Plant Noncoding RNAs: Hidden Players in Development and Stress Responses

Abstract

A large and significant portion of eukaryotic transcriptomes consists of noncoding RNAs (ncRNAs) that have minimal or no protein-coding capacity but are functional. Diverse ncRNAs, including both small RNAs and long ncRNAs (lncRNAs), play essential regulatory roles in almost all biological processes by modulating gene expression at the transcriptional and posttranscriptional levels. In this review, we summarize the current knowledge of plant small RNAs and lncRNAs, with a focus on their biogenesis, modes of action, local and systemic movement, and functions at the nexus of plant development and environmental responses. The complex connections among small RNAs, lncRNAs, and small peptides in plants are also discussed, along with the challenges of identifying and investigating new classes of ncRNAs.

Keywords: circRNA; lncRNA; microRNA; plant development; siRNA; stress response.

Figure 1

Biogenesis and modes of action of plant small RNAs. (a) A MIR gene is transcribed into a pri-miRNA, which is sequentially processed first into a pre-miRNA and then into a miRNA/miRNA* duplex. The duplex is methylated by HEN1, and the miRNA strand is loaded into AGO1 in the nucleus. The miRNA-AGO1 complex is transported to the cytoplasm and regulates target gene expression through transcript cleavage and/or translation repression. (b) Pol IV generates single-stranded siRNA precursors, which are converted into dsRNAs and processed into 24-nt siRNA duplexes.Methylated siRNAs are loaded into AGO4 in the cytoplasm and are transported to the nucleus, followed by the recruitment of these siRNA-AGO4 complexes to Pol V transcripts. The subsequent recruitment of DRM2 catalyzes DNA methylation at RdDM target loci. (c) TAS or PHAS loci are transcribed into single-stranded RNAs that are targeted by an miRNA-AGO1/7 complex. The 5′ or 3′ cleavage fragment is protected by SGS3 and converted into dsRNA by RDR6. DCL proteins process these dsRNAs into 21- or 24-nt phasiRNAs. The 21-nt tasiRNAs, which are phasiRNAs from TAS loci, are primarily loaded into AGO1 and guide transcript cleavage of their targets. Abbreviations: AGO, ARGONAUTE; AMP1, ALTERED MERISTEM PROGRAM 1; CBC, CAP-BINDING COMPLEX; DCL, DICER-LIKE; DDL, DAWDLE; DRM2, DOMAINS REARRANGED METHYLASE 2; dsRNA, double-stranded RNA; HEN1, HUA ENHANCER 1; HST, HASTY; HYL1, HYPONASTIC LEAVES 1; Me, methylated; phasiRNA, phased siRNA; Pol, RNA polymerase; pre-miRNA, precursor miRNA; pri-miRNA, primary miRNA; RdDM, RNA-directed DNA methylation; RDR2/6, RNA-DEPENDENT RNA POLYMERASE 2/6; SE, SERRATE; SGS3, SUPPRESSOR OF GENE SILENCING 3; siRNA, small interfering RNA; tasiRNA, trans-acting siRNA; TRN1, TRANSPORTIN 1.

Figure 2

Functions of miRNAs in plant development and stress responses and an overview of the current understanding of miRNA-mediated regulation during development (inner circle) and responses to biotic and abiotic stresses (outer circle) in Arabidopsis and rice. Red font indicates miRNA-target modules that act in rice, but not in Arabidopsis.

Figure 3

Representative models for the roles of plant long noncoding RNAs (lncRNAs). lncRNAs can serve as scaffolds, molecular mimics and sponges, and small interfering RNA precursors. They can also be translated into small peptides to regulate target genes in cis or in trans during plant development. The expression of most reported plant lncRNAs is induced by diverse environmental conditions. COLDAIR, COOLAIR, MAS, and LAIR are lncRNAs regulating mRNA transcription in cis. PMS1T is a lncRNA acting as a phasiRNA precursor. IPS1 regulates PHO2 by acting as the endogenous target mimic of miR399 and affects phosphate homeostasis together with another lncRNA, NAT_pho1;2. Pri-miR171b is a peptide-encoding lncRNA. PROMPTs and ASCO-lncRNA are protein-binding lncRNAs that suppress the function of target proteins.