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. 2023 Nov 17;10(12):uhad234.
doi: 10.1093/hr/uhad234. eCollection 2023 Dec.

LncRNAs exert indispensable roles in orchestrating the interaction among diverse noncoding RNAs and enrich the regulatory network of plant growth and its adaptive environmental stress response

Lingling Zhang  1 , Tao Lin  2 , Guoning Zhu  1 , Bin Wu  3 , Chunjiao Zhang  4 , Hongliang Zhu  1
Affiliations

LncRNAs exert indispensable roles in orchestrating the interaction among diverse noncoding RNAs and enrich the regulatory network of plant growth and its adaptive environmental stress response

Lingling Zhang et al. Hortic Res. .

Abstract

With the advent of advanced sequencing technologies, non-coding RNAs (ncRNAs) are increasingly pivotal and play highly regulated roles in the modulation of diverse aspects of plant growth and stress response. This includes a spectrum of ncRNA classes, ranging from small RNAs to long non-coding RNAs (lncRNAs). Notably, among these, lncRNAs emerge as significant and intricate components within the broader ncRNA regulatory networks. Here, we categorize ncRNAs based on their length and structure into small RNAs, medium-sized ncRNAs, lncRNAs, and circle RNAs. Furthermore, the review delves into the detailed biosynthesis and origin of these ncRNAs. Subsequently, we emphasize the diverse regulatory mechanisms employed by lncRNAs that are located at various gene regions of coding genes, embodying promoters, 5'UTRs, introns, exons, and 3'UTR regions. Furthermore, we elucidate these regulatory modes through one or two concrete examples. Besides, lncRNAs have emerged as novel central components that participate in phase separation processes. Moreover, we illustrate the coordinated regulatory mechanisms among lncRNAs, miRNAs, and siRNAs with a particular emphasis on the central role of lncRNAs in serving as sponges, precursors, spliceosome, stabilization, scaffolds, or interaction factors to bridge interactions with other ncRNAs. The review also sheds light on the intriguing possibility that some ncRNAs may encode functional micropeptides. Therefore, the review underscores the emergent roles of ncRNAs as potent regulatory factors that significantly enrich the regulatory network governing plant growth, development, and responses to environmental stimuli. There are yet-to-be-discovered roles of ncRNAs waiting for us to explore.

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Conflict of interest statement

All the authors have no conflict of competing interest to declare for this manuscript submission.

Figures

Figure 1
Figure 1
The classification of main ncRNAs in plants. A, the classification of small RNAs, the display from left to right represents hierarchical relationships, every solid box presents one type of small RNA. B, the classification of medium-sized ncRNAs. C, the classification of lncRNAs, the green line and arrow represent lncRNAs transcription direction while the black line and arrow represent coding genes. D, the diagrammatic sketch of circular RNAs. hpRNA, hairpin RNA; siRNA, small interfering RNA; miRNA, microRNA; NAT-siRNA, natural antisense transcript siRNA; phasi RNAs, phased small interfering RNAs; U6 snRNA, U6 small nuclear RNA; snoRNA, small nucleolar RNA; TSS, transcription start site; TTS, transcription termination site.
Figure 2
Figure 2
Source and production of miRNA, siRNA, and lncRNA. . A, the production diagram of miRNA, two solid lines separate the nucleus and cytoplasm. B, the production diagram of different lengths of siRNAs. C, the production source of lncRNAs, the red box represents the exon of coding genes, the green box represents the exon of lncRNAs, the triangle represents an insertion event, and the small grid represents a repeat event. (1) Frame disruptions of coding genes into ncRNAs; (2) Chromosome’ rearrangement; (3) Retrotransposition of non-coding genes; (4) Neighboring repeats within a ncRNAs; (5) Insertion of a transposable element. MIR, microRNA genes; SE, zinc finger protein SERRATE; TGH, G-patch domain tough; HYL1, HYPONASTIC LEAVES 1; DCL, RNase III family DICER-LIKE; AGO 1, ARGONAUTE 1; HEN1, methyltransferase HUA ENHANCER 1; HSP90, HEAT SHOCK PROTEIN90; TRN1, TRANSPORTIN 1; CRM1, CRM1/EXPORTIN1; SDN1, SMALL RNA DEGRADING NUCLEASE 1; HESO1, HEN1 SUPPRESSOR1. RDR, RNA-DEPENDENT RNA POLYMERASE 6; RDM1, DNA-binding protein; DRM2, DOMAINS REARRANGED METHYLTRANSFERASE 2.
Figure 3
Figure 3
The classic regulation mode of lncRNAs in plants. A, The location of lncRNAs relative to coding genes and some classic regulation modes. The thick arrows indicate different examples involved in various mechanisms, the orange box represents the promoter region, the sky blue box represents the exon region, the green box represents lncRNAs, and the light blue box represents coding genes. The classic regulation modes of lncRNAs from promoter to termination site of the coding genes including promoter-related lncRNA ELENA1 and APOLO, 5′ UTR-related lncRNA PUAR and Ptlinc-NAC72, intron-related lncRNA AG-incRNA4 and RIFLA, exon-related lncRNA nalncFL7, the 3′ UTR -related lncRNA SEAIRa, TE-lincRNAs ARTA and other lncRNA SABC1.B, The lncRNAs participating in phase separation. PR1, pathogen response gene; HID, HIDDEN TREASURE 1; MED19a, Mediator subunit 19a; PRC1, polycomb repressive complex 1; PRC2, polycomb repressive complex 2; RDD, ROS1, DML2, and DML3, demethylases decrease; PHYA, PHYTOCHROMES; PIF7, PHYTOCHROMES INTERACTING; AG, AGAMOUS; CLF, CURLY LEAF; SE, SERRATE protein; PUB25/26, plant U-box protein; RUB1, ubiquitin-like protein related to ubiquitin 1; RH11, RNA helicase; MPK3/6, MITOGEN-ACTIVATED PROTEIN KINASE 3/6; HAI1, HIGHLY ABA-INDUCED PP2C1; FL7, FORKED-LIKE7; BPL3, BPA1-LIKE PROTEIN3; FIB2, FIBRILLARIN 2; SABC1, acid biogenesis controller 1; NAC3, transcription factor; ICS1, isochorismate synthase 1; SA, salicylic acid; ABA, abscisic acid; SAD2, importin β-like protein; MYB7, transcription factor; ABI5, the bZIP transcription factor; PYR, pyrabactin resistance; PYL1, pyrabactin resistance 1-like.
Figure 4
Figure 4
The coordinated regulation among ncRNAs (miRNAs and siRNAs) and lncRNAs. The upper diagram shows lncRNAs as a blocking factor, a precursor, and a sponge for miRNAs. The lower diagram shows the production origin of siRNAs from lncRNAs CHH hypermethylation and dicer cleavage, or lncRNAs as a stabilization factor of the transcription complex, as scaffolds to bind the AGO4-siRNA complex to exert a regulation effect. TYLCV, tomato yellow leaf curl virus.
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