICE1, RISC-INTERACTING CLEARING 3′–5′ EXORIBONUCLEASE 1.
Fig. 3
Fig. 3
Mechanisms of plant microRNA (miRNA) turnover. miRNA degradation starts with the removal of the methyl group at the 3′ end by SMALL RNA DEGRADING NUCLEASE 1 (SDN1), which is followed by 3′ uridylation through HEN1 SUPPRESSOR 1 (HESO1) and/or UTP:RNA URIDYLYLTRANSFERASE 1 (URT1). The tailed miRNAs are subsequently degraded by an unknown exonuclease. SDN1 and nucleotidyl transferases (HESO1 and URT1) can act on both ARGONAUTE (AGO)-bound miRNAs and free miRNAs in the cytoplasm. Free miRNAs are also degraded by SDN1 directly. The degradation of AGO1 via autophagy may also contribute to miRNA turnover.
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