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

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.


Introduction
As is widely recognized, only approximately 1.8% of the eukaryotic genome transcript is conventionally believed to contain proteincoding information.Traditionally, a substantial portion of transcripts were viewed as seemingly non-functional and were often regarded as transcriptional 'garbage' within eukaryotic organisms [1].In the current era, propelled by the advancements in microarrays and high-throughput sequencing technology, there have been substantial portions of eukaryotic genomes transcribed.This transcription has brought forth an expanding spectrum of ncRNAs that play a pivotal part in orchestrating and regulating the intricate processes that underlie these vital aspects of plants, particularly in the context of plant growth, maturation, and their ability to adapt to external environmental stress.The emergence of ncRNAs substantially enriches the regulation network, where lncRNAs as prominent representatives have been reported extensively to exert pivotal and indispensable functions.
This review primarily focuses on plants to summarize our current understanding regarding the synergetic regulation of the ncRNAs.To begin with, we present a comprehensive classification of ncRNAs or own poor coding capacity RNAs based on their length, comprising small RNAs (18-30 nucleotides (nt)), mediumsized ncRNAs (31-200 nt), lncRNAs (>200 nt), and circle RNAs [2], and brief ly provide synthetic sources of these various classes of ncRNAs.According to the findings from published research, it had been established that ncRNAs originate from a variety of sources, including gene breakage, intergenic area, transposons impact, insert of the genome, repetitive sequences and pseudogenes, and others [3].Subsequently, the review delves into the coordination mechanism of ncRNAs and classic cases.Notably, the review also places a strong emphasis on the interaction relationship between small RNAs and lncRNAs.This interaction is of particular importance due to its capacity to induce potent regulation in the realms of plant development and environmental stress.Of course, other noteworthy regulatory mechanisms of lncRNAs are also illustrated.For instance, recent advancements in ribosome sequence have revealed the coding potential of lncRNAs for micropeptides, which is an intriguing facet.Finally, this review not only delineates 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.
the existing problems and challenges within the field but also provides forward-looking prospects and potential directions for further exploration.

Small RNAs
Here, the endogenous expressed small RNAs in plants originate from the cleavage action of the Dicer-like (DCL) protein and the binding of Argonaute protein [4].Small RNAs have been documented that many classifications at different levels originate from the procedure of helical RNA precursors initially, including single-stand RNA precursors displaying a self-complementary 'hairpin' structure and double-strand RNA precursor (dsRNA) featuring an intermolecular hybridization structure.Therefore, at the primary level of classification, single-stand RNA precursors yield a category known as hairpin RNAs (hpRNAs) while dsRNAs generate small interfering RNAs (siRNAs).In the secondary distinction level, hpRNAs are further segregated into microRNAs (miRNAs) and other hpRNAs.siRNAs are mainly categorized into three types of secondary siRNAs, denoted as heterochromatic siRNAs, secondary siRNAs, and natural antisense transcript siRNAs (NAT-siRNAs).Within the tertiary level of categorization, miRNAs are divided into two subcategories, named lineage-specific miRNAs in minority species and long miRNAs (23-24 nt) [5].Furthermore, secondary siRNAs are further subdivided into phased siRNAs or trans-acting siRNAs.NAT-siRNAs are divided into cis-NAT-siRNAs and trans-NAT-siRNAs.The primary focus of attention centers around miRNAs and siRNAs in current small RNA research [5] (Fig. 1A).miRNAs miRNAs, as one of the principal small RNAs, ranging from 20-to 24-nt length, driving from highly precise excision of functional products, which usually own a well-defined set of mRNA targets.21-nt miRNAs are prevalent in the majority of plant species.Besides, 22-nt miRNAs predominantly originate from foldback precursors that feature asymmetric bulges, only these 22-nt miRNAs possess the capability to initiate the emergence of RDR6dependent siRNAs (RNA-dependent RNA polymerase (RDR)) from target RNAs in Arabidopsis [6].23-nt miRNAs typically originate from DCL3 cleavage directly of the hairpin structure.Furthermore, the authors detected that 23-nt miR156/157, miR164, and miR390 accumulated in members of the Brassicaceae, Solanaceae, and Poaceae families, respectively [7].It is worth mentioning the existence of many 24-nt miRNAs within rice and Arabidopsis [8].Moreover, the authors also reported 24-nt miRNAs in vitro plantlets of ponkan, the distribution of unique 24-nt miRNAs of ponkan leaves accounted for approximately 20.54%, followed by 20-nt miRNAs (22.15%) [9].The biosynthesis process of miRNAs is a sophisticated and intricate regulatory process encompassing multiple pivotal stages, namely the transcription level, processing stage, modification step, and final assembly [10,11].In the transcription level, the microRNA genes (MIRs) are transcribed into stable pri-miRNAs with 5 7-methylguanosine cap and 3polyadenylated tail by DNA-dependent RNA POLYMERASE II (Pol II).In the processing stage, pri-miRNAs are first sliced into precursor miRNAs (pre-miRNAs) characterized by a stem-loop structure.Subsequently, pre-miRNAs are further processed into short miRNA/miRNA * duplex by an RNase III family DCL enzyme, which includes DCL1, or its homologous protein DCL2, DCL3, DCL4 [12].These enzymatic activities are facilitated with the assistance of HYPONASTIC LEAVES 1 (HYL1) and zinc finger protein SERRATE (SE) and G-patch domain tough (TGH) or other factors (regulatory factor: CBP20/80, STA1, SIC, DBR1, GRP7, et al.).As a modification step, the miRNA/miRNA * duplex is methylated by 2'O-methylation on 3 terminal ribosomes, which is catalyzed by the methyltransferase HUA ENHANCER 1 (HEN1) [13] and subsequently is degraded by 3 -5 exonuclease (sRNA degrading nuclease1,2,3) [14].In the final assembly, miRNAs are mainly assembled by AGO1 in the nucleus and then the miRNA * strand is exported to the cytoplasm to silence mRNA or inhibitof translation [15] (Fig. 2A).Furthermore, the intensity of miRNAmediated inhibition is determined by polymorphisms within the hairpin precursors and the degree of complementarity between miRNAs and their targets [5,16].Additionally, there exists another category of miRNAs referred as to lineage-specific miRNAs.These miRNAs are characterized by their transient presence in the evolution history, lower expression levels, limited functionality, poor conservation, relative instability, and a lack of specific targets [5].siRNAs siRNAs ranging in length from 21-to 25-nt, are double-stranded RNA molecules characterized by a specific chemical structure.The siRNAs can be detected in some homology-dependent RNA silencing events, often identified as the products of RNA degradation of both sense and antisense polarities [17].In plants, most siRNAs are heterochromatic siRNAs that originate from repeat sequences and transposable elements (TEs) and are primarily responsible for silencing gene expression at the epigenetic level by promoting DNA methylation state and histone methylation activity of genes [5].There are two different origins to generate siRNAs.One, referred to as RNA-directed DNA methylation (RdDM), contributes to forming 24-nt siRNAs.In this process, the chromatin remodeling factors CLASSY initially recruit Pol IV to bind to the RdDM loci site, which leads to generating singlestrand siRNA precursors [13].Subsequently, the precursors of siRNAs fold into double-stranded siRNA structures with the assistance of an RDR2.Finally, the immature double-stranded siRNA molecules are processed into mature siRNAs with the aid of DCL3.siRNAs typically bind to AGO4 protein to produce a significant effect mediated by Pol V. Parallel to this, Pol II contributes to an alternative biosynthesis pathway, named noncanonical RdDM.The pathway primarily produces 21-to 22-nt siRNAs, which are responsible for the initiation of DNA methylation [18] (Fig. 2B).

Medium-sized ncRNAs
Certain members of noncoding RNAs are non-polyadenylated ncRNAs lacking poly (A) tails with lengths ranging from 50-to 300nt, commonly referred to as im-ncRNAs.They have low expression levels that make them challenging to detect through experimental technology.Additionally, at the 5 end of ncRNAs, possessing one phosphate, three phosphates, or trimethylguanosine cap may inf luence the stability, processing, and regulation of im-ncRNAs [19].As illustrated in Fig. 1B, various types of im-ncRNAs are transcribed by Pol III, including tRNA, 5s rRNA, U6 snRNA, small nuclear RNA, 7SL/MRP (mitochondria recognition particle) RNA, NAT RNAs, and small nucleolar RNAs, which play roles in guiding ribosome modification [4].Furthermore, Pol III contributes to the translation process by generating tRNA adaptor molecules that facilitate the transformation of mRNA codon information into amino acids [20].Wang et al. revealed 838 im-ncRNAs and found an interesting phenomenon in which certain novel im-ncRNAs, derived from the 5'UTR of genes, consistently exhibited high expression levels [21].The application of deep-sequencing technology is expected to discover more im-ncRNAs.It is worth noting that forthcoming research endeavors are anticipated to provide insights into the upstream regulatory factors and mechanisms of these im-ncRNAs.

LncRNAs
LncRNAs are distinguishable from the small RNAs which own a determined base length and clear biological significance.However, lncRNAs typically arise through specific mechanisms and can be characterized using various criteria of their functionality as ncRNAs, their limited coding potential, and their significant nucleotide length (>200 nt) [22].Similar to mRNAs, some lncRNAs also exhibit an m7G cap at the 5 end and a poly-A tail at the 3 end.These lncRNAs are transcribed by specific polymerases, such as PolI and Pol III.PolI, for instance, is predominantly associated with the transcription of genes containing lncRNAs within ribonucleoprotein complexes.It is responsible for transcribing some tandemly repeated genes into long rRNA precursors, then processing and assembling to form ribosomal subunits [22].Furthermore, Pol III is primarily responsible for catalyzing relatively short (<500 nt) lncRNAs [22].In addition, Pol II also produces a range of lncRNAs and pays some contributions to the lncRNAs' production by ensuring the correct structure, accurate localization, and expression level [23].Moreover, two plant-specific RNA polymerases, both of Pol IV and Pol V are involved in the generation of lncRNAs which can identify and repress TEs within the genome [24].Based on the relative position between the lncRNAs and neighboring coding genes, lncRNAs can be categorized into five distinct classes, including promoter-associated lncRNAs (antisense ncRNAs mainly are upstream of coding gene), enhancer-associated lncRNAs (lncRNAs are associated with enhancer regions), gene body-associated lncRNAs (antisense and sense lncRNAs within the gene body of coding genes), and intervening associated lncRNAs (lncRNAs are positioned between two coding genes, lincRNAs) [22] (Fig. 1C).The origin of lncRNAs can be attributed in multiple ways.Firstly, lncRNAs may emerge through frame disruptions of coding genes, resulting in ncRNA sequences that retain some previous coding sequences.Secondly, nontranscribed genes or distanced sequence regions can give rise to multi-exon ncRNAs through chromosomal rearrangement.Thirdly, there is a retrotransposition function that makes some noncoding genes produce functional noncoding retrogene or nonfunction retropseudogene through duplication events.Fourthly, the presence of adjacent repeats of ncRNAs can lead to novel lncRNAs.Finally, the insert event of TEs gives rise to functional noncoding RNAs [25] (Fig. 2C).

Circular RNAs
In addition to line RNAs, researchers also have unveiled the presence of thousands of endogenous circular RNAs (circRNAs) that are widespread in plants.Unlike linear mRNAs, circular RNAs formed a covalent closed-loop structure by splicing the RNAs' head (5 upstream acceptor) and tail (3 downstream donor) and then combining them.The process, named back splicing, happens at post-transcriptional and co-transcriptional levels [26,27].The circRNAs are always considered an alternative form of pre-mRNA splicing [28] (Fig. 1D).The research indicated that circularization was more stable, enhancing their resistance to RNase R, and the half-life was more than 48 h in vitro when compared to linear RNAs [26].Additionally, circRNAs are further divided into exon-intron circRNA (eIciRNA), exonic circRNA, intronic circRNA, and tRNA introns (tricRNA) based on gene location [29].It has been acknowledged that plant circRNAs own the conservation characteristics.Researchers discovered that in Oryza sativa and Arabidopsis, the parent genes of over 700 exonic circRNAs exhibited as homologous [30].Current research suggested the R-loop of circRNAs might modulate alternative splicing by binding miR-NAs [31].In Arabidopsis, an exonic circRNA originating from the SPEALLATA3 (SEP3) could form a DNA-RNA duplex with its parent genes to promote the event of the nascent transcript into the exon 6-skipped SEP3.3 isoform, finally contributing to the development of f loral homeotic phenotypes [32].In maize and rice, the research identified 149 differentially expressed circRNAs that responded to various environmental stresses such as heat, cold, or drought [33].Furthermore, in tomatoes, overexpression of PSY1-circ1 (involved in carotenoid biosynthesis) resulted in the yellow pericarp phenotype and PDS-circ1 might regulate the expression of PDS mRNA to inf luence the color of plant organs [34].Moreover, some lncRNAs can adopt circular RNAs and may compete with the linear pre-mRNAs for the recognition of splicing protein complexes, or as circular lncRNAs to sponge miRNAs [35].

LncRNAs play multiple roles
Based on the relative location of lncRNAs to coding genes, lncR-NAs play multiple roles at multifaceted levels, encompassing the epigenetic, transcription, and post-transcription levels [22].According to the orientation of transcription, the description is structured to cover aspects from the promoter regions to the termination of coding genes.
To begin, the short promoter-related lncRNAs are typically generated within the promoter regions, which are caused by the early termination of gene transcription by Pol II [36].In contrast, lncR-NAs would either directly or indirectly regulate promoter activity.For example, in plant immunity, lncRNA ELENA1 possessed the capability to dissociate the FIB2/MED19a protein complex and released the FIB2 protein from its repressive inf luence on the PR1 promoter [37].Furthermore, lncRNAs not only regulate adjacent genes in transcription levels but also affect distal genes by bringing them into close spatial proximity, contributing to forming a three-dimensional genome organization in trans.As an example, a distant lncRNA, such as APOLO, was typically derived from a genomic locus located approximately 5 kb upstream of the gene PID.There was a chromosome loop formed between the APOLO and the PID promoter, mainly by recruiting epigenetic marks like histone H3 lysine 27 trimethylation (H3K27me3) and DNA methylation, which were instrumental in the regulation of auxin transport in Arabidopsis [38].Moreover, the lncRNA APOLO was also substantiated to interact with the transcription factor WRKY42 and then modulate the binding of WRKY42 to the promoter of ROOT HAIR DEFECTIVE 6 (RHD6), ultimately triggering root hair cell expansion in response to cold stress in Arabidopsis [39].Furthermore, lncRNA would establish an intragenic gene loop.For instance, the lncRNA COLDWRAP was transcribed from the locus between the promoter and first intron of FLOWERING LOCUS C (FLC) which played a pivotal regulation role in f lowering time during Arabidopsis vernalization [40].Furthermore, some lncRNAs originate from the promoters of TEs and can inf luence gene promoters by RdDM at the edges of TEs [41].Likewise, during the photomorphogenesis process under contributing red light exposure, another promoter-associated lncRNA HIDDEN TREA-SURE 1 (HID1) was reported as a composition of the large nuclear ribonucleoprotein complexes to repress the transcription level of PHYTOCHROMEINTERACTING FACTOR 3, consequently enhancing the photomorphogenesis process [42] (Fig. 3A).
Secondly, the 5 UTR refers to the genomic interval between TSS where Pol II initiates transcription and the AUG start codon of the associated mRNAs.An update reported that a lncRNA related to the 5 UTR regions, named PUAR (PHYTOCHROMES (PHYA) UTR antisense RNA), is involved in the plants' shade avoidance syndrome (SAS) phenomenon, which helps plants get more light by initiating a sequence of morphological and physiological changes.LncRNA PUAR was primarily induced by plant shade areas, then reduced the accumulation of PHYA, and finally enhanced shade-induced hypocotyl elongation.Furthermore, the researchers also discovered that PUAR would block a positive regulator, PHYTOCHROMES INTERACTING (PIF7), which was binding to the 5 UTR of PHYA [43].Under salt stress conditions, another 5 UTR-related lncRNA was capable of binding to a specific motif within 5 UTR not coming from the 5 UTR region.An example of this was Ptlinc-NAC72 upregulated ptNAC72.A/B by identifying a tandem element (GAAAAA) of the 5 UTR of two ptNAC72.A/B genes in Populus trichocarpa [44].Furthermore, in Arabidopsis, the DCL4 gene utilized lncRNAs to inf luence TSS selection and gene sequence.The mutant of missing lncRNA of DCL4 would reduce the DNA methylation and alter the selection of the gene TSS locations by Pol II [45].
Thirdly, some intron regions can produce lncRNAs, as an example, AG-incRNA4, one transcript originating from the second intron of AG (AGAMOUS), which encodes a MADS-box protein involved in stamen and carpel fates of Arabidopsis flowers.The AG-incRNA4 knockdown mutant reduced the recruitment ability of PRC and decreased the H3K27me3 level within the AG gene body to accumulate the AG mRNA level [46].Some intron-derived lncRNAs act as components of complexes to exert inf luence.For instance, RIFLA (RICE FLOWERING ASSOCIATED) was transcribed from the first intron of OsMADSD56 (MIKC-type MADS-box protein 56), and it was believed that RIFLA might interact with osiEZ1 (one gene related histone H3K27-specific methyltransferase) to form a complex and then reduced OsMADSD56 expression to regulate the f lowering of O. sativa L [47] (Fig. 3A).Furthermore, the exon-related lncRNAs had been found within the TFIIIA gene and participated in the synthesis process of Pol III GTF TFIIIA.A noncoding 5S rRNA structural mimic (P5SM), as the second isoform, mainly bound L5 ribosomal protein, hereby promoted the synthesis of Pol III.Additionally, P5SM was instrumental in maintaining the levels of L5 protein and 5S rRNA [48].Moreover, it had been reported that nalncFL7 was one transcript derived from the antisense strand of FORKED-LIKE7 (FL7, At4g060410), which overlapped with exon 2-7 of the FL7 locus in Arabidopsis.Research findings further revealed that the nalncFL7 transcript bound BPL3 (an RNA binding protein) and inhabited the transcript level of FL7, further regulated HIGHLY ABA-INDUCED PP2C1 (HA1)-mediated MPK3/6 dephosphorylation, and ultimately participated in the immunity reaction triggered by Phytophthora capsicum [49] (Fig. 3A).
Fourthly, some intragenic lncRNAs that are derived from the 3 end of coding genes would participate in the RNA process.As an example, an antisense intragenic lncRNA SEAIRa originated from the 3 end of the SERRATE (SE) gene and downregulated the expression level of SE to regulate serrated leaves of Arabidopsis.SEAIRa accomplished the process by recruiting plant U-box protein PUB25/26 and a ubiquitin-like protein related to ubiquitin 1(RUB1) for H2Aub, resulting in recruiting H3K27me3 marks, which accumulated at the first exon of SE [50].(Fig. 3A).
Furthermore, some lncRNAs originate from the sequence area of transcription terminators of coding genes due to a failure in terminating transcription, and many of these are antisense lncRNAs [51].For example, one cold-related lncRNA SVALKA was triggered from a neighboring downstream gene and participated in a cold tolerance event mediated by the C repeat/dehydration-responsive (CBF1) transcription factor.SVALKA had interacted with a cryptic lncRNA asCBF1 which came from the antisense strand of the overlapping CBF1.The cascade of SVALKA and asCBF1 modulated the cold acclimation process of the plants by affecting the expression level of CBF1 mRNA [52].The opinion on the relationship between transcription termination and lncRNA production is centered on the following aspects.Transcription termination itself likely regulates the activity of the antisense transcript promoters and controls lncRNA production [22].In addition, lncRNAs would regulate the initiation of antisense transcription by forming R-loops [53].What is more, the genomic regions located beyond the transcription terminator would affect the expression of the coding gene; as an example, lncRNA SUF in male identification of plants [54].
Lastly, in addition to the lncRNAs that are directly related to certain genes, there are also some lincRNAs or lncRNAs from other origins that play crucial roles in responding to environmental stimuli and regulating plant growth.For instance, lincRNA SABC1 acted to suppress a transcription factor NAC3 in cis and subsequently triggered the expression of the salicylic acid (SA) biosynthesis enzyme, named isochorismate synthase 1 (ICS1), leading to a dampened immunity response and promoting healthy plant growth [55].Furthermore, some lincRNAs exert effort in plant development and ripening.Zhu and their teams focused on the roles of lncRNAs in tomatoes which serve as typical respiratory climacteric model plants [56].They first identified 3679 lncR-NAs (approximately 85.1%) belonging to lincRNAs types related to tomato ripening.Moreover, in classical ripening mutants rin (RIPENING INHIBITOR), they also found 490 up-regulated lncRNAs and 187 down-regulated lncRNAs [56].The subsequent research revealed that 187 RIN-targeted lncRNAs had been identified as having a RIN binding site in their promoter regions.Particularly, one lncRNA among them, named lncRNA2155, had been shown to have a delaying effect on tomato fruit ripening in vivo and in vitro [57].Additionally, another paper cloned the full length of lncRNA1459, and in the loss-of-function mutant of lncRNA1459, ethylene production, and lycopene accumulation, two key factors in fruit ripening, were notably inhibited [58].Some lncRNAs come from TEs, named TE-lincRNAs.A TE-lincRNAs ARTA mainly bound to the carboxyl-terminal area of an import β-like protein known as SAD2, and then inhibited the entry of the transcription factor MYB7 into the nucleus to free the inhibition of MYB7 to ABI5 (the bZIP transcription factor).Moreover, the regulation process was induced by abscisic acid (ABA).Under ABA treatment, the regulation led to an accumulation of AR expression and then positively regulated the expression level of ABI5, thereby reducing drought tolerance in Arabidopsis [59] (Fig. 3A).During the early endosperm development of O. sativa, there was a parent-of-origin lncRNA MISSEN that played a role in hindering the function of the helicase family protein (HeFP).This interference affected the expression of the tubulin gene and resulted in the abnormal aggregation of the cytoskeleton.As a consequence, this disruption in the cytoskeletal organization led to obvious dents and protrusions on seeds [60].Furthermore, some lncRNAs exert a significant inf luence on alternative splicing (AS) events; for example, lncRNA ACoS-AS1 partic-ipated in the trans-splicing between SlPsy1 (regulation enzyme in carotenoids biosynthesis pathway) and ACoS-AS1, resulting in a yellow tomato fruits phenotype [61].Other research teams found that 72.55% of lncRNAs caused AS in different tomato tissues, including the root, leaf, and f lower.Particularly, during the initial f lowering time of tomato, which yielded a range of 16 995 AS events, among the various types of them, ranked first is alternative first exon (AFE), followed by a retained intron (RI) events [62].Furthermore, lncRNA ASCO contributed to the assembly of key splicing composition PREMRNA PROCESSING 8 (PRP8) and SmD1, which inf luenced the binding of PRP8 to a subset of its pre-mRNA targets in Arabidopsis [63].Researchers reported that the combination of factors of methyl jasmonate (MeJA) treatment and transcription factor NtMYC2 would also regulate the expression levels of several lncRNAs through qPCR detection and gene editing technology [64].

LncRNAs may participate in phase separation
Phase separation is a newly emerging phenomenon that introduced an additional regulatory mechanism in cells in response to environmental stimuli.In countless pieces of research, phase separation has been recognized as the basis or a contributing factor to the formation of biomolecular condensates [65].Correspondingly, in the cellular microenvironment, the biomolecular condensates typically represent membrane-less compartments comprised of non-stoichiometric assemblies of proteins or nucleic acids [66].The condensates mainly encompass two molecular complexes: one type is stress granules (SG) which consist of a dense core containing all pivotal components and a peripheral shell that serves a sequestration function.These condensates often develop major responses to environmental changes through a conserved transient mechanism.Another type of biomolecular condensate is referred to as the process body (P-body), which is independent of stress conditions [66].Nevertheless, it is worth noting that there is limited evidence regarding whether lncRNAs were SG-enriched RNA species due to the poor detection technology.However, lncRNAs were also core components of recruiters.For example, under oxidative stress, some lncRNAs had been detected in cells.Moreover, those lncRNAs accumulated in SGs tend to have lower cellular expression levels than those missing in SGs [67].It is well-established that lncRNAs exhibited tissue or cell-type specificity and low expression levels compared to other ncRNAs.Furthermore, there was evidence to suggest that the interaction between lncRNAs and P-bodies or SGs is relatively short-lived [68,69].Moreover, the lncRNAs in P-bodies or SGs are easy to overlook or not observed because of limited approaches.Hence, we look forward to more methods being developed.The related views had been reported in animal cells that lncRNAs were reported as elements of SGs.There are around 60% of lncRNAs transcripts localized to SGs during the DNA damage process [67] (Fig. 3B).

Coordinated regulation between lncRNA-miRNA
Usually, the formation of lncRNA-RNA duplexes is associated with post-transcriptional regulation, where lncRNAs interact with other RNA molecules to regulate the coding gene expression.Moreover, in plants, the form of lncRNAs are cis NATs, which mainly affect gene silencing or translational promotion [70].For example, approximately 70% of annotated mRNAs of Arabidopsis species were associated with detectable lncNATs [42].These lncR-NAs always play various roles in the regulatory network between lncRNAs and miRNAs, serve as a source of miRNAs, act as bait and sponge to sequester miRNAs, or interfere with the precise cleavage process of pri-RNA, and, in turn, inf luence the target mRNAs [71].For example, lncRNA NAT398b and NAT398c were in co-expression with MIR398b and MIR398c in Arabidopsis, respectively.Overexpression of lncRNA NAT398b and NAT398c negatively regulated the biosynthesis of miR398 by destabilizing the pri-miR398b/c, leading to the upregulation of miR398-targeted genes CSD1/2/3 and CCS.These target genes primarily participated in processes related to cell death, oxidative stress and heat stress, ultimately affecting the thermotolerance of Arabidopsis [72].In plants, lncRNAs also known as 'target mimics' (TMs), could function as competing endogenous RNAs (ceRNAs).These lncRNAs owned quite similar target binding sites of miRNAs (some miRNA recognition sequences) within incomplete base pairing.Moreover, these lncR-NAs impaired the activity of the miRNAs and blocked the miRNAs binding to their authentic target transcripts [73].A classic example of this competitive mechanism in plants was the noncoding gene IPS1 (INDUCED BY PHOSPHATE STARVATION1), which owned a conserved 23-nt-long motif with sequence complementarity with miR399.Thus, IPS1 would bind miR399 by forming a mismatched loop to the accumulation of the target mRNA PHO2, further resulting in lower inorganic phosphate (Pi) content and reduced Pi remobilization in the shoot, which was first reported in Arabidopsis [74].Furthermore, in a study by Hou et al, lncRNA39026 was identified as an endogenous target-mimicry for miR168a.The interaction enhances tomato resistance to Phytophthora infestans by inducing the expression of PR genes [75].In response to blue light stress and mannitol stress, the researchers revealed the existence of blue light-induced lncRNA BLIL1.lncRNA BLIL1 competed with miRNA167 and inf luenced the target mRNA ARF6/8.Hence, the authors put forward the BLIL1-miRNA167-ARF6/8 regulation network in the hypocotyl elongation in Arabidopsis [76].Additionally, in the context of the plant resistance process, silencing specific lncRNA23468 led to the accumulation of the expression level of miR482b and resulted in reduced levels of the target gene NBS-LRRs.NBS-LRRs gene mainly took part in resistance of phytophthora infestation in tomatoes [77].Several reports have presented that certain lncRNAs can serve as precursors for miR-NAs through intracellular cleavage activities.One study described a pair of lncRNAs derived from cotton subgenomes that could generate miRNA397.Furthermore, miRNA397 mainly repressed the expression level of LAC4 by guiding mRNA degradation.The process involved the regulatory process of lignin metabolism and the domestication of tetraploid cotton fibers [78].Furthermore, an additional research team discovered that miRNA397 down-regulated its target laccase-like gene transcripts in rice [79].Furthermore, the investigators presented compelling evidence that certain stress-related transcripts, named TapmlnRNA8, TapmlnRNA19, and TalnRNA5 owned stable hairpin structures and served as precursors for miRNAs during powdery mildew infection in wheat by mapping miRNA technology.Among these, two lncRNAs (TalnRNA5 and TapmlnRNA19) and TapmlnRNA8 emerged as the precursors of miR2004 and miR2066, respectively.Additionally, within the same context of publication, the authors also identified a lncRNA, denoted TahlnRNA27, which possessed a sequence from the Ta-miR2010 gene family and was notably up-regulated in 'TAM107' cultivar (a heat tolerant wheat cultivar) after heat treatment [80] (Fig. 4).

The coordinated regulation between lncRNA-siRNA
Plant-specific Pol IV and Pol V have been conventionally recognized as key enzymes in the production process of 24-nt siRNAs [24].Furthermore, lncRNAs transcribed by Pol V have been observed to facilitate the recruitment of silencing machinery compositions to the gene promoter region, thereby affecting repression of gene expression [81] and impeding the read-though of the genes [82].Some ncRNAs can create double-stranded RNA structures through binding to NATs.This interaction serves as the foundation for generating siRNAs, including lncRNAs, thus lncRNAs as a source of siRNAs.Within this context, two NATs molecules, Delta(1)-pyrroline-5-carboxylate dehydrogenase (P5CDH) and an unidentified gene, SRO5, had been identified as responsible for generating 21-nt siRNA by DCL1.The coordination process regulated salt tolerance in Arabidopsis [83].A research team identified that the stress-responsive lncRNAs also served as the origin of siRNAs in cassava [84].Moreover, when subject to cold treatment, the researchers observed that approximately 18.34% of lncNATs might potentially serve as precursors for the ranging in 19-25 nt of siRNAs.For example, lncNAT14-Manes.05G207400and lncNAT179-Manes.14G040500produced a significant number of 2127 siRNAs through mapping these siRNAs reads to the overlap region of the two lncNATs [85].Recently, a novel model describing the interaction between siRNAs and their host lncRNAs came to light.This model meant that the generation of siRNAs transcribed from lncNATs might regulate the expression of their corresponding complementary sense strands.In the context of resistance against TYLCV, researchers found that the viral siRNA (vsRNA) generated from the 25-nt noncoding intergenic region (IR), which displayed a near-perfect complementary with a lncRNA slLNR in TYLCV-susceptible tomato cultivars.Furthermore, they also found the expression of vsRNAs would induce silencing slLNR1, which was related to the manifestation of curled leaf and stunted plant phenotypes, highly akin to TYLCV symptoms [86].Under heat stress and powdery mildew infection in a wheat cultivar, both TalnRNA9 and TalnRNA12 were identified as variants of signal recognition particle (SRP) 7S RNA.Additionally, TapmlnRNA11, TapmlnRNA41, and TapmlnRNA42 were observed to be modulated by 24-nt siRNAs, encompassing five groups that exhibited matching with both TalnRNA9 and TalnRNA12.Furthermore, when considering different susceptible and resistant wheat cultivars, the act of inoculation with powdery mildew was found to increase the expression level of TalnRNA9 and TalnRNA12 and concurrently decrease the abundance of the antisense sequence [80].It is important to note that in the model plant Arabidopsis, an intricate process was referred to as the RNAmediated transcriptional gene silencing pathway or RdDM [87].
The key factors of the process encompassed lncRNA, siRNA, and conserved AGO [81].Specifically, siRNAs produced from PoI IV, RDR2, and DCL3 were responsible for binding ARGONAUTE 4 (AGO4).This interaction served to establish sequence specificity via base-pair complementation at specific loci [88].The acquisition of lncRNAs mediated by PoI II and plant-specific PoI V served as scaffolds for binding the AGO4-siRNA complex and directing targeted AGO4 to specific genomic loci [89].Typically, the lncRNAs derived from Pol V collaborated with siRNAs to facilitate the locus-specific establishment of RdDM [90].Some lncRNAs are associated with epigenetic regulation, especially the DNA methylation of cytosine [91].Researchers had highlighted that in a null mutant of OsMET1-2 −/− , a DNA methyltransferase 1 in rice, the TEs family En/Spm experienced transcriptional de-repression because of the genome-wide erasure of CG methylation.This phenomenon led to the production of plenty of specific lncRNAs [92].Additionally, there was an accumulation of RdDM-mediated CHH hypermethylation in the 5 -upstream genomic regions of lncRNAs.Furthermore, a substantial number of siRNAs and distinctive hypermethylated regions were found to co-localize by sRNA sequence technology.These regions were related to both common and mutant-specific lincRNAs [92,93].For instance, among them, 61.49% and 74.53% exhibited CHH hypermethylation and were enriched with siRNAs in their 5 -upstream region, respectively.Additionally, it was obverted that the simultaneous presence of CHH hypermethylation and the higher abundance of siRNAs was found to be approximately 52.17%.These findings suggested that siRNAs may take part in the regulation of lncRNA expression by DNA methylation [92].Furthermore, the paper uncovered that the transcription of Pol V was diminished in mutants lacking key components of the RdDM.The observation implied the existence of a positive feedback loop between DNA methylation and noncoding transcription, which served to reinforce the process of transcriptional silencing [90] (Fig. 4).

Coordinated regulation of other RNAs
Authors had reported that circRNAs acting as ceRNAs exert a regulated role in the expression level of miRNAs by absorbing and competitively suppressing the activity of miRNAs within plant systems.For example, the mechanism was exemplified in the diR156-related circRNA-miRNA-mRNA network in Arabidopsis through establishing and analyzing by comprehensive investigations of the PlantCircNet.Within this network, certain circRNAs and mRNAs had been predicted to serve as targets of miRNA156a-5p.Moreover, within the network, AT1G27370, AT1G53160, AT3G15270, and AT5G43270 had been experimentally validated [94].Furthermore, the paper provided another regulatory network about a Heat Shock Protein 18.2 (HSP18.2,AT5G59720), regarded as circRNAs-miR414-AT5G59720 in Arabidopsis.As per the findings, HSP18.2 could generate 19 circRNAs, which were targeted by miR414, the only miRNA in this network [94].As we all know, miRNA414 exhibited a high degree of conservation and assumed crucial roles in various processes throughout plant growth and development.Particularly, the significance is pronounced in response to alterations in environmental conditions, such as high or low temperature, oxygen concentration and irradiation intensity [95,96].Also, circRNA ATH_circ09039 was predictively correlated to light-related (PRJNA218215) and stress-related (PRJNA213635) samples in this regulatory network [94].Moreover, the plant circRNAs serve as miRNA sponges, for example, in tomatoes, 163 circRNAs had demonstrated a chilling response.Among these, 102 circRNAs were predicted to contain miRNAbinding sites [97].Furthermore, the coordinated regulatory network of ncRNAs actively participated in the silencing of gene transcription by modulating chromatin modifications, primarily targeted towards TEs and other repetitive gene regions, further inf luencing the specific gene expression patterns [81].The characteristic of lncRNAs was the absence of long ORFs (Open Reading Frames), making them suitable precursors for the generation of miRNAs and 21-nt phasiRNAs.The research evidence indicated that photoperiod-sensitive genic male sterility 1 (Pms1) locus encoded a lncRNA PMS1T, which was targeted for miR2118, leading to the production of 21-nt phasiRNAs, which predominantly accumulated in the PSMS strains (a line coming from two-line hybrid rice breeding) under long-day conditions [98].Furthermore, a lncRNA, designated as LDMAR, was essential for maintaining normal male fertility in rice plants exposed to extended periods of sunlight.Additionally, a siRNA, known as Psi-LDMAR came from the sense strand of the AK111270 transcript of the LDMAR promoter region [99].The vast majority of phasiRNAs were generated from the 1171 intergenic range, more specifically, within this range, over 700 were lincRNAs, bearing consensus sequences that were complementary to miR218 that were specifically transcribed in inf lorescences.Consequently, it could be deduced that lincRNAs, phasRNAs, and miR218 participated in the reproductive-specific stage [100].In addition, an increasing body of research indicated that the factors associated with miRNAs engaged with a broader array of ncRNAs by utilizing to compete for miRNA-binding sites, or by sequestering miRNA transcripts to inf luence the expression of target mRNAs [101].In the realm of ceRNA or TMs in experimental and computational identified processes within plants were contained protein-coding RNAs, lncRNAs, viral RNAs, pseudogenes, circRNA species, and artificial RNAs [71].When it comes to the classification of ceRNAs, artificial RNAs represent a type of engineered artificial target mimics (aTMs) created through the short-tandem target mimicry (STTM) technology apart from naturally occurring endogenous target mimics (eTMs) [102] (Fig. 4).

ncRNAs drive some functional micropeptides
LncRNAs have conventionally been characterized by their lack of protein-coding potential [25].However, with the emergence and growing application of techniques such as polysome profiling, techniques of purification, or sequencing of the ribosome, it has become possible that some lncRNAs may indeed encode functional micropeptides due to the presence of some short ORFs within lncRNAs [103].Moreover, a report detailed the integrated strategies adopted to investigate and characterize the extensive translation of functional micropeptides [104].Furthermore, lncRNAs translated into micropeptides depended on two regulatory factors located upstream of ORFs, including internal ribosome entry site (IRES) and N6-methyladenosine (m6A) methylation conserved sites.IRES is responsible for recruiting and assembling ribosomes, while m6A methylation is associated with the activation of endogenous ncRNAs translation [105].In G.max and G.sojae root tissues, it was revealed that 179 lncRNAs code 153 micropeptides, which were mainly co-expression processes related to coding proteins.These proteins are mainly related to precursors of metabolites and energy, ATP synthesis coupled electronic transmission, light reaction, response to defense, and photosynthesis [106].In Physcomitrella patens, several micropeptides lncRNA-sORFs were identified and participated in growth and development in moss, including Pp3c9_sORF1544, Pp3c18_sORF57, Pp3c25_sORF1000, Pp3c25_sORF1253 [107].Moreover, it predicted that most circRNAs had the potential to code for micropeptides.For example, the hop stunt viroid (HSV) and eggplant latent viroid (ELV) circRNAs had been associated with polysomes, presenting their capacity for translation, which was supported by the existence of several putative ORFs with encoding potential and subcellular localization signals [108].Pri-miRNAs could encode micropeptides in plants, referred to as miPEPs, such as miPEP17b from M. truncatula, and the small peptide VVI-miPEP171d1 originated from the first ORF of grapevine pri-miR171d.These miPEPs often enhance the transcription of respective pri-miRNAs to fulfill regulation roles [104].In Arabidopsis, micropeptide miPEP858a and miPEP156a are encoded from pri-miR858a and pri-miR156a, respectively.miPEP858a was involved in the phenylpropanoid pathway and plant growth while miPEP156a inf luenced root development [109].

Conclusion
This review delves into the multifaceted roles of ncRNAs in various aspects of plant growth and response to environmental stimuli.To structure the discussion, first, the ncRNAs are categorized into small RNAs, medium RNAs, lncRNAs, and circle RNAs based on their length and structure form.Furthermore, the review provides a comprehensive exploration of the origin and the mechanism underlying the production of these ncRNAs.Subsequently, the focus shifts to the regulatory mode of lncRNA in proximity to coding genes, which can be situated in various coding gene regions, including promoters, 5 UTRs, introns, exons, and 3 UTRs.Additionally, this review highlights the novel roles that lncRNAs as core components can participate in phase separation with the advance of sequence technology.This review also underscores the coordinated regulation involving lncRNAs, miRNAs, and siRNAs based on the pivotal roles of lncRNAs.Finally, as an emerging theme, this review addressed the growing body of evidence that some ncRNAs could code certain function micropeptides, overturning the traditional notion of ncRNAs with non-coding capacity.
Indeed, the ever-mounting evidence of lncRNAs involvement underscores their diverse and inf luential roles in plant growth and response to environmental stimuli.While certain advanced methods and computational algorithms have been proposed for predicting functional lncRNAs, the subsequent high-cost validation methods can impede the rapid development of our understanding in this field.Consequently, there is a pressing need to explore more efficient and cost-effective approaches for lncRNAs research, of course, the methods originated from animals will be a great inspiration for us.
The interconnected regulation between lncRNAs and other ncRNAs highlights the importance of constructing a comprehensive and coordinated regulation network among these ncRNA types, which is very necessary for us to understand the real function of lncRNAs.Despite the limited sequence conservation of lncRNAs, the rich landscape of ncRNAs as robust regulatory elements significantly augment our understanding of intricate regulatory networks governing plant growth, development, and stress responses.The ever-evolving landscape holds the promise of even more intriguing and uncharted roles for ncRNAs awaiting our exploration.

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 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.