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.

Acknowledgements

This review was supported by the National Key Research and Development Program of China (Grant No. 2022YFD2100101), the National Natural Science Foundation of China to G.Z. (Grant No. 32302623), the Joint NSFC-ISF Research Program (Grant No. 32061143022), and the National Natural Sciences Foundation of China (Grant No. 32172639).

Data availability

Data availability does not apply to this review article as no new data were created or analysed in this study.

Conflict of interest statement

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

References

[1] Rai MI, Alam M, Lightfoot DA et al. Classification and experimental identification of plant long non-coding RNAs. Genomics. 2019; 111: 997-1005

[2] Chao HY, Hu Y, Zhao L et al. Biogenesis, functions, interactions, and resources of non-coding RNAs in plants. Int J Mol Sci. 2022; 23: 3695

[3] Yu Y, Zhang YC, Chen XM et al. Plant noncoding RNAs: hidden players in development and stress responses. Annu Rev Cell Dev Bi. 2019; 35: 407-31

[4] Ben Amor B, Wirth S, Merchan F et al. Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res. 2009; 19: 57-69

[5] Axtell MJ . Classification and comparison of small RNAs from plants. Annu Rev Plant Biol. 2013; 64: 137-59

[6] Cuperus JT, Carbonell A, Fahlgren N et al. Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in. Nat Struct Mol Biol. 2010; 17: 997-1003

[7] Vazquez F, Blevins T, Ailhas J et al. Evolution of genes generates novel microRNA classes. Nucleic Acids Res. 2008; 36: 6429-38

[8] Henderson IR, Zhang X, Lu C et al. Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning . Nat Genet. 2006; 38: 721-5

[9] Guo R, Chen X, Lin Y et al. Identification of novel and conserved miRNAs in leaves of in vitro grown Citrus reticulata "Lugan" plantlets by Solexa sequencing . Front Plant Sci. 2015; 6: 1212

[10] Rogers K, Chen XM . Biogenesis, turnover, and mode of action of plant MicroRNAs. Plant Cell. 2013; 25: 2383-99

[11] Song X, Li Y, Cao X et al. MicroRNAs and their regulatory roles in plant-environment interactions. Annu Rev Plant Biol. 2019; 70: 489-525

[12] Deleris A, Gallego-Bartolome J, Bao J et al. Hierarchical action and inhibition of plant dicer-like proteins in antiviral defense. Science. 2006; 313: 68-71

[13] Li J, Yang Z, Yu B et al. Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol. 2005; 15: 1501-7

[14] Ren G, Xie M, Zhang S et al. Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage. Proc Natl Acad Sci U S A. 2014; 111: 6365-70

[15] Baldrich P, Beric A, Meyers BC . Despacito: the slow evolutionary changes in plant microRNAs. Curr Opin Plant Biol. 2018; 42: 16-22

[16] Debernardi JM, Rodriguez RE, Mecchia MA et al. Functional specialization of the plant miR396 regulatory network through distinct MicroRNA-target interactions. PLoS Genet. 2012; 8: e1002419

[17] Agrawal N, Dasaradhi PVN, Mohmmed A et al. RNA interference: biology, mechanism, and applications. Microbiol Mol Biol R. 2003; 67: 657-85

[18] Cuerda-Gil D, Slotkin RK . Non-canonical RNA-directed DNA methylation. Nat Plants. 2016; 2: 16163

[19] Liu TT, Zhu D, Chen W et al. A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa. Mol Plant. 2013; 6: 830-46

[20] Franz W, Witold F . U6 snRNA genes of Arabidopsis are transcribed by RNA polymerase III but contain the same two upstream promoter elements as RNA polymerase II-transcribed U-snRNA genes. Nucleic Acids Res. 1990; 18: 3451-8

[21] Wang YQ, Wang X, Deng W et al. Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. Mol Plant. 2014; 7: 514-27

[22] Wierzbicki AT, Blevins T, Swiezewski S . Long noncoding RNAs in plants. Annu Rev Plant Biol. 2021; 72: 245-71

[23] Marquardt S, Raitskin O, Wu Z et al. Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol Cell. 2014; 54: 156-65

[24] Matzke MA, Mosher RA . RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet 2014; 15: 394.

[25] Ponting CP, Oliver PL, Reik W . Evolution and functions of long noncoding RNAs. Cell. 2009; 136: 629-41

[26] Jeck WR, Sharpless NE . Detecting and characterizing circular RNAs. Nat Biotechnol. 2014; 32: 453-61

[27] Zhang XO, Dong R, Zhang Y et al. Diverse alternative back-splicing and alternative splicing landscape of circular RNAs. Genome Res. 2016; 26: 1277-87

[28] Chen LL, Yang L . Regulation of circRNA biogenesis. RNA Biol. 2015; 12: 381-8

[29] Lu Z, Grigory SF, Noto JJ et al. Metazoan tRNA introns generate stable circular RNAs in vivo. RNA. 2015; 21: 1554-65

[30] Ye CY, Chen L, Liu C et al. Widespread noncoding circular RNAs in plants. New Phytol. 2015; 208: 88-95

[31] Lai D, Meyer IM . A comprehensive comparison of general RNA-RNA interaction prediction methods. Nucleic Acids Res. 2016; 44: e61

[32] Conn VM, Hugouvieux V, Nayak A et al. A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat Plants. 2017; 3: 17053

[33] Tang BH, Hao ZQ, Zhu YF et al. Genome-wide identification and functional analysis of circRNAs in Zea mays. PLoS One. 2018; 13: e0202375

[34] Tan JJ, Zhou ZJ, Niu YJ et al. Identification and functional characterization of tomato CircRNAs derived from genes involved in fruit pigment accumulation. Sci Rep-Uk. 2017; 7: 8594

[35] Chen LL . The biogenesis and emerging roles of circular RNAs. Nat Rev Mol Cell Bio. 2016; 17: 205-11

[36] Thomas QA, Ard R, Liu J et al. Transcript isoform sequencing reveals widespread promoter-proximal transcriptional termination in Arabidopsis. Nat Commun. 2020; 11: 2589

[37] Seo JS, Diloknawarit P, Park BS et al. ELF18-INDUCED LONG NONCODING RNA 1 evicts fibrillarin from mediator subunit to enhance PATHOGENESIS-RELATED GENE 1 (PR1) expression. New Phytol. 2019; 221: 2067-79

[38] Ariel F, Teddy J, Latrasse D et al. Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Molcular Cell. 2014; 55: 383-96

[39] Moison M, Pacheco JM, Lucero L et al. The lncRNA interacts with the transcription factor WRKY42 to trigger root hair cell expansion in response to cold. Mol Plant. 2021; 14: 937-48

[40] Kim DH, Sung S . Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev Cell. 2017; 40: 302-312.e4

[41] Li Q, Gent JI, Zynda G et al. RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome. Proc Natl Acad Sci U S A. 2015; 112: 14728-33

[42] Wang H, Chung PJ, Liu J et al. Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res. 2014; 24: 444-53

[43] Zhu T, Yang C, Xie Y et al. Shade-induced lncRNA PUAR promotes shade response by repressing PHYA expression. EMBO Rep. 2023; 24: e56105

[44] Ye X, Wang S, Zhao X et al. Role of lncRNAs in cis- and trans-regulatory responses to salt in Populus trichocarpa . Plant J. 2022; 110: 978-93

[45] Pumplin N, Sarazin A, Jullien PE et al. DNA methylation influences the expression of isoforms, which encode proteins of alternative localization and function. Plant Cell. 2016; 28: 2786-804

[46] Wu HW, Deng S, Xu H et al. A noncoding RNA transcribed from the AGAMOUS (AG) second intron binds to CURLY LEAF and represses AG expression in leaves. New Phytol. 2018; 219: 1480-91

[47] Shin WJ, Nam AH, Kim JY et al. Intronic long noncoding RNA, RICE FLOWERING ASSOCIATED (RIFLA) regulates OsMADS56-mediated flowering in rice. Plant Sci. 2022; 320: 111278

[48] Hammond MC, Wachter A, Breaker RR . A plant 5S ribosomal RNA mimic regulates alternative splicing of transcription factor IIIA pre-mRNAs. Nat Struct Mol Biol. 2009; 16: 541-9

[49] Ai G, Li T, Zhu H et al. BPL3 binds the long non-coding RNA nalncFL7 to suppress FORKED-LIKE7 and modulate HAI1-mediated MPK3/6 dephosphorylation in plant immunity. Plant Cell. 2023; 35: 598-616

[50] Chen W, Zhu T, Shi Y et al. An antisense intragenic lncRNA SEAIRa mediates transcriptional and epigenetic repression of SERRATE in Arabidopsis. Proc Natl Acad Sci U S A. 2023; 120: e2216062120

[51] Krzyszton M, Zakrzewska-Placzek M, Kwasnik A et al. Defective XRN3-mediated transcription termination in Arabidopsis affects the expression of protein-coding genes. Plant J. 2018; 93: 1017-31

[52] Kindgren P, Ard R, Ivanov M et al. Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nat Commun. 2018; 9: 4561

[53] Xu W, Xu H, Li K et al. The R-loop is a common chromatin feature of the Arabidopsis genome. Nat Plants. 2017; 3: 704-14

[54] Hisanaga T, Okahashi K, Yamaoka S et al. A cis-acting bidirectional transcription switch controls sexual dimorphism in the liverwort . EMBO J. 2019; 38: e100240

[55] Liu NK, Xu Y, Li Q et al. A lncRNA fine-tunes salicylic acid biosynthesis to balance plant immunity and growth. Cell Host Microbe. 2022; 30: 1124-38

[56] Zhu BZ, Yang Y, Li R et al. RNA sequencing and functional analysis implicate the regulatory role of long non-coding RNAs in tomato fruit ripening. J Exp Bot. 2015; 66: 4483-95

[57] Yu TT, Tzeng DTW, Li R et al. Genome-wide identification of long non-coding RNA targets of the tomato MADS box transcription factor RIN and function analysis. Ann Bot-London. 2019; 123: 469-82

[58] Li R, Fu DQ, Zhu BZ et al. CRISPR/Cas9-mediated mutagenesis of lncRNA1459 alters tomato fruit ripening. Plant J. 2018; 94: 513-24

[59] Yang J, He R, Qu Z et al. Long noncoding RNA ARTA controls ABA response through MYB7 nuclear trafficking in Arabidopsis. Dev Cell. 2023; 58: 1206-1217.e4

[60] Zhou YF, Zhang YC, Sun YM et al. The parent-of-origin lncRNA regulates rice endosperm development. Nat Commun. 2021; 12: 6525

[61] Xiao Y, Kang B, Li M et al. Transcription of lncRNA ACoS-AS1 is essential to trans-splicing between SlPsy1 and ACoS-AS1 that causes yellow fruit in tomato. RNA Biol. 2020; 17: 596-607

[62] Yang ZC, Yang Z, Yang C et al. Identification and genetic analysis of alternative splicing of long non-coding RNAs in tomato initial flowering stage. Genomics. 2020; 112: 897-907

[63] Rigo R, Bazin J, Romero-Barrios N et al. The Arabidopsis lncRNA ASCO modulates the transcriptome through interaction with splicing factors. EMBO Rep. 2020; 21: e48977

[64] Xie XD, Jin J, Wang C et al. Investigating nicotine pathway-related long non-coding RNAs in tobacco. Front Genet. 2023; 13: 1102183

[65] Kosmacz M, Gorka M, Schmidt S et al. Protein and metabolite composition of Arabidopsis stress granules. New Phytol. 2019; 222: 1420-33

[66] Emenecker RJ, Holehouse AS, Strader LC . Emerging roles for phase separation in plants. Dev Cell. 2020; 55: 69-83

[67] Khong A, Matheny T, Jain S et al. The stress granule transcriptome reveals principles of mRNA accumulation in stress granules. Mol Cell. 2017; 68: 808-820.e5

[68] Kearly A, Nelson ADL, Skirycz A et al. Composition and function of stress granules and P-bodies in plants. Semin Cell Dev Biol. 2022; 156: 167-75

[69] Pitchiaya S, Mourao MDA, Jalihal AP et al. Dynamic recruitment of single RNAs to processing bodies depends on RNA functionality. Mol Cell. 2019; 74: 521-533.e6

[70] Ariel F, Jegu T, Latrasse D et al. Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol Cell. 2014; 55: 383-96

[71] Thomson DW, Dinger ME . Endogenous microRNA sponges: evidence and controversy. Nat Rev Genet. 2016; 17: 272-83

[72] Li YJ, Li XR, Yang J et al. Natural antisense transcripts of MIR398 genes suppress microR398 processing and attenuate plant thermotolerance. Nat Commun. 2020; 11: 5351

[73] Salmena L, Poliseno L, Tay Y et al. A ceRNA hypothesis: the Rosetta stone of a hidden RNA language? Cell. 2011; 146: 353-8

[74] Franco-Zorrilla JM, Valli A, Todesco M et al. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet. 2007; 39: 1033-7

[75] Hou X, Cui J, Liu W et al. LncRNA39026 enhances tomato resistance to Phytophthora infestans by decoying miR168a and inducing PR gene expression . Phytopathology. 2019; 110: 873-80

[76] Sun Z, Huang K, Han Z et al. Author correction: genome-wide identification of Arabidopsis long noncoding RNAs in response to the blue light. Sci Rep-Uk. 2020; 10: 11446

[77] Jiang N, Cui J, Shi Y et al. Tomato lncRNA23468 functions as a competing endogenous RNA to modulate NBS-LRR genes by decoying miR482b in the tomato-Phytophthora infestans interaction. Hortic Res. 2019; 6: 28

[78] Wang MJ, Yuan D, Tu L et al. Long noncoding RNAs and their proposed functions in fibre development of cotton (Gossypium spp.). New Phytol. 2015; 207: 1181-97

[79] Zhang YC, Yu Y, Wang CY et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol. 2013; 31: 848-52

[80] Xin MM, Wang Y, Yao Y et al. Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol. 2011; 11: 61

[81] Zheng Q, Rowley MJ, Böhmdorfer G et al. RNA polymerase V targets transcriptional silencing components to promoters of protein-coding genes. Plant J. 2013; 73: 179-89

[82] McKinlay A, Podicheti R, Wendte JM et al. RNA polymerases IV and V influence the 3 boundaries of polymerase II transcription units in Arabidopsis. RNA Biol. 2018; 15: 269-79

[83] Borsani O, Zhu JH, Verslues PE et al. Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell. 2005; 123: 1279-91

[84] Li S, Yu X, Lei N et al. Genome-wide identification and functional prediction of cold and/or drought-responsive lncRNAs in cassava. Sci Rep. 2017; 7: 45981

[85] Xia J, Zeng C, Chen Z et al. Endogenous small-noncoding RNAs and their roles in chilling response and stress acclimation in Cassava. BMC Genomics. 2014; 15: 634

[86] Yang YW, Liu T, Shen D et al. Tomato yellow leaf curl virus intergenic siRNAs target a host long noncoding RNA to modulate disease symptoms. PLoS Pathog. 2019; 15: e1007534

[87] Zilberman D, Cao XF, Jacobsen SE . ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation. Science. 2003; 299: 716-9

[88] Qi YJ, He X, Wang XJ et al. Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature. 2006; 443: 1008-12

[89] Wierzbicki AT, Ream TS, Haag JR et al. RNA polymerase V transcription guides ARGONAUTE4 to chromatin. Nat Genet. 2009; 41: 630-4

[90] Rothi MH, Tsuzuki M, Sethuraman S et al. Reinforcement of transcriptional silencing by a positive feedback between DNA methylation and non-coding transcription. Nucleic Acids Res. 2021; 49: 9799-808

[91] Matzke M, Kanno T, Daxinger L et al. RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol. 2009; 21: 367-76

[92] Li JZ, Li N, Zhu L et al. Mutation of a major CG methylase alters genome-wide lncRNA expression in rice. G3. 2021; 11: jkab049

[93] Lu X, Wang X, Chen X et al. Single-base resolution methylomes of upland cotton (Gossypium hirsutum L.) reveal epigenome modifications in response to drought stress . BMC Genomics. 2017; 18: 297

[94] Zhang PJ, Meng X, Chen H et al. PlantCircNet: a database for plant circRNA-miRNA-mRNA regulatory networks. Database-Oxford. 2017; 2017: bax089

[95] Macovei A, Tuteja N . microRNAs targeting DEAD-box helicases are involved in salinity stress response in rice (Oryza sativa L.). BMC Plant Biol. 2012; 12: 183

[96] Guleria P, Yadav SK . Identification of miR414 and expression analysis of conserved miRNAs from Stevia rebaudiana. Genom Proteom Bioinform. 2011; 9: 211-7

[97] Zuo JH, Wang Q, Zhu BZ et al. Deciphering the roles of circRNAs on chilling injury in tomato. Biochem Biophys Res Commun. 2016; 479: 132-8

[98] Fan YR, Yang J, Mathioni SM et al. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc Natl Acad Sci U S A. 2016; 113: 15144-9

[99] Ding JH, Shen J, Mao H et al. RNA-directed DNA methylation is involved in regulating photoperiod-sensitive male sterility in rice. Mol Plant. 2012; 5: 1210-6

[100] Komiya R, Ohyanagi H, Niihama M et al. Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J. 2014; 78: 385-97

[101] Paschoal AR, Lozada-Chavez I, Domingues DS et al. ceRNAs in plants: computational approaches and associated challenges for target mimic research. Brief Bioinform. 2018; 19: 1273-89

[102] Zand Karimi H, Innes RW . Molecular mechanisms underlying host-induced gene silencing. Plant Cell. 2022; 34: 3183-99

[103] Ruiz-Orera J, Messeguer X, Subirana JA et al. Long non coding RNAs as a source of new peptides. elife. 2014; 3: 1-24

[104] Chen YJ, Li D, Fan W et al. PsORF: a database of small ORFs in plants. Plant Biotechnol J. 2020; 18: 2158-60

[105] Yang YB, Gao X, Zhang M et al. Novel role of FBXW7 circular RNA in repressing Glioma tumorigenesis. Jnci-J Natl Cancer I. 2018; 110: 304-15

[106] Lin X, Lin W, Ku YS et al. Analysis of soybean long non-coding RNAs reveals a subset of small peptide-coding transcripts(1[OPEN]). Plant Physiol. 2020; 182: 1359-74

[107] Fesenko I, Kirov I, Kniazev A et al. Distinct types of short open reading frames are translated in plant cells. Genome Res. 2019; 29: 1464-77

[108] Marquez-Molins J, Navarro JA, Seco LC et al. Might exogenous circular RNAs act as protein-coding transcripts in plants? RNA Biol. 2021; 18: 98-107

[109] Sharma A, Badola PK, Bhatia C et al. Primary transcript of miR858 encodes regulatory peptide and controls flavonoid biosynthesis and development in Arabidopsis. Nat Plants. 2020; 6: 1262-74