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Chen, M.; , .; Hu, Y.; Zhao, L. Non-Coding RNAs in Plants. Encyclopedia. Available online: https://encyclopedia.pub/entry/21755 (accessed on 28 July 2024).
Chen M,  , Hu Y, Zhao L. Non-Coding RNAs in Plants. Encyclopedia. Available at: https://encyclopedia.pub/entry/21755. Accessed July 28, 2024.
Chen, Ming, , Yueming Hu, Liang Zhao. "Non-Coding RNAs in Plants" Encyclopedia, https://encyclopedia.pub/entry/21755 (accessed July 28, 2024).
Chen, M., , ., Hu, Y., & Zhao, L. (2022, April 14). Non-Coding RNAs in Plants. In Encyclopedia. https://encyclopedia.pub/entry/21755
Chen, Ming, et al. "Non-Coding RNAs in Plants." Encyclopedia. Web. 14 April, 2022.
Non-Coding RNAs in Plants
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This entry is adapted from the peer-reviewed paper 10.3390/ijms23073695

Plant transcriptomes encompass a large number of functional non-coding RNAs (ncRNAs), only some of which have protein-coding capacity. Since their initial discovery, ncRNAs have been classified into two broad categories based on their biogenesis and mechanisms of action, housekeeping ncRNAs and regulatory ncRNAs. With advances in RNA sequencing technology and computational methods, bioinformatics resources continue to emerge and update rapidly, including workflow for in silico ncRNA analysis, up-to-date platforms, databases, and tools dedicated to ncRNA identification and functional annotation.

ncRNA plant ncRNA resource ncRNA function ncRNA interaction

1. Introduction

In the last few years, a number of non-coding RNAs (ncRNAs) have been described in plants involved in several processes, ranging from RNA maturation, splicing, regulation of transcription, post-transcriptional RNA modifications, and nucleosome remodeling. Therefore, it is unquestionable that ncRNAs play a significant role in gene regulatory network [1][2][3][4]. With extensive transcriptome analysis, up to 90% of the eukaryotic genome is transcribed into RNA, of which only 1–2% corresponds to protein-coding mRNA [5][6]. Although the remaining transcripts lack minimal protein-coding capacity and poorly conserved sequences [2][5][7], the emergence of ncRNAs as novel ribose regulators of gene expression sheds light on the so-called “dark matter” of the genome.
Current studies have revealed that ncRNAs can be transcribed from DNA sequences in protein-coding genes, intergenic or intronic regions [8]. In terms of their regulatory roles, ncRNAs could be divided into two major categories in plants (Figure 1). Among them, housekeeping ncRNAs are necessary for fundamental biological processes of life, so the content is relatively constant. Regulatory ncRNAs vary in size, shape, and accumulation patterns, so their expression is temporal and spatially specific [9]. Notably, any ncRNAs classification system is defined as an intelligent construct that is unlikely to perfectly reflect nature [10]. To date, many ncRNAs have not been described in plants, such as PIWI-interacting RNA (piRNA), an animal-specific small silencing RNA [11][12], enhancer RNAs (eRNAs), which play critical role in transcriptional activation in mammalian cells and are transcribed from enhancers [13][14][15], and Y RNAs, which are necessary for DNA replication in humans [16][17].
Figure 1. ncRNAs category in plants. From top to bottom, there are primary classification, secondary classification, abbreviations, secondary structures, size, and functions of ncRNAs. Since some ncRNAs contain multiple types, one is selected and annotated with text in the lower right corner of the secondary structure. The sizes of ncRNAs are approximate. Diverse functions include gene expression regulation, translation inhibition, plant immunity, stress response, etc. Abbreviations: tRNA, transfer RNA; rRNA, ribosomal RNA; snRNA, small nuclear RNA; snoRNA, small nucleolar RNA; miRNA, micro RNA; siRNA, small interfering RNA; tsRNA, tRNA-derived small RNA; circRNA, circular RNA; lncRNA, long non-coding RNA; tiRNA, stress-induced tRNA or tRNA halves; nt, nucleotides.
So far, the biogenesis of some regulatory ncRNAs has been clearly described [18][19][20]; however, siRNA and tsRNA are poorly defined in plants. As further studies have shown, ncRNAs participate in the maintenance of homeostasis in plants by ncRNA-associated interaction with other biomolecules and microorganisms, which is of great significance to growth, development, differentiation, and reproduction of plants.
With the advancement of high-throughput RNA-seq technologies, the diversity of ncRNAs world has been unveiled. To date, numerous studies have applied RNA-seq technology to discover known and novel classes of ncRNAs in diverse tissues and developmental stages [21]. These precious data have been mined and stored in public databases.

2. Biogenesis and Functions of ncRNAs in Plants

Currently, massive endogenous ncRNAs with various regulatory potentials have been discovered in various plant species [22][23]. Based on their average size, regulatory ncRNAs could be further categorized into small RNAs (18–30 nt), medium-sized ncRNAs (31–200 nt), and lncRNAs (>200 nt). In addition, it can be classified into linear or circular according to its morphology (Figure 1). In general, 200 nt is regarded as the dividing line in the regulatory ncRNAs world, but this size consideration is arbitrary because circRNAs, eRNAs, and promoter-associated transcripts (PATs) have displayed variable lengths [8]. Recently, regulatory small RNAs (sRNAs), namely, miRNA and siRNA, are considered to have tiny sizes but play important roles in response to stress or environmental changes by regulating the expression of target genes [24][25][26][27]. Likewise, lncRNAs were contemplated as transcriptional noise but later gained importance as one of the wide-ranging and heterogeneous groups of ncRNAs [28]. Notably, unlike other linear regulatory ncRNAs, circRNAs are a novel class of ncRNAs that lack free 5′ and 3′ terminus, which have been extensively explored in the past few years [29]. Besides, many small ncRNAs derived from tRNAs, called tsRNAs, have also been identified in plants with a broad size range of 15–42 nt [30][31][32]. Here, researchers classified tsRNAs as regulatory ncRNA according to their diverse functions (Figure 1). In general, the functions of some regulatory ncRNAs are similar, while a few are distinct, nevertheless overlapping in silencing pathways [33]. Next, researchers will introduce their biogenesis and functions in plants in detail.

2.1. miRNA

miRNA biogenesis is a multistep process involving transcription, processing, modification, and assembly of the RNA-induced silencing complex (RISC) (Figure 2A) [34][35][36]. First, primary miRNAs (pri-miRNAs) are transcribed by RNA POLYMERASE II (Pol II) containing hairpin RNA secondary structures. Then, an RNase III family DICER-LIKE (DCL) enzyme, usually DCL1 [37], assisted by HYPONASTIC LEAVES 1 (HYL1) and SERRATE (SE), cleaves from the base of the pri-miRNA hairpin to yield a precursor-miRNA (pre-miRNA) hairpin and cleaves again to release a miRNA/miRNA* duplex [38]. Next, the 3′-most nucleotides of the initial miRNA/miRNA* duplex are then 2′-O-methylated by the nuclear HUA ENHANCER 1 (HEN1) protein for stabilizing miRNA [39]. Finally, most mature miRNA strands are incorporated into ARGONAUTE 1 (AGO1) in the nucleus (unlike in animals, where it occurs in the cytoplasm [40]), with the removal of the miRNA* strand and the transport of the miRNA-AGO1 complex to the cytoplasm, where miRNAs induce post-transcriptional gene silencing by transcript cleavage and translation repression [24][35][41][42].
Figure 2. Regulator ncRNAs biogenesis landscape and functions in plants. The inside of the circle represents the nucleus, and the outside represents cytoplasm. All ncRNAs types are marked in purple. The background of each color represents biogenesis and functions of (A) miRNA; (B) siRNA; (C) tsRNA; (D) circRNA; (E) lncRNA, respectively.
As post-transcriptional gene regulators, miRNAs are up- or down-regulated for improving plant productivity and stress tolerance in numerous species [43][44]. Therefore, studying the expression patterns of miRNAs can help researchers better understand the regulatory networks of stress response and environmental adaptation. In general, miRNAs have several features in regulatory pathways. (1) Evolutionarily conserved RNAs tend to have conserved targets in related plant species. For example, miR159 targets MYB genes and is down-regulated in salt-stress responses among Arabidopsis [45], tobacco [46], and kidney bean [47]. miR172 targets AP2 genes for regulating floral development in Arabidopsis, rice, soybean, barley, and maize [27]. A list of conserved miRNAs suggests a common regulatory mechanism across different species. (2) A single miRNA can participate in a variety of stress responses and developmental processes. For instance, cold-inducible miR393 targets TIR1/AFB genes and is up-regulated for enhancing cold tolerance [48]. miR393 is also induced by PAMP flagellin (flg22) to down-regulate the levels of TIR1/AFB genes for antibacterial defense [49]. Besides, miR393 is also involved in regulating arbuscule formation [50], inhibiting root elongation, and promoting lateral root initiation [51]. (3) Multiple miRNAs can participate in one biological process. For example, in rice, miR156, miR396, and miR397 cooperate in the regulation of grain size. miR156, miR393, and miR444 participate in tillering together [27]. (4) The expression patterns of miRNAs rely on the specific condition. As mentioned above, miRNAs are up- or down-regulated according to specific stress or specific tissue. Another example can also be supported. miR1425 will influence the number of fertile pollen grains by regulating a pentatricopeptide repeat (PPR)-containing protein under cold stress [52].

2.2. siRNA

According to the mode of action, siRNA can be simply divided into three secondary categories, namely trans-acting siRNAs (ta-siRNA), heterochromatic siRNAs (hc-siRNA), and natural antisense siRNAs (nat-siRNAs). However, in fact, ta-siRNAs belong to the so-called “secondary siRNAs” category, including ta-siRNA and phased siRNAs. Here, since many of the known ta-siRNAs are also phased [10], researchers use ta-siRNA instead of “secondary siRNAs” for discussion. Generally, they both play a role in transcriptional gene silencing by complementary target mRNAs or directing DNA and histone methylation through RNA-directed DNA methylation (RdDM) process [53][54].
ta-siRNAs are generated from TAS genes (Figure 2B) [24][55]. Firstly, TAS genes are transcribed into single-stranded RNAs by RNA Pol II, and then they loose the cap and mostly also the poly-A end upon miRNA-AGO1 complex guided cleavage. Secondly, the 5′ or 3′ cleavage fragments are protected by SUPPRESSOR OF GENE SILENCING 3 (SGS3) and converted to double-stranded RNA (dsRNA) by RNA-dependent RNA polymerases 6 (RDR6) [56]. Finally, they are methylated and processed into 21–24 nt ta-siRNAs by HEN1 and various DCL activities. The 21–22 nt size class are loaded onto AGO1 or AGO7 to induce post-transcriptional gene silencing of complementary target mRNAs in the cytoplasm, while some ta-siRNAs are incorporated into AGO4/6 to guide RNA Pol V-mediated de novo DNA methylation of TAS genes [54]. In Arabidopsis, miR173 targets TAS1 and TAS2 genes to generate ta-siRNAs [55][57]. The TAS1 ta-siRNAs target the heat stress transcription factor genes, HEAT-INDUCED TAS1 TARGET 1 (HTT1) and HTT2, to regulate plant thermotolerance [58].
nat-siRNAs can be divided into two categories, cis-NAT-siRNAs and trans-NAT-siRNAs. However, only cis-NAT-siRNAs have been described in plants. trans-NAT-siRNAs remain only a hypothetical possibility. Therefore, in this entry, cis-NAT-siRNAs are collectively referred to as nat-siRNAs. Previously, nat-siRNAs were thought to be generated by the hybridization of separately transcribed complementary RNAs. However, to date, many of the nat-siRNAs investigated depend on RDR for their accumulation [10][59][60][61][62]. This RDR dependency suggests that the precursor dsRNA did not derive from the hybridization of two separately transcribed, complementary mRNAs. Thus, the biogenesis of nat-siRNAs is not well defined and appears to be very complex with some important unanswered questions. Based on available data, Zhang et al. speculated that there are at least five possible mechanisms to generate nat-siRNAs [63]. However, it is clear that nat-siRNAs can be induced by salt [59], pathogen [63], and control sperm function during double fertilization in Arabidopsis [61].
The biogenesis of hc-siRNA begins with the transcription of RNA Pol IV from the intergenic or repetitive genomic regions to generate single-stranded siRNA precursors [64][65][66], which are converted into dsRNA and processed into 24 nt siRNA duplexes. Methylated hc-siRNAs are loaded into AGO4 in the cytoplasm and are transported to the nucleus [67], followed by the recruitment of these hc-siRNA-AGO4 complexes to RNA Pol V transcripts. The subsequent recruitment of DOMAINS REARRANGED METHYLASE 2 (DRM2) catalyzes DNA methylation at RdDM target loci [53][67].

2.3. tsRNA

With a broad size range of 15–42 nt, tsRNAs are a new category of regulatory ncRNAs, which are classified into five categories according to the cleavage sites, namely tRF-1s, tRF-2s, tRF-3s, tRF-5s, and tiRNA (Figure 2C). However, the study in plants has just started, and many questions remain to be answered. For example, the biogenesis pathway of tsRNAs in plants is still unclear, and the physiological function of certain tsRNA in plants is currently very limited [68]. In this entry, researchers propose a hypothesis of tsRNAs biogenesis in plants based on previous studies. First, RNA poly III transcribes tRNA gene as precursor tRNA (pre-tRNA) [69], which includes a 5′ leader, a mature tRNA backbone, a 3′ U trailer, and sometimes an intron [70]. Then, the 5′ leader, 3′ U trailer, and intronic sequences are cleaved by RNase P, RNase Z, and tRNA-splicing endonucleases (TSEN) to produce mature tRNA and tRF-1s (tRF-1s could be derived from 3′-end of pre-tRNA) [71][72][73]. The mature tRNA (73–90 nt) forms a secondary cloverleaf structure with a D-loop (left), a T-loop (right), anticodon loop (bottom), a variable loop, and an acceptor stem (Figure 2C). Finally, the mature tRNAs could be cleavaged by Arabidopsis S-like Ribonuclease 1 (RNS1) and/or DCL1 to form tRF-2s, tRF-3s, tRF-5s, and tiRNA (Figure 2C) [30][31]. In mammals, tsRNAs incorporate into silencing AGO and trigger RNA interference [74]. Likewise, AGO-associated tsRNAs have been predicted in Arabidopsis and rice [30][75]. An in vitro assay has shown that certain tsRNAs regulate gene expression by translation inhibition, and tsRNA-AGO1 complex tends to target transposable element transcripts and probably maintains genome stability [31][76][77].

2.4. circRNA

CircRNAs were first discovered in plant viruses by Sanger’s group in 1976. Studies have shown that circRNAs are circular, single-stranded, and covalently closed RNA biomolecules [78]. The composition of circRNAs can be divided into three categories (Figure 2D). (1) Exonic circRNAs are formed by lariat-driven circularization and intron pairing-driven circularization [79]. (2) Intronic circRNAs are the source of introns generated by the partial degradation of introns after the formation of the lasso structure. (3) Exonic-intronic circRNAs, which are composed of exons and introns, are cyclized during splicing. In 2013, Jeck et al., proposed that exon skipping and intron pairing reduced the distance between splicing sites and promoted the reverse splicing of pre-mRNA [80]. This leads to the deletion of the 3′ and 5′ ends of circRNAs [81]. Several distinct functional mechanisms for animal circRNAs have been identified, suggesting that plant circRNAs may exhibit similar conserved functions. These include miRNA decoys [82], transcriptional modulation [83], translation of circRNAs into small peptides [84]. Besides, circRNAs can play an important role in plant development and stress responses. For example, Vv-circATS1 responds to cold stress by regulating the expression of stimulus-responsive genes in grape [85]. Under dehydration-stressed conditions, many differentially expressed circRNAs have been detected in wheat [86], pear [87], maize, and Arabidopsis [88]. These studies suggest that circRNAs have post-transcriptional roles. However, the mechanism of this remains to be elucidated.

2.5. lncRNA

The biogenesis of lncRNAs can be divided into five categories according to the transcribed site by Pol II: (1) sense lncRNAs are transcribed on the same strand as exons; (2) antisense lncRNAs are transcribed on the opposite strand of exons; (3) intronic lncRNAs are transcribed on introns; (4) intergenic lncRNAs are located between two distinct genes; (5) enhancer lncRNAs emerge from an enhancer region of protein-coding genes (Figure 2E) [89]. They can control target regulation by multiple ways, including chromatin remodeling [90][91][92], transcriptional repression, RNA splicing and transcriptional enhancer [93][94]. In addition, lncRNAs may encode small peptides (Figure 2E), which are required for various cellular processes [95]. Notably, numerous plant lncRNAs are regulated by abiotic stresses. For example, many differentially expressed lncRNAs have been identified in Arabidopsis under drought, cold, salinity, heat, and abscisic acid stresses [96]. Besides, biotic stress-responsive lncRNAs have also been identified in wheat [97], Arabidopsis [98], and tomato [99].

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Subjects: Plant Sciences
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Ming Chen
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Yueming Hu
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Liang Zhao
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