Research Advance on Plant Long Noncoding RNAs

doi:10.13560/j.cnki.biotech.bull.1985.2018-0167

Abstract

Abstract: Long noncoding RNAs（lncRNAs）refers to those RNAs having >200 nucleotides while containing ORF of less than 100 amino acids.. Based on their locations to nearby protein-coding genes,lncRNAs can be roughly classified into four types：long noncoding natural antisense transcripts（lincNATs）,intron lncRNAs,promoter lncRNAs and long intergenic ncRNAs（lincRNAs）. lncRNAs can function as recruiters,tethers,guides,decoys and signals for other biological molecules via interactions with epigenetic,transcriptional,post-transcriptional and translation control. A larger number of lncRNAs have been identified in many plant species and have shown to be important regulators in plant growth and development such as vernalization and flowering induction,formation of nodules in leguminous plants,pollen development and male sterility,photomorphogenesis,Pi absorption,lateral root development,auxin transport and development signal output,plant responses to diverse stresses and diseases,etc. lncRNAs are of great significance for the regulation of plant growth and development,also potent tools for the improvement of crop cultivar. In recent years,the research on plant lncRNAs increased drastically,and the literature on this field has grown rapidly. This review integrates the current knowledge on the classification,identification and research,molecular regulatory mechanisms and functions of plant lncRNAs in order to provide references for researchers.

Key words: long noncoding RNAs（lncRNAs）, molecular regulatory mechanisms, transcriptional regulation, post-transcriptional regulation, epigenetics

TAN Yu-rong, WANG Dan, GAO Xuan, LIU Jin-ping. Research Advance on Plant Long Noncoding RNAs[J]. Biotechnology Bulletin, 2018, 34(10): 1-10.

References

[1] Pandey RR, Kanduri C.Transcriptional and posttranscriptional programming by long noncoding RNAs[M]//Ugarković Ð(ed.)Long Non-Coding RNAs, Progress in Molecular and Subcellular Biology 51. Heidelberg:Springer-Verlag, 2011:1-27.
[2] Djebali S, Davis CA, Merkel A, et al.Landscape of transcription in human cells[J]. Nature, 2012, 489(7414):101-108.
[3] Encode Project Consortium.An integrated encyclopedia of DNA elements in the human genome[J]. Nature, 2012, 489(7414):57-74.
[4] Vickers KC, Roteta LA, Hucheson-Dilks H, et al.Mining diverse small RNA species in the deep transcriptome[J]. Trends Biochem Sci, 2015, 40(1):4-7.
[5] D’Ario M, Griffiths-Jones S, Kim M. Small RNAs:Big impact on plant development[J]. Trends Plant Sci, 2017, 22(12):1056-1068.
[6] Yu Y, Jia T, Chen X.The ‘how’ and ‘where’ of plant microRNAs[J]. New Phytol, 2017, 216(4):1002-1017.
[7] Liu J, Wang H, Chua NH.Long noncoding RNA transcriptome of plants[J]. Plant Biotechnol J, 2015, 13(3):319-328.
[8] Ariel F, Romero-Barrios N, Jégu T, et al.Battles and hijacks:non-coding transcription in plants[J]. Trends Plant Sci, 2015, 20(6):362-371.
[9] Rymarquis LA, Kastenmayer JP, Huttenhofer AG, et al.Diamonds in the rough:mRNA-like non-coding RNAs[J]. Trends Plant Sci, 2008, 13:329-334.
[10] Jouannet V, Crespi M.Long nonprotein-coding RNAs in plants[J].
Prog Mol Subcell Biol, 2011, 51:179-200.
[11] Yamada M.Functions of long intergenic non-coding(linc)RNAs in plants[J]. J Plant Res, 2017, 130(1):67-73.
[12] St Laurent G, Wahlestedt C, Kapranov P.The Landscape of long noncoding RNA classification[J]. Trends Genet, 2015, 31(5):239-251.
[13] Ulitsky I.Evolution to the rescue:using comparative genomics to understand long non-coding RNAs[J]. Nat Rev Genet, 2016, 17(10):601-614.
[14] Sanbonmatsu KY.Towards structural classification of long non-coding RNAs[J]. Biochim Biophys Acta, 2016, 1859(1):41-45.
[15] 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[J]. Mol Plant, 2013, 6:830-846.
[16] Wang Y, Wang X, Deng W, et al.Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis[J]. Mol Plant, 2014, 7:514-527.
[17] Kashi K, Henderson L, Bonetti A, et al.Discovery and functional analysis of lncRNAs:Methodologies to investigate an uncharacterized transcriptome[J]. Biochim Biophys Acta. 2016, 1859(1):3-15.
[18] Ma H, Hao Y, Dong X, et al.Molecular mechanisms and function prediction of long noncoding RNA[J]. Scientific World Journal, 2012, 2012:541786.
[19] Ulitsky I, Bartel DP.LincRNAs:genomics, evolution, and mechanisms[J]. Cell, 2013, 154:26-46.
[20] Adiconis X, Borges-Rivera D, Satija R, et al.Comparative analysis of RNA sequencing methods for degraded or low-input samples[J]. Nat Methods, 2013, 10(7):623-629.
[21] Mattick JS.The genetic signatures of noncoding RNAs[J]. PLoS Genet, 2009, 5(4):e1000459.
[22] Fu XD.Non-coding RNA:a new frontier in regulatory biology[J]. Natl Sci Rev, 2014, 1(2):190-204.
[23] Iwakiri J, Hamada M, Asai K.Bioinformatics tools for lncRNA research[J]. Biochim Biophys Acta, 2016, 1859(1):23-30.
[24] Zhang Y, Tao Y, Liao Q.Long noncoding RNA:a crosslink in biological regulatory network[J]. Brief Bioinform, 2017,(5):930-945.
[25] Gomes AQ, Nolasco S, Soares H.Non-coding RNAs:multi-tasking molecules in the cell[J]. Int J Mol Sci, 2013, 14(8):16010-16039.
[26] Wu HJ, Wang ZM, Wang M, et al.Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants[J]. Plant Physiol, 2013, 161:1875-1884.
[27] Nakagawa S, Kageyama Y.Nuclear lncRNAs as epigenetic regulators-beyond skepticism[J]. Biochim Biophys Acta, 2014, 1839(3):215-222.
[28] Shafik A, Schumann U, Evers M, et al.The emerging epitranscriptomics of long noncoding RNAs[J]. Biochim Biophys Acta, 2016, 1859(1):59-70.
[29] Nachtergaele S, He C.The emerging biology of RNA post-transcriptional modifications[J]. RNA Biol, 2017, 14(2):156-163.
[30] Betancur JG.Pervasive lncRNA binding by epigenetic modifying complexes--The challenges ahead[J]. Biochim Biophys Acta, 2016, 1859(1):93-101.
[31] Lipshitz HD, Peattie DA, Hogness DS.Novel transcripts from the Ultrabithorax domain of the bithorax complex[J]. Gene Dev, 1987, 1:307-322.
[32] Brockdorff N, Ashworth A, Kay GF, et al.Conservation of position and exclusive expression of mouse Xist from the inactive X chromosome[J]. Nature, 1991, 351:329-331.
[33] Brown CJ, Ballabio A, Rupert JL, et al.A gene from the region of the human X inactivation centre is expressed exclusively from the inactive X chromosome[J]. Nature, 1991, 349:38-44.
[34] Ben Amor B, Wirth S, Merchan F, et al.Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses[J]. Genome Res, 2009, 19:57-69.
[35] Matsui A, Ishida J, Morosawa T, et al.Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array[J]. Plant Cell Physiol, 2008, 49:1135-1149.
[36] Okamoto M, Tatematsu K, Matsui A, et al.Genome-wide analysis of endogenous abscisic acid-mediated transcription in dry and imbibed seeds of Arabidopsis using tiling arrays[J]. Plant J, 2010, 62:39-51.
[37] Wang H, Chung PJ, Liu J, et al.Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis[J]. Genome Res, 2014, 24:444-453.
[38] MacIntosh GC, Wilkerson C, Green PJ. Identification and analysis of Arabidopsis expressed sequence tags characteristic of non-coding RNAs[J]. Plant Physiol, 2001, 127:765-776.
[39] Li S, Yamada M, Han X, et al.High-resolution expression map of the Arabidopsis root reveals alternative splicing and lincRNA regulation[J]. Dev Cell, 2016, 39:508-522.
[40] Liu J, Jung C, Xu J, et al.Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis[J]. Plant Cell, 2012, 24:4333-4345.
[41] Zhang YC, Liao JY, Li ZY, et al.Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice[J]. Genome Biol, 2014, 15:512.
[42] Lu T, Zhu C, Lu G, et al.Strand-specific RNA-seq reveals widespread occurrence of novel cis-natural antisense transcripts in rice[J]. BMC Genom, 2012, 13:721.
[43] Xin M, 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[J]. BMC Plant Biol, 2011, 11:61.
[44] Cagirici HB, Alptekin B, Budak H.RNA Sequencing and Co-expressed long non-coding RNA in modern and wild wheats[J]. Sci Rep, 2017, 7(1):10670.
[45] Li L, Eichten SR, Shimizu R, et al.Genome-wide discovery and characterization of maize long non-coding RNAs[J]. Genome Biol, 2014, 15:R40.
[46] Boerner S, McGinnis KM. Computational identification and functional predictions of long noncoding RNA in Zea mays[J]. PLoS One, 2012, 7:e43047.
[47] Qi X, Xie S, Liu Y, et al.Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing[J]. Plant Mol Biol, 2013, 83:459-473.
[48] Lu X, Chen X, Mu M, et al.Genome-wide analysis of long noncoding RNAs and their responses to drought stress in cotton(Gossypium hirsutum L.)[J]. PLoS One, 2016, 11(6):e0156723.
[49] Zou C, Wang Q, Lu C, et al.Transcriptome analysis reveals long noncoding RNAs involved in fiber development in cotton(Gossypium arboreum)[J]. Sci China Life Sci, 2016, 59(2):164-171.
[50] Wen J, Parker BJ, Weiller GF.In silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula[J]. In Silico Biol, 2007, 7:485-505.
[51] Wang L, Zhao S, Gu C, et al.Deep RNA-Seq uncovers the peach transcriptome landscape[J]. Plant Mol Biol, 2013, 83:365-377.
[52] Chen J, Quan M, Zhang D.Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-seq[J]. Planta, 2015, 241:125-143.
[53] Shuai P, Liang D, Tang S, et al.Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa[J]. J Exp Bot, 2014, 65:4975-4983.
[54] Song Y, Ci D, Tian M, et al.Stable methylation of a non-coding RNA gene regulates gene expression in response to abiotic stress in Populus simonii[J]. J Exp Bot, 2016, 67(5):1477-1492.
[55] Tang W, Zheng Y, Dong J, et al.Comprehensive transcriptome profiling reveals long noncoding RNA expression and alternative splicing regulation during fruit development and ripening in kiwifruit(Actinidia chinensis)[J]. Front Plant Sci, 2016, 7:335.
[56] Song X, Liu G, Huang Z, et al.Temperature expression patterns of genes and their coexpression with LncRNAs revealed by RNA-Seq in non-heading Chinese cabbage[J]. BMC Genomics, 2016, 17:297.
[57] Hao Z, Fan C, Cheng T, et al.Genome-wide identification, characterization and evolutionary analysis of long intergenic noncoding RNAs in cucumber[J]. PLoS One, 2015, 10(3):e0121800.
[58] Flórez-Zapata NM, Reyes-Valdés MH, Martínez O.Long non-coding RNAs are major contributors to transcriptome changes in sunflower meiocytes with different recombination rates[J]. BMC Genomics, 2016, 17:490.
[59] Zhu Y, Chen L, Zhang C, et al.Global transcriptome analysis reveals extensive gene remodeling, alternative splicing and differential transcription profiles in non-seed vascular plant Selaginella moellendorffii[J]. BMC Genomics, 2017, 18(Suppl 1):1042.
[60] Zhang G, Duan A, Zhang J, et al.Genome-wide analysis of long non-coding RNAs at the mature stage of sea buckthorn(Hippophae rhamnoides Linn)fruit[J]. Gene, 2017, 596:130-136.
[61] Xu Q, Song Z, Zhu C, et al.Systematic comparison of lncRNAs with protein coding mRNAs in population expression and their response to environmental change[J]. BMC Plant Biol, 2017, 17(1):42.
[62] Heo JB, Sung S.Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA[J]. Science, 2011, 331:76-79.
[63] Kim DH, Sung S.Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs[J]. Dev Cell, 2017, 40(3):302-312.
[64] Csorba T, Questa JI, Sun Q, et al.Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization[J]. Proc Natl Acad Sci USA, 2014, 111:16160-16165.
[65] Marquardt S, Raitskin O, Wu Z, et al.Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription[J]. Mol Cell, 2014, 54:156-165.
[66] Crespi M, Jurkevitch E, Poiret M, et al.enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth[J]. EMBO J, 1994, 13:5099-5112.
[67] Girard G, Roussis A, Gultyaev AP, et al.Structural motifs in the RNA encoded by the early nodulation gene enod40 of soybean[J]. Nucleic Acids Res, 2003, 31:5003-5015.
[68] Rohrig H, Schmidt J, Miklashevichs E, et al.Soybean ENOD40 encodes two peptides that bind to sucrose synthase[J]. Proc Natl Acad Sci USA, 2002, 99:1915-1920.
[69] Charon C, Sousa C, Crespi M, et al.Alteration of enod40 expression modifies Medicago truncatula root nodule development induced by Sinorhizobium meliloti[J]. Plant Cell, 1999, 11:1953-1966.
[70] Wan X, Hontelez J, Lillo A, et al.Medicago truncatula ENOD40-1 and ENOD40-2 are both involved in nodule initiation and bacteroid development[J]. J Exp Bot, 2007, 58:2033-2041.
[71] Campalans A, Kondorosi A, Crespi M.Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula[J]. Plant Cell, 2004, 16:1047-1059.
[72] Ding J, Lu Q, Ouyang Y, et al.A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice[J]. Proc Natl Acad Sci USA, 2012, 109(7):2654-2659.
[73] Ding J, Shen J, Mao H, et al.RNA-directed DNA methylation is involved in regulating photoperiod-sensitive male sterility in rice[J]. Mol Plant, 2012, 5(6):1210-1216.
[74] Wang Y, Fan X, Lin F, et al.Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light[J]. Proc Natl Acad Sci USA, 2014, 111:10359-10364.
[75] Chiou TJ, Aung K, Lin SI, et al.Regulation of phosphate homeostasis by MicroRNA in Arabidopsis[J]. Plant Cell, 2006, 18:412-421.
[76] Franco-Zorrilla JM, Valli A, Todesco M, et al.Target mimicry provides a new mechanism for regulation of microRNA activity[J]. Nat Genet, 2007, 39:1033-1037.
[77] Jabnoune M, Secco D, Lecampion C, et al.A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness[J]. Plant Cell, 2013, 25:4166-4182.
[78] Schindler S, Szafranski K, Hiller M, et al.Alternative splicing at NAGNAG acceptors in Arabidopsis thaliana SR and SR-related proteincoding genes[J]. BMC Genomics, 2008, 9:159.
[79] Bardou F, Ariel F, Simpson CG, et al.Long noncoding RNA modulates alternative splicing regulators in Arabidopsis[J]. Dev Cell, 2014, 30:166-176.
[80] Ariel F, Jegu T, Latrasse D, et al.Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop[J]. Mol Cell, 2014, 55(3):383-396.
[81] Zhang L, Wang M, Li N, et al.Long noncoding RNAs involve in resistance to Verticillium dahliae, a fungal disease in cotton[J]. Plant Biotechnol J, 2018, 16(6):1172-1185.
[82] Cui J, Luan Y, Jiang N, et al.Comparative transcriptome analysis between resistant and susceptible tomato allows the identification of lncRNA16397 conferring resistance to Phytophthora infestans by co-expressing glutaredoxin[J]. Plant J, 2017, 89(3):577-589.
[83] Zhu QH, Stephen S, Taylor J, et al.Long noncoding RNAs responsive to Fusarium oxysporum infection in Arabidopsis thaliana[J]. New Phytol, 2014, 201(2):574-584.
[84] Qin T, Zhao H, Cui P, et al.A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance[J]. Plant Physiol, 2017, 175(3):1321-1336.
[85] Wang H, Chua NH, Wang XJ.Prediction of trans-antisense transcripts in Arabidopsis thaliana[J]. Genome Biol, 2006, 7(10):R92.
[86] Borsani O, Zhu J, Verslues PE, et al.Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis[J]. Cell, 2005, 123(7):1279-1291.
[87] Wunderlich M, Gross-Hardt R, Schöffl F.Heat shock factor HSFB2a involved in gametophyte development of Arabidopsis thaliana and its expression is controlled by a heat-inducible long non-coding antisense RNA[J]. Plant Mol Biol, 2014, 85(6):541-550.
[88] Zubko E, Meyer P.A natural antisense transcript of the Petunia hybrida Sho gene suggests a role for an antisense mechanism in cytokinin regulation[J]. Plant J, 2007, 52:1131-1139.
[89] Ron M, Alandete Saez M, et al.Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis[J]. Genes Dev, 2010, 24(10):1010-1021.
[90] Held MA, Penning B, Brandt AS, et al.Small-interfering RNAs from natural antisense transcripts derived from a cellulose synthase gene modulate cell wall biosynthesis in barley[J]. Proc Natl Acad Sci USA, 2008, 105(51):20534-20539.
[91] Katiyar-Agarwal S, Morgan R, Dahlbeck D, et al.A pathogen-inducible endogenous siRNA in plant immunity[J]. Proc Natl Acad Sci USA, 2006, 103:18002-18007.
[92] Wang H, Niu QW, Wu HW, et al.Analysis of non-coding transcriptome in rice and maize uncovers roles of conserved lncRNAs associated with agriculture traits[J]. Plant J, 2015, 84(2):404-416.
[93] Liu R, Zhu JK.Non-coding RNAs as potent tools for crop improvement[J]. National Science Review, 2014, 1(2):186-189.