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Long non-coding RNAs: Fine-tuning the developmental responses in plants

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Abstract

Plant developmental biology is associated with various gene regulatory pathways involved in different phases of their life cycle. In course of development, growth and differentiation of different organs in plants are regulated by specific sets of gene expression. With the advances in genomic and bioinformatic techniques, particularly high-throughput sequencing technology, many transcriptional units with no protein-coding potential have been discovered. Previously thought to be the dark matters of genome, long non-coding RNAs (lncRNAs) are gradually gaining importance as crucial players in gene regulation during different developmental phases. Some lncRNAs, showing complementarity to microRNAs (miRNAs), are used as endogenous target mimics of specific miRNA family. A number of lncRNAs can also act as natural antisense transcripts to attenuate the expression of coding genes. Although lncRNA-mediated regulations have extensively been studied in animals, plant lncRNA research is still in its initial phase. The present review highlights the regulatory mechanism and different physiological aspects of lncRNAs in plant development. In plants, lncRNAs are found to be associated with a number of plant developmental functions such as lateral root development, vernalization, photomorphogenesis, pollen development, fiber development and nodulation. Understanding these potent roles of lncRNAs in plant development can further provide novel tools for crop improvement programs in future.

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Abbreviations

ABA:

abscisic acid

APOLO:

auxin-regulated promoter loop

ARF:

auxin response factor

ASCO-RNA:

alternative splicing competitor long non-coding RNA

CBP:

cap-binding protein

eTM:

endogenous target mimic

FLC:

FLOWERING LOCUS C

FT:

FLOWERING LOCUS T

HID1:

hidden treasure 1

LDMAR:

long day (LD)-specific male-fertility associated RNA

lincRNA:

long intergenic non-coding RNA

lncRNA:

long non-coding RNA

miRNA:

microRNAs

NAT:

natural antisense transcript

ncRNA:

non-coding RNA

NMD:

nonsense-mediated-mRNA decay

NSR:

nuclear speckle RNA-binding protein

PID:

PINOID

PIF:

phytochrome-interacting factor

PRC1:

polycomb recessive complex 1

RBP1:

RNA binding protein 1

RdDM:

RNA-dependent DNA methylation

siRNA:

small interfering RNA

sncRNA:

small non-coding RNA

snRNA:

small nuclear RNA

UBP1:

ubiquitin specific protease 1

UPF:

UP-frameshift protein

References

  • Akua T and Shaul O 2013 The Arabidopsis thaliana MHX gene includes an intronic element that boosts translation when localized in a 5′ UTR intron. J. Exp. Bot. 64 4255–4270

    Article  CAS  Google Scholar 

  • Ariel F, Jegu T, Latrasse D, Romero-Barrios N, Christ A, Benhamed M and Crespi M 2014 Noncoding transcription by alternative RNA polymerases dynamically regulates an auxin-driven chromatin loop. Mol. Cell 55 383–396

    Article  CAS  Google Scholar 

  • Axtell MJ 2013 Classification and comparison of small RNAs from plants. Annu. Rev. Plant Biol. 64 137–159

    Article  CAS  Google Scholar 

  • Bardou F, Ariel F, Simpson CG, Romero-Barrios N, Laporte P, Balzergue S, Brown JWS and Crespi M 2014 Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev. Cell 30 166–176

    Article  CAS  Google Scholar 

  • Batista PJ and Chang HY 2013 Cytotopic localization by long noncoding RNAs. Curr. Opin. Cell Biol. 25 195–199

    Article  CAS  Google Scholar 

  • Blevins T, Pontvianne F, Cocklin R, Podicheti R, Chandrasekhara C, Yerneni S, Braun C, Lee B, Rusch D, Mockaitis K, Tang H and Pikkard CS 2014 A two-step process for epigenetic inheritance in Arabidopsis. Mol. Cell 54 30–42

    Article  CAS  Google Scholar 

  • Campalans A, Kondorosi A and Crespi M 2004 Enod40, a short open reading frame-containing mRNA, induces cytoplasmic localization of a nuclear RNA binding protein in Medicago truncatula. Plant Cell 16 1047–1059

    Article  CAS  Google Scholar 

  • Chekanova JA, Gregory BD, Reverdatto SV, Chen H, Kumar R, Hooker T, Yazaki J, Li P, Skiba N, Peng Q, Alonso J, Brukhin V, Grossniklaus U, Ecker JR and Belostotsky DA 2007 Genome-wide high-resolution mapping of exosome substrates reveals hidden features in the Arabidopsis transcriptome. Cell 131 1340–1353

    Article  CAS  Google Scholar 

  • Chen M and Chory J 2011 Phytochrome signaling mechanisms and the control of plant development. Trends Cell Biol. 21 664–671

    Article  CAS  Google Scholar 

  • Chew GL, Pauli A, Rinn JL, Regev A, Schier AF and Valen E 2013 Ribosome profiling reveals resemblance between long non-coding RNAs and 5′ leaders of coding RNAs. Development 140 2828–2834

    Article  CAS  Google Scholar 

  • Chitwood DH and Sinha NR 2014 Plant development: Small RNAs and the metamorphosis of leaves. Curr. Biol. 24 R1087–R1089

    Article  CAS  Google Scholar 

  • Cho J and Paszkowski J 2017 Regulation of rice root development by a retrotransposon acting as a microRNA sponge. eLife 6 e30038

  • Christie M, Croft LJ and Carroll BJ 2011 Intron splicing suppresses RNA silencing in Arabidopsis. Plant J. 68 159–167

    Article  CAS  Google Scholar 

  • Crevillén P, Yang H, Cui X, Greeff C, Trick M, Qiu Q, Cao X and Dean C 2014 Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515 587–590

    Article  Google Scholar 

  • Di C, Yuan J, Wu Y, Li J, Lin H, Hu L, Zhang T, Qi Y, Gerstein MB, Guo Y and Lu ZJ 2014 Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. Plant J. 80 848–861

    Article  CAS  Google Scholar 

  • Dong C, Liu S, Lv Y, Zhang C, Gao H, Tan L and Wang H 2016 Long non-coding RNA HOTAIR regulates proliferation and invasion via activating Notch signalling pathway in retinoblastoma. J. Biosci. 41 677–687

    Article  CAS  Google Scholar 

  • van Dijk EL, Chen CL, d’Aubenton-Carafa Y, Gourvennec S, Kwapisz M, Roche V, Bertrand C, Silvain M, Legoix-Né P, Loeillet S, Nicolas A, Thermes C and Morillon A 2011 XUTs are a class of Xrn1-sensitive antisense regulatory non-coding RNA in yeast. Nature 475 114–117

    Article  Google Scholar 

  • Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J and Zhang Q 2012 A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl. Acad. Sci. U S A 109 2654–2659

    Article  CAS  Google Scholar 

  • Flynn RA, Almada AE, Zamudio JR and Sharp PA 2011 Antisense RNA polymerase II divergent transcripts are P-TEFb dependent and substrates for the RNA exosome. Proc. Natl. Acad. Sci. U S A 108 10460–10465

    Article  CAS  Google Scholar 

  • Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, García JA and Paz-Ares J 2007 Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39 1033–1037

    Article  CAS  Google Scholar 

  • Golicz AA, Bhalla PL and Singh MB 2018 lncRNAs in plant and animal sexual reproduction. Trends Plant Sci. 23 195–205

    Article  CAS  Google Scholar 

  • Guttman M, Russell P, Ingolia NT, Weissman JS and Lander ES 2013 Ribosome profiling provides evidence that large noncoding RNAs do not encode proteins. Cell 154 240–251

    Article  CAS  Google Scholar 

  • He X-J, Ma Z-Y and Liu Z-W 2014 Non-coding RNA transcription and RNA-directed DNA methylation in Arabidopsis. Mol. Plant 7 1406–1414

    Article  CAS  Google Scholar 

  • Helliwell CA, Robertson M, Finnegan EJ, Buzas DM and Dennis ES 2011 Vernalization-repression of Arabidopsis FLC requires promoter sequences but not antisense transcripts. PLoS ONE 6 e21513

    Article  CAS  Google Scholar 

  • Heo JB and Sung S 2011 Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331 76–79

    Article  CAS  Google Scholar 

  • Hu H, Wang M, Ding Y, Zhu S, Zhao G, Tu L and Zhang X 2018 Transcriptomic repertoires depict the initiation of lint and fuzz fibres in cotton (Gossypium hirsutum L.). Plant Biotechnol. J. 16 1002–1012

    Article  CAS  Google Scholar 

  • Huang L, Dong H, Zhou D, Li M, Liu Y, Zhang F, Feng Y, Yu D, Lin S and Cao J 2018 Systematic identification of long non-coding RNAs during pollen development and fertilization in Brassica rapa. Plant J. 96 203–222

    Article  CAS  Google Scholar 

  • Irish VF 2010 The flowering of Arabidopsis flower development. Plant J. 61 1014–1028

    Article  CAS  Google Scholar 

  • Jensen TH, Jacquier A and Libri D 2013 Dealing with pervasive transcription. Mol. Cell 52 473–484

    Article  CAS  Google Scholar 

  • Kang C and Liu Z 2015 Global identification and analysis of long non-coding RNAs in diploid strawberry Fragaria vesca during flower and fruit development. BMC Genomics 16 815

    Article  Google Scholar 

  • Khemka N, Singh VK, Garg R and Jain M 2016 Genome-wide analysis of long intergenic non-coding RNAs in chickpea and their potential role in flower development. Sci. Rep. 6 33297

    Article  CAS  Google Scholar 

  • Kim E-D and Sung S 2012 Long noncoding RNA: Unveiling hidden layer of gene regulatory networks. Trends Plant Sci. 17 16–21

    Article  CAS  Google Scholar 

  • Kim J, Yi H, Choi G, Shin B, Song P-S and Choi G 2003 Functional characterization of phytochrome interacting factor 3 in phytochrome-mediated light signal transduction. Plant Cell 15 2399–2407

    Article  CAS  Google Scholar 

  • Kurihara Y, Matsui A, Hanada K, Kawashima M, Ishida J, Morosawa T, Tanaka M, Kaminuma E, Mochizuki Y, Matsushima A, Toyoda T, Shinozaki K and Seki M 2009 Genome-wide suppression of aberrant mRNA-like noncoding RNAs by NMD in Arabidopsis. Proc. Natl. Acad. Sci. USA 106 2453–2458

    Article  CAS  Google Scholar 

  • Li L, Eichten SR, Shimizu R, Petsch K, Yeh C-T, Wu W, Chettoor AM, Givan SA, Cole RA, Fowler JE, Evans MMS, Scanlon MJ, Yu J, Schnable PS, Timmermans MCP, Springer NM and Muelhbaer GJ 2014 Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biol. 15 R40

    Article  Google Scholar 

  • Liu F, Marquardt S, Lister C, Swiezewski S and Dean C 2010 Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327 94–97

    Article  CAS  Google Scholar 

  • Liu J, Jung C, Xu J, Wang H, Deng S, Bernad L, Arenas-Huertero C and Chua N-H 2012 Genome-wide analysis uncovers regulation of long intergenic noncoding RNAs in Arabidopsis. Plant Cell 24 4333–4345

    Article  CAS  Google Scholar 

  • Liu T-T, Zhu D, Chen W, Den W, He H, He G, Bai B, Qi Y, Chen R and Deng XW 2013 A global identification and analysis of small nucleolar RNAs and possible intermediate-sized non-coding RNAs in Oryza sativa. Mol. Plant 6 830–846

    Article  CAS  Google Scholar 

  • Lu T, Zhu C, Lu G, Guo Y, Zhou Y, Zhang Z, Zhao Y, Li W, Lu Y, Tang W, Feng Q and Han B 2012 Strand-specific RNA-seq reveals widespread occurrence of novel cis-natural antisense transcripts in rice. BMC Genomics 13 721

    Article  CAS  Google Scholar 

  • Ma J, Yan B, Qu Y, Qin F, Yang Y, Hao X, Yu J, Zhao Q, Zhu D and Ao G 2008 Zm401, a short-open reading-frame mRNA or noncoding RNA, is essential for tapetum and microspore development and can regulate the floret formation in maize. J. Cell. Biochem. 105 136–146

    Article  CAS  Google Scholar 

  • Meng Y, Shao C, Wang H and Jin Y 2012 Target mimics: An embedded layer of microRNA-involved gene regulatory networks in plants. BMC Genomics 13 197

    Article  CAS  Google Scholar 

  • Morange M 2008 What history tells us. XIV. Regulation of gene expression by non-coding RNAs: The early steps. J. Biosci. 33 327–331

    Article  CAS  Google Scholar 

  • Ntini E, Järvelin AI, Bornholdt J, Chen Y, Boyd M, Jørgensen M, Andersson R, Hoof I, Schein A, Andersen PR, Andersen PK, Precker P, Valen E, Zhao X, Pelenchano V, Steinmetz LM, Sandelin A and Jensen TH 2013 Polyadenylation site-induced decay of upstream transcripts enforces promoter directionality. Nat. Struct. Mol. Biol. 20 923–928

    Article  CAS  Google Scholar 

  • Rinn JL and Chang HY 2012 Genome regulation by long noncoding RNAs. Annu. Rev. Biochem. 81 145–166

    Article  CAS  Google Scholar 

  • Rymarquis LA, Kastenmayer JP, Hüttenhofer AG and Green PJ 2008 Diamonds in the rough: mRNA-like non-coding RNAs. Trends Plant Sci. 13 329–334

    Article  CAS  Google Scholar 

  • Shuai P, Liang D, Tang S, Zhang Z, Ye C-Y, Su Y, Xia X and Yin W 2014 Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. J. Exp. Bot. 65 4975–4983

    Article  CAS  Google Scholar 

  • Singh PK, Ganguli S and Pal A 2018 Functions of long non-coding RNAs in plants: A riddle to explore. Nucleus 61 261–272

    Article  Google Scholar 

  • Song D, Yang Y, Yu B, Zheng B, Deng Z, Lu B-L, Chen X and Jiang T 2009 Computational prediction of novel non-coding RNAs in Arabidopsis thaliana. BMC Bioinf. 10 1–12

    Article  Google Scholar 

  • Song J-H, Cao J-S, Yu X-L and Xiang X 2007 BcMF11, a putative pollen-specific non-coding RNA from Brassica campestris ssp. chinensis. J. Plant Physiol. 164 1097–1100

    Article  CAS  Google Scholar 

  • Song J-H, Cao J-S and Wang C-G 2013 BcMF11, a novel non-coding RNA gene from Brassica campestris, is required for pollen development and male fertility. Plant Cell Rep. 32 21–30

    Article  CAS  Google Scholar 

  • Sousa C, Johansson C, Charon C, Manyani H, Sautter C, Kondorosi A and Crespi M 2001 Translational and structural requirements of the early nodulin gene enod40, a short-open reading frame-containing RNA, for elicitation of a cell-specific growth response in the alfalfa root cortex. Mol. Cell. Biol. 21 354–366

    Article  CAS  Google Scholar 

  • Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ and Dean C 2013 R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340 619–621

    Article  CAS  Google Scholar 

  • Ulitsky I and Bartel DP 2013 lincRNAs: Genomics, evolution, and mechanisms. Cell 154 26–46

    Article  CAS  Google Scholar 

  • Wahba L and Koshland D 2013 The Rs of biology: R-loops and the regulation of regulators. Mol. Cell 50 611–612

    Article  CAS  Google Scholar 

  • Wang L, Mai YX, Zhang YC, Luo Q and Yang H Q 2010 MicroRNA171c-targeted SCL6-II, SCL6-III, and SCL6-IV genes regulate shoot branching in Arabidopsis. Mol. Plant 3 794–806

    Article  Google Scholar 

  • Wang Y, Wang X, Deng W, Fan X, Liu T-T, He G, Chen R, Terzaghi W, Zhu D and Deng XW 2014a Genomic features and regulatory roles of intermediate-sized non-coding RNAs in Arabidopsis. Mol. Plant 7 514–527

    Article  CAS  Google Scholar 

  • Wang Y, Fan X, Lin F, He G, Terzaghi W, Zhu D and Deng XW 2014b Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. Proc. Natl. Acad. Sci. USA 111 10359–10364

    Article  CAS  Google Scholar 

  • Wang H, Chung JP, Liu J, Jang I-C, Kean MJ, Xu J and Chua NH 2014c Genome wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res. 24:444–453

    Article  CAS  Google Scholar 

  • Wang M, Yuan D, Tu L, Gao W, He Y, Hu H, Wang P, Liu N, Lindsey K and Zhang X 2015 Long noncoding RNAs and their proposed functions in fibre development of cotton (Gossypium spp.). New Phytol. 207 1181–1197

    Article  CAS  Google Scholar 

  • Wang C-Y, Liu S-R, Zhang X-Y, Ma Y-J, Hu C-G and Zhang J-Z 2017 Genome-wide screening and characterization of long non-coding RNAs involved in flowering development of trifoliate orange (Poncirus trifoliata L. Raf.). Sci. Rep. 7 43226

    Article  CAS  Google Scholar 

  • Wang M, Zhao W, Gao L and Zhao L 2018 Genome-wide profiling of long non-coding RNAs from tomato and a comparison with mRNAs associated with the regulation of fruit ripening. BMC Plant Biol. 18 75

    Article  Google Scholar 

  • Wen J, Parker BJ and Weiller GF 2007 In silico identification and characterization of mRNA-like noncoding transcripts in Medicago truncatula. In Silico Biol. (Gedrukt) 7 485–505

    CAS  Google Scholar 

  • Wierzbicki AT, Haag JR and Pikaard CS 2008 Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135 635–648

    Article  CAS  Google Scholar 

  • Wu H-J, Wang Z-M, Wang M and Wang X-J 2013 Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol. 161 1875–1884

    Article  CAS  Google Scholar 

  • Xie M, Zhang S and Yu B 2015 microRNA biogenesis, degradation and activity in plants. Cell. Mol. Life Sci. 72 87–99

    Article  CAS  Google Scholar 

  • Xin M, Wang Y, Yao Y, Song N, Hu Z, Qin D, Xie C, Peng H, Ni Z and Sun Q 2011 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. 11 61

    Article  CAS  Google Scholar 

  • Yan J, Gu Y, Jia X, Kang W, Pan S, Tang X, Chen X and Tang G 2012 Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24 415–427

    Article  CAS  Google Scholar 

  • Zhang G, Chen D, Zhang T, Duan A, Zhang J and He C 2018 Transcriptomic and functional analyses unveil the role of long non-coding RNAs in anthocyanin biosynthesis during sea buckthorn fruit ripening. DNA Res. 25 465–476

    Article  CAS  Google Scholar 

  • Zhou H, Liu Q, Li J, Jiang D, Zhou L, Wu P, Lu S, Li F, Liu Z, Chen L, Liu YG and Zhuang C 2012 Photoperiod- and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 22 649–660

    Article  CAS  Google Scholar 

  • Zhou P, Silverstein KA, Gao L, Walton JD, Nallu S, Guhlin J and Young ND 2013 Detecting small plant peptides using SPADA (small peptide alignment discovery application). BMC Bioinf. 14 335

    Article  Google Scholar 

  • Zhu Q-H, Stephen S, Taylor J, Helliwell CA and Wang M-B 2014 Long noncoding RNAs responsive to Fusarium oxysporum infection in Arabidopsis thaliana. New Phytol. 201 574–584

    Article  CAS  Google Scholar 

  • Zhu B, Yang Y, Li R, Fu D, Wen L, Luo Y and Zhu H 2015 RNA sequencing and functional analysis implicate the regulatory role of long non-coding RNAs in tomato fruit ripening. J. Exp. Bot. 66 4483–4495

    Article  CAS  Google Scholar 

  • Zou C, Wang Q, Lu C, Yang W, Zhang Y, Cheng H, Feng X, Prosper MA and Song G 2016 Transcriptome analysis reveals long noncoding RNAs involved in fiber development in cotton (Gossypium arboreum). Sci. China: Life Sci. 59 164–171

    Article  CAS  Google Scholar 

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Acknowledgements

We are thankful to the Department of Botany, University of Calcutta, 35, Ballygunge Circular Road, Kolkata 700019, West Bengal, India and Dr. A. P. J. Abdul Kalam Government College, New Town, Rajarhat, Kolkata 700156, West Bengal, India for necessary support.

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Correspondence to Soumitra Paul.

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Communicated by Manchikatla Venkat Rajam.

Corresponding editor: Manchikatla Venkat Rajam

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Datta, R., Paul, S. Long non-coding RNAs: Fine-tuning the developmental responses in plants. J Biosci 44, 77 (2019). https://doi.org/10.1007/s12038-019-9910-6

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