1932

Abstract

A large and significant portion of eukaryotic transcriptomes consists of noncoding RNAs (ncRNAs) that have minimal or no protein-coding capacity but are functional. Diverse ncRNAs, including both small RNAs and long ncRNAs (lncRNAs), play essential regulatory roles in almost all biological processes by modulating gene expression at the transcriptional and posttranscriptional levels. In this review, we summarize the current knowledge of plant small RNAs and lncRNAs, with a focus on their biogenesis, modes of action, local and systemic movement, and functions at the nexus of plant development and environmental responses. The complex connections among small RNAs, lncRNAs, and small peptides in plants are also discussed, along with the challenges of identifying and investigating new classes of ncRNAs.

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2019-10-06
2024-06-23
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Literature Cited

  1. Aktaş T, Avşar Ilık I, Maticzka D, Bhardwaj V, Pessoa Rodrigues C et al. 2017. DHX9 suppresses RNA processing defects originating from the Alu invasion of the human genome. Nature 544:115–19
    [Google Scholar]
  2. Ariel F, Romero-Barrios N, Jégu T, Benhamed M, Crespi M 2015. Battles and hijacks: noncoding transcription in plants. Trends Plant Sci 20:362–71
    [Google Scholar]
  3. Arif MA, Fattash I, Ma Z, Cho SH, Beike AK et al. 2012. DICER-LIKE3 activity in Physcomitrella patens DICER-LIKE4 mutants causes severe developmental dysfunction and sterility. Mol. Plant 5:1281–94
    [Google Scholar]
  4. Aukerman MJ, Sakai H. 2003. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15:2730–41
    [Google Scholar]
  5. Axtell MJ, Jan C, Rajagopalan R, Bartel DP 2006. A two-hit trigger for siRNA biogenesis in plants. Cell 127:565–77
    [Google Scholar]
  6. Bai S, Kasai A, Yamada K, Li T, Harada T 2011. A mobile signal transported over a long distance induces systemic transcriptional gene silencing in a grafted partner. J. Exp. Bot. 62:4561–70
    [Google Scholar]
  7. Bardou F, Ariel F, Simpson CG, Romero-Barrios N, Laporte P et al. 2014. Long noncoding RNA modulates alternative splicing regulators in Arabidopsis. Dev. Cell 30:166–76
    [Google Scholar]
  8. Baumberger N, Baulcombe DC. 2005. Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. PNAS 102:11928–33
    [Google Scholar]
  9. Begcy K, Dresselhaus T. 2018. Epigenetic responses to abiotic stresses during reproductive development in cereals. Plant Reprod 31:343–55
    [Google Scholar]
  10. Ben Amor B, Wirth S, Merchan F, Laporte P, d'Aubenton-Carafa Y et al. 2009. Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res 19:57–69
    [Google Scholar]
  11. Benkovics AH, Timmermans MC. 2014. Developmental patterning by gradients of mobile small RNAs. Curr. Opin. Genet. Dev. 27:83–91
    [Google Scholar]
  12. Blevins T, Podicheti R, Mishra V, Marasco M, Wang J et al. 2015. Identification of Pol IV and RDR2-dependent precursors of 24 nt siRNAs guiding de novo DNA methylation in Arabidopsis. eLife 4:e09591
    [Google Scholar]
  13. Böhmdorfer G, Wierzbicki AT. 2015. Control of chromatin structure by long noncoding RNA. Trends Cell Biol 25:623–32
    [Google Scholar]
  14. Bologna NG, Iselin R, Abriata LA, Sarazin A, Pumplin N et al. 2018. Nucleo-cytosolic shuttling of ARGONAUTE1 prompts a revised model of the plant microRNA pathway. Mol. Cell 68:709–19
    [Google Scholar]
  15. Bouyer D, Kramdi A, Kassam M, Heese M, Schnittger A et al. 2017. DNA methylation dynamics during early plant life. Genome Biol 18:179
    [Google Scholar]
  16. Buhtz A, Pieritz J, Springer F, Kehr J 2010. Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64
    [Google Scholar]
  17. Buhtz A, Springer F, Chappell L, Baulcombe DC, Kehr J 2008. Identification and characterization of small RNAs from the phloem of Brassica napus. Plant J 53:739–49
    [Google Scholar]
  18. Cai Q, Liang C, Wang S, Hou Y, Gao L et al. 2018. The disease resistance protein SNC1 represses the biogenesis of microRNAs and phased siRNAs. Nat. Commun. 9:5080
    [Google Scholar]
  19. Calarco J, Borges F, Donoghue MA, Vanex F, Jullien P et al. 2012. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205
    [Google Scholar]
  20. Campalans A, Kondorosi A, 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 16:1047–59
    [Google Scholar]
  21. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S et al. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–21
    [Google Scholar]
  22. Chekanova JA. 2015. Long non-coding RNAs and their functions in plants. Curr. Opin. Plant Biol. 27:207–16
    [Google Scholar]
  23. Chen G, Cui J, Wang L, Zhu Y, Lu Z, Jin B 2017. Genome-wide identification of circular RNAs in Arabidopsis thaliana. Front. Plant Sci 8:1678
    [Google Scholar]
  24. Chen HM, Chen LT, Patel K, Li YH, Baulcombe DC, Wu SH 2010. 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. PNAS 107:15269–74
    [Google Scholar]
  25. Chen L, Ding X, Zhang H, He T, Li Y et al. 2018a. Comparative analysis of circular RNAs between soybean cytoplasmic male-sterile line NJCMS1A and its maintainer NJCMS1B by high-throughput sequencing. BMC Genom 19:663
    [Google Scholar]
  26. Chen L, Zhang P, Fan Y, Lu Q, Li Q et al. 2018b. Circular RNAs mediated by transposons are associated with transcriptomic and phenotypic variation in maize. New Phytol 217:1292–306
    [Google Scholar]
  27. Chen M, Penfield S. 2018. Feedback regulation of COOLAIR expression controls seed dormancy and flowering time. Science 360:1014–17
    [Google Scholar]
  28. Chen X. 2004. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–25
    [Google Scholar]
  29. Chen X. 2009. Small RNAs and their roles in plant development. Annu. Rev. Cell Dev. Biol. 25:21–44
    [Google Scholar]
  30. Chitwood DH, Nogueira FT, Howell MD, Montgomery TA, Carrington JC, Timmermans MC 2009. Pattern formation via small RNA mobility. Genes Dev 23:549–54
    [Google Scholar]
  31. Chitwood DH, Timmermans MCP. 2010. Small RNAs are on the move. Nature 467:415
    [Google Scholar]
  32. Cho SH, Coruh C, Axtell MJ 2012. miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 24:4837–49
    [Google Scholar]
  33. Chu Q, Bai P, Zhu X, Zhang X, Mao L et al. 2018. Characteristics of plant circular RNAs. Brief. Bioinform. https://doi.org/10.1093/bib/bby111
    [Crossref] [Google Scholar]
  34. Conn VM, Hugouvieux V, Nayak A, Conos SA, Capovilla G et al. 2017. A circRNA from SEPALLATA3 regulates splicing of its cognate mRNA through R-loop formation. Nat. Plants 3:17053
    [Google Scholar]
  35. Cuerda-Gil D, Slotkin RK. 2016. Non-canonical RNA-directed DNA methylation. Nat. Plants 2:16163
    [Google Scholar]
  36. Cui J, Luan Y, Jiang N, Bao H, Meng J 2017. Comparative transcriptome analysis between resistant and susceptible tomato allows the identification of lncRNA16397 conferring resistance to Phytophthora infestans by co-expressing glutaredoxin. Plant J 89:577–89
    [Google Scholar]
  37. Curaba J, Talbot M, Li Z, Helliwell C 2013. Over-expression of microRNA171 affects phase transitions and floral meristem determinancy in barley. BMC Plant Biol 13:6
    [Google Scholar]
  38. D'Ario M, Griffiths-Jones S, Kim M 2017. Small RNAs: big impact on plant development. Trends Plant Sci 22:1056–68
    [Google Scholar]
  39. Darbani B, Noeparvar S, Borg S 2016. Identification of circular RNAs from the parental genes involved in multiple aspects of cellular metabolism in barley. Front. Plant Sci. 7:776
    [Google Scholar]
  40. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C 2008. A PHD-polycomb Repressive Complex 2 triggers the epigenetic silencing of FLC during vernalization. PNAS 105:16831–36
    [Google Scholar]
  41. Di C, Yuan J, Wu Y, Li J, Lin H et al. 2014. Characterization of stress-responsive lncRNAs in Arabidopsis thaliana by integrating expression, epigenetic and structural features. Plant J 80:848–61
    [Google Scholar]
  42. Ding B, Itaya A, Zhong X 2005. Viroid trafficking: a small RNA makes a big move. Curr. Opin. Plant Biol. 8:606–12
    [Google Scholar]
  43. Ding J, Lu Q, Ouyang Y, Mao H, Zhang P et al. 2012a. A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. PNAS 109:2654–59
    [Google Scholar]
  44. Ding J, Shen J, Mao H, Xie W, Li X, Zhang Q 2012b. RNA-directed DNA methylation is involved in regulating photoperiod-sensitive male sterility in rice. Mol. Plant 5:1210–16
    [Google Scholar]
  45. Ding Z, Tie W, Fu L, Yan Y, Liu G et al. 2019. Strand-specific RNA-seq based identification and functional prediction of drought-responsive lncRNAs in cassava. BMC Genom 20:214
    [Google Scholar]
  46. Du J, Johnson LM, Jacobsen SE, Patel DJ 2015. DNA methylation pathways and their crosstalk with histone methylation. Nat. Rev. Mol. Cell Biol. 16:519–32
    [Google Scholar]
  47. Du Q, Wang K, Zou C, Xu C, Li WX 2018. The PILNCR1-miR399 regulatory module is important for low phosphate tolerance in maize. Plant Physiol 177:1743–53
    [Google Scholar]
  48. Fan Y, Yang J, Mathioni SM, Yu J, Shen J et al. 2016. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. PNAS 113:15144–49
    [Google Scholar]
  49. Fanale D, Taverna S, Russo A, Bazan V 2018. Circular RNA in exosomes. Adv. Exp. Med. Biol. 1087:109–17
    [Google Scholar]
  50. Fei Q, Li P, Teng C, Meyers BC 2015. Secondary siRNAs from Medicago NB-LRRs modulated via miRNA-target interactions and their abundances. Plant J 83:451–65
    [Google Scholar]
  51. Fei Q, Xia R, Meyers BC 2013. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–15
    [Google Scholar]
  52. Fei Q, Yu Y, Liu L, Zhang Y, Baldrich P et al. 2018. Biogenesis of a 22-nt microRNA in Phaseoleae species by precursor-programmed uridylation. PNAS 115:8037–42
    [Google Scholar]
  53. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI et al. 2007. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39:1033–37
    [Google Scholar]
  54. Garcia-Ruiz H, Takeda A, Chapman EJ, Sullivan CM, Fahlgren N et al. 2010. Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip Mosaic Virus infection. Plant Cell 22:481–96
    [Google Scholar]
  55. Gouil Q, Baulcombe DC. 2018. Paramutation-like features of multiple natural epialleles in tomato. BMC Genom 19:203
    [Google Scholar]
  56. Guo HS, Xie Q, Fei JF, Chua NH 2005. MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell 17:1376–86
    [Google Scholar]
  57. Guo S, Xu Y, Liu H, Mao Z, Zhang C et al. 2013. The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat. Commun 4:1566
    [Google Scholar]
  58. Gursanscky NR, Searle IR, Carroll BJ 2011. Mobile microRNAs hit the target. Traffic 12:1475–82
    [Google Scholar]
  59. Henriques R, Wang H, Liu J, Boix M, Huang LF, Chua NH 2017. The antiphasic regulatory module comprising CDF5 and its antisense RNA FLORE links the circadian clock to photoperiodic flowering. New Phytol 216:854–67
    [Google Scholar]
  60. Hou Y, Zhai Y, Feng L, Karimi HZ, Rutter BD et al. 2018. A Phytophthora effector suppresses trans-kingdom RNAi to promote disease susceptibility. Cell Host Microbe 25:153–65.e5
    [Google Scholar]
  61. Huang J, Wang C, Wang H, Lu P, Zheng B et al. 2019. Meiocyte-specific and AtSPO11-1-dependent small RNAs and their association with meiotic gene expression and recombination. Plant Cell 31:444–64
    [Google Scholar]
  62. Ibarra CA, Feng X, Schoft VK, Hsieh T-F, Uzawa R et al. 2012. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:1360–64
    [Google Scholar]
  63. Ito H, Gaubert H, Bucher E, Mirouze M, Vaillant I, Paszkowski J 2011. An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress. Nature 472:115
    [Google Scholar]
  64. Jabnoune M, Secco D, Lecampion C, Robaglia C, Shu Q, Poirier Y 2013. A rice cis-natural antisense RNA acts as a translational enhancer for its cognate mRNA and contributes to phosphate homeostasis and plant fitness. Plant Cell 25:4166–82
    [Google Scholar]
  65. Jiang N, Cui J, Shi Y, Yang G, Zhou X et al. 2019. Tomato lncRNA23468 functions as a competing endogenous RNA to modulate NBS-LRR genes by decoying miR482b in the tomato–Phytophthora infestans interaction. Hortic. Res. 6:28
    [Google Scholar]
  66. Jullien PE, Susaki D, Yelagandula R, Higashiyama T, Berger F 2012. DNA methylation dynamics during sexual reproduction in Arabidopsis thaliana. Curr. Biol 22:1825–30
    [Google Scholar]
  67. Kakrana A, Mathioni SM, Huang K, Hammond R, Vandivier L et al. 2018. Plant 24-nt reproductive phasiRNAs from intramolecular duplex mRNAs in diverse monocots. Genome Res 28:1333–44
    [Google Scholar]
  68. Khan GA, Bouraine S, Wege S, Li Y, de Carbonnel M et al. 2014. Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1;H3 in Arabidopsis. J. Exp. Bot 65:871–84
    [Google Scholar]
  69. Kim DH, Sung S. 2013. Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis. Plant Cell 25:454–69
    [Google Scholar]
  70. Kindgren P, Ard R, Ivanov M, Marquardt S 2018. Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation. Nat. Commun. 9:4561
    [Google Scholar]
  71. Kiss T. 2002. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 109:145–48
    [Google Scholar]
  72. Knauer S, Holt AL, Rubio-Somoza I, Tucker EJ, Hinze A et al. 2013. A protodermal miR394 signal defines a region of stem cell competence in the Arabidopsis shoot meristem. Dev. Cell 24:125–32
    [Google Scholar]
  73. Komiya R, Ohyanagi H, Niihama M, Watanabe T, Nakano M et al. 2014. Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J 78:385–97
    [Google Scholar]
  74. Lai X, Bazin J, Webb S, Crespi M, Zubieta C, Conn SJ 2018. CircRNAs in plants. Adv. Exp. Med. Biol. 1087:329–43
    [Google Scholar]
  75. Laporte P, Satiat-Jeunemaitre B, Velasco I, Csorba T, Van de Velde W et al. 2010. A novel RNA-binding peptide regulates the establishment of the Medicago truncatulaSinorhizobium meliloti nitrogen-fixing symbiosis. Plant J 62:24–38
    [Google Scholar]
  76. Lauressergues D, Couzigou JM, Clemente HS, Martinez Y, Dunand C et al. 2015. Primary transcripts of microRNAs encode regulatory peptides. Nature 520:90–93
    [Google Scholar]
  77. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11:204–20
    [Google Scholar]
  78. Lewsey MG, Hardcastle TJ, Melnyk CW, Molnar A, Valli A et al. 2016. Mobile small RNAs regulate genome-wide DNA methylation. PNAS 113:E801–10
    [Google Scholar]
  79. Li F, Orban R, Baker B 2012. SoMART: a web server for plant miRNA, tasiRNA and target gene analysis. Plant J 70:891–901
    [Google Scholar]
  80. Li J, Guo G, Guo W, Guo G, Tong D et al. 2012. miRNA164-directed cleavage of ZmNAC1 confers lateral root development in maize (Zea mays L.). BMC Plant Biol 12:220
    [Google Scholar]
  81. Li Q, Gent JI, Zynda G, Song J, Makarevitch I et al. 2015. RNA-directed DNA methylation enforces boundaries between heterochromatin and euchromatin in the maize genome. PNAS 112:14728–33
    [Google Scholar]
  82. Li S, He Y. 2014. HEAT-INDUCED TAS1 TARGET1 mediates thermotolerance via HEAT STRESS TRANSCRIPTION FACTOR A1a–directed pathways in Arabidopsis. Plant Cell 26:1764–80
    [Google Scholar]
  83. Li S, Le B, Ma X, Li S, You C et al. 2016. Biogenesis of phased siRNAs on membrane-bound polysomes in Arabidopsis. eLife 5:e22750
    [Google Scholar]
  84. Li S, Liu L, Zhuang X, Yu Y, Liu X et al. 2013. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153:562–74
    [Google Scholar]
  85. Li S, Vandivier LE, Tu B, Gao L, Won SY et al. 2015. Detection of Pol IV/RDR2-dependent transcripts at the genomic scale in Arabidopsis reveals features and regulation of siRNA biogenesis. Genome Res 25:235–45
    [Google Scholar]
  86. Li X, Yang L, Chen LL 2018. The biogenesis, functions, and challenges of circular RNAs. Mol. Cell 71:428–42
    [Google Scholar]
  87. Lin SI, Chiang SF, Lin WY, Chen JW, Tseng CY et al. 2008. Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol 147:732–46
    [Google Scholar]
  88. Liu J, Wang H, Chua NH 2015. Long noncoding RNA transcriptome of plants. Plant Biotechnol. J. 13:319–28
    [Google Scholar]
  89. Liu Q, Yao X, Pi L, Wang H, Cui X, Huang H 2009. The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J 58:27–40
    [Google Scholar]
  90. Lloyd JP, Tsai ZT-Y, Sowers RP, Panchy NL, Shiu S-H 2018. A model-based approach for identifying functional intergenic transcribed regions and noncoding RNAs. Mol. Biol. Evol. 35:1422–36
    [Google Scholar]
  91. Lu T, Cui L, Zhou Y, Zhu C, Fan D et al. 2015. Transcriptome-wide investigation of circular RNAs in rice. RNA 21:2076–87
    [Google Scholar]
  92. Luo QJ, Mittal A, Jia F, Rock CDR 2012. An autoregulatory feedback loop involving PAP1 and TAS4 in response to sugars in Arabidopsis. Plant Mol. Biol 80:117–29
    [Google Scholar]
  93. Marquardt S, Raitskin O, Wu Z, Liu F, Sun Q, Dean C 2014. Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol. Cell 54:156–65
    [Google Scholar]
  94. Martinez G, Köhler C. 2017. Role of small RNAs in epigenetic reprogramming during plant sexual reproduction. Curr. Opin. Plant Biol. 36:22–28
    [Google Scholar]
  95. Martínez G, Panda K, Köhler C, Slotkin RK 2016. Silencing in sperm cells is directed by RNA movement from the surrounding nurse cell. Nat. Plants 2:16030
    [Google Scholar]
  96. Martinez G, Wolff P, Wang Z, Moreno-Romero J, Santos-Gonzalez J et al. 2018. Paternal easiRNAs regulate parental genome dosage in Arabidopsis. Nat. Genet 50:193–98
    [Google Scholar]
  97. Matsumoto A, Nakayama KI. 2018. Hidden peptides encoded by putative noncoding RNAs. Cell Struct. Funct. 43:75–83
    [Google Scholar]
  98. Matzke MA, Kanno T, Matzke AJ 2015. RNA-directed DNA methylation: the evolution of a complex epigenetic pathway in flowering plants. Annu. Rev. Plant Biol. 66:243–67
    [Google Scholar]
  99. Melnyk CW, Molnar A, Bassett A, Baulcombe DC 2011a. Mobile 24 nt small RNAs direct transcriptional gene silencing in the root meristems of Arabidopsis thaliana. Curr. Biol 21:1678–83
    [Google Scholar]
  100. Melnyk CW, Molnar A, Baulcombe DC 2011b. Intercellular and systemic movement of RNA silencing signals. EMBO J 30:3553–63
    [Google Scholar]
  101. Miyashima S, Koi S, Hashimoto T, Nakajima K 2011. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138:2303–13
    [Google Scholar]
  102. Nejat N, Mantri N. 2018. Emerging roles of long non-coding RNAs in plant response to biotic and abiotic stresses. Crit. Rev. Biotechnol. 38:93–105
    [Google Scholar]
  103. Ono S, Liu H, Tsuda K, Fukai E, Tanaka K et al. 2018. EAT1 transcription factor, a non-cell-autonomous regulator of pollen production, activates meiotic small RNA biogenesis in rice anther tapetum. PLOS Genet 14:e1007238
    [Google Scholar]
  104. Pamudurti NR, Bartok O, Jens M, Ashwal-Fluss R, Stottmeister C et al. 2017. Translation of circRNAs. Mol. Cell 66:9–21.e7
    [Google Scholar]
  105. Pan T, Sun X, Liu Y, Li H, Deng G et al. 2018. Heat stress alters genome-wide profiles of circular RNAs in Arabidopsis. Plant Mol. Biol 96:217–29
    [Google Scholar]
  106. Pang J, Zhang X, Ma X, Zhao J 2019. Spatio-temporal transcriptional dynamics of maize long non-coding RNAs responsive to drought stress. Genes 10:138
    [Google Scholar]
  107. Pant BD, Buhtz A, Kehr J, Scheible WR 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–38
    [Google Scholar]
  108. Patel P, Mathioni S, Kakrana A, Shatkay H, Meyers BC 2018. Reproductive phasiRNAs in grasses are compositionally distinct from other classes of small RNAs. New Phytol 220:851–64
    [Google Scholar]
  109. Pauli A, Rinn JL, Schier AF 2011. Non-coding RNAs as regulators of embryogenesis. Nat. Rev. Genet. 12:136
    [Google Scholar]
  110. Plaza S, Menschaert G, Payre F 2017. In search of lost small peptides. Annu. Rev. Cell Dev. Biol. 33:391–416
    [Google Scholar]
  111. Qi X, Xie S, Liu Y, Yi F, Yu J 2013. Genome-wide annotation of genes and noncoding RNAs of foxtail millet in response to simulated drought stress by deep sequencing. Plant Mol. Biol. 83:459–73
    [Google Scholar]
  112. Qin T, Zhao H, Cui P, Albesher N, Xiong L 2017. A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance. Plant Physiol 175:1321–36
    [Google Scholar]
  113. Rai MI, Alam M, Lightfoot DA, Gurha P, Afzal AJ 2018. Classification and experimental identification of plant long non-coding RNAs. Genomics In press. https://doi.org/10.1016/j.ygeno.2018.04.014
    [Crossref] [Google Scholar]
  114. Rogers K, Chen X. 2013. Biogenesis, turnover, and mode of action of plant microRNAs. Plant Cell 25:2383–99
    [Google Scholar]
  115. Rohrig H, Schmidt J, Miklashevichs E, Schell J, John M 2002. Soybean ENOD40 encodes two peptides that bind to sucrose synthase. PNAS 99:1915–20
    [Google Scholar]
  116. Sanei M, Chen X. 2015. Mechanisms of microRNA turnover. Curr. Opin. Plant Biol. 27:199–206
    [Google Scholar]
  117. Seo JS, Sun HX, Park BS, Huang CH, Yeh SD et al. 2017. ELF18-INDUCED LONG-NONCODING RNA associates with mediator to enhance expression of innate immune response genes in Arabidopsis. Plant Cell 29:1024–38
    [Google Scholar]
  118. Shivaprasad PV, Dunn RM, Santos BACM, Bassett A, Baulcombe DC 2014. Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J 31:257–66
    [Google Scholar]
  119. Silva GFF, Silva EM, Correa JPO, Vicente MH, Jiang N et al. 2018. Tomato floral induction and flower development are orchestrated by the interplay between gibberellin and two unrelated microRNA-controlled modules. New Phytol 221:1328–44
    [Google Scholar]
  120. Skopelitis DS, Hill K, Klesen S, Marco CF, von Born P et al. 2018. Gating of miRNA movement at defined cell-cell interfaces governs their impact as positional signals. Nat. Commun. 9:3107
    [Google Scholar]
  121. Slotkin RK, Vaughn M, Borges F, Tanurdzić M, Becker JD et al. 2009. Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–72
    [Google Scholar]
  122. Song Q, Zhang T, Stelly DM, Chen ZJ 2017. Epigenomic and functional analyses reveal roles of epialleles in the loss of photoperiod sensitivity during domestication of allotetraploid cottons. Genome Biol 18:99
    [Google Scholar]
  123. Song Y, Xuan A, Bu C, Ci D, Tian M, Zhang D 2018. Osmotic stress-responsive promoter upstream transcripts (PROMPTs) act as carriers of MYB transcription factors to induce the expression of target genes in Populus simonii. Plant Biotechnol. J 17:164–77
    [Google Scholar]
  124. Sousa C, Johansson C, Charon C, Manyani H, Sautter C et al. 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. 21:354–66
    [Google Scholar]
  125. Sun Q, Liu X, Yang J, Liu W, Du Q et al. 2018. microRNA528 affects lodging resistance of maize by regulating lignin biosynthesis under nitrogen-luxury conditions. Mol. Plant 11:806–14
    [Google Scholar]
  126. Sung S, Amasino RM. 2004. Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–64
    [Google Scholar]
  127. Tamiru M, Hardcastle TJ, Lewsey MG 2018. Regulation of genome-wide DNA methylation by mobile small RNAs. New Phytol 217:540–46
    [Google Scholar]
  128. Tan J, Zhou Z, Niu Y, Sun X, Deng Z 2017. Identification and functional characterization of tomato circRNAs derived from genes involved in fruit pigment accumulation. Sci. Rep. 7:8594
    [Google Scholar]
  129. Tang B, Hao Z, Zhu Y, Zhang H, Li G 2018. Genome-wide identification and functional analysis of circRNAs in Zea mays. PLOS ONE 13:e0202375
    [Google Scholar]
  130. Tang J, Chu C. 2017. MicroRNAs in crop improvement: fine-tuners for complex traits. Nat. Plants 3:17077
    [Google Scholar]
  131. Todesco M, Rubio-Somoza I, Paz-Ares J, Weigel D 2010. A collection of target mimics for comprehensive analysis of microRNA function in Arabidopsis thaliana. PLOS Genet 6:e1001031
    [Google Scholar]
  132. Tsikou D, Yan Z, Holt DB, Abel NB, Reid DE et al. 2018. Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA. Science 362:233–36
    [Google Scholar]
  133. Tu B, Liu L, Xu C, Zhai J, Li S et al. 2015. Distinct and cooperative activities of HESO1 and URT1 nucleotidyl transferases in microRNA turnover in Arabidopsis. PLOS Genet 11:e1005119
    [Google Scholar]
  134. Ulitsky I, Bartel DP. 2013. lincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46
    [Google Scholar]
  135. Wang A, Hu J, Gao C, Chen G, Wang B et al. 2019. Genome-wide analysis of long non-coding RNAs unveils the regulatory roles in the heat tolerance of Chinese cabbage (Brassica rapa ssp. chinensis). Sci. Rep. 9:5002
    [Google Scholar]
  136. Wang H, Chung PJ, Liu J, Jang IC, Kean MJ et al. 2014. Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24:444–53
    [Google Scholar]
  137. Wang H, Jiao X, Kong X, Humaira S, Wu Y et al. 2016. A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol 170:2365–77
    [Google Scholar]
  138. Wang J. 2014. Regulation of flowering time by the miR156-mediated age pathway. J. Exp. Bot. 65:4723–30
    [Google Scholar]
  139. Wang J, Yu W, Yang Y, Li X, Chen T et al. 2015. Genome-wide analysis of tomato long non-coding RNAs and identification as endogenous target mimic for microRNA in response to TYLCV infection. Sci. Rep. 5:16946
    [Google Scholar]
  140. Wang J, Zhou L, Shi H, Chern M, Yu H et al. 2018. A single transcription factor promotes both yield and immunity in rice. Science 361:1026–28
    [Google Scholar]
  141. Wang JW, Czech B, Weigel D 2009. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138:738–49
    [Google Scholar]
  142. Wang P, Dai L, Ai J, Wang Y, Ren F 2019. Identification and functional prediction of cold-related long non-coding RNA (lncRNA) in grapevine. Sci. Rep. 9:6638
    [Google Scholar]
  143. Wang TZ, Liu M, Zhao MG, Chen R, Zhang WH 2015. Identification and characterization of long non-coding RNAs involved in osmotic and salt stress in Medicago truncatula using genome-wide high-throughput sequencing. BMC Plant Biol 15:131
    [Google Scholar]
  144. Wang Y, Ding B. 2010. Viroids: small probes for exploring the vast universe of RNA trafficking in plants. J. Integr. Plant Biol. 52:28–39
    [Google Scholar]
  145. Wang Y, Fan X, Lin F, He G, Terzaghi W et al. 2014. Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. PNAS 111:10359–64
    [Google Scholar]
  146. Wang Y, Luo X, Sun F, Hu J, Zha X et al. 2018. Overexpressing lncRNA LAIR increases grain yield and regulates neighbouring gene cluster expression in rice. Nat. Commun. 9:3516
    [Google Scholar]
  147. Wang Y, Yang M, Wei S, Qin F, Zhao H, Suo B 2016. Identification of circular RNAs and their targets in leaves of Triticum aestivum L. under dehydration stress. Front. Plant Sci. 7:2024
    [Google Scholar]
  148. Wang Z, Liu Y, Li D, Li L, Zhang Q et al. 2017. Identification of circular RNAs in kiwifruit and their species-specific response to bacterial canker pathogen invasion. Front. Plant Sci. 8:413
    [Google Scholar]
  149. Whittaker C, Dean C. 2017. The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu. Rev. Cell Dev. Biol. 33:555–75
    [Google Scholar]
  150. Wierzbicki AT, Haag JR, Pikaard CS 2008. Noncoding transcription by RNA polymerase Pol IVb/Pol V mediates transcriptional silencing of overlapping and adjacent genes. Cell 135:635–48
    [Google Scholar]
  151. Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750–59
    [Google Scholar]
  152. Wu H, Yang L, Chen LL 2017. The diversity of long noncoding RNAs and their generation. Trends Genet 33:540–52
    [Google Scholar]
  153. Wu HJ, Wang ZM, Wang M, Wang XJ 2013. Widespread long noncoding RNAs as endogenous target mimics for microRNAs in plants. Plant Physiol 161:1875–84
    [Google Scholar]
  154. Xia R, Meyers BC, Liu Z, Beers EP, Ye S, Liu Z 2013. MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA biogenesis in eudicots. Plant Cell 25:1555–72
    [Google Scholar]
  155. Xia R, Xu J, Meyers BC 2016. The emergence, evolution, and diversification of the miR390-TAS3-ARF pathway in land plants. Plant Cell 29:1232–47
    [Google Scholar]
  156. Xiang L, Cai C, Cheng J, Wang L, Wu C et al. 2018. Identification of circularRNAs and their targets in Gossypium under Verticillium wilt stress based on RNA-seq. PeerJ 6:e4500
    [Google Scholar]
  157. Xin M, Wang Y, Yao Y, Song N, Hu Z et al. 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
    [Google Scholar]
  158. Xing Q, Zhang W, Liu M, Li L, Li X et al. 2019. Genome-wide identification of long non-coding RNAs responsive to Lasiodiplodia theobromae infection in grapevine. Evol. Bioinform. Online 15:1176934319841362
    [Google Scholar]
  159. Yan J, Gu Y, Jia X, Kang W, Pan S et al. 2012. Effective small RNA destruction by the expression of a short tandem target mimic in Arabidopsis. Plant Cell 24:415–27
    [Google Scholar]
  160. Yang L, Froberg JE, Lee JT 2014. Long noncoding RNAs: fresh perspectives into the RNA world. Trends Biochem. Sci. 39:35–43
    [Google Scholar]
  161. Yang Y, Zhou Y, Zhang Y, Chen Y 2018. Grass phasiRNAs and male fertility. Sci. China Life Sci. 61:1–7
    [Google Scholar]
  162. Ye CY, Chen L, Liu C, Zhu QH, Fan L 2015. Widespread noncoding circular RNAs in plants. New Phytol 208:88–95
    [Google Scholar]
  163. Ye CY, Zhang X, Chu Q, Liu C, Yu Y et al. 2017. Full-length sequence assembly reveals circular RNAs with diverse non-GT/AG splicing signals in rice. RNA Biol 14:1055–63
    [Google Scholar]
  164. Yin H, Zhang X, Zhang B, Luo H, He C 2019. Revealing the dominant long noncoding RNAs responding to the infection with Colletotrichum gloeosporioides in Hevea brasiliensis. Biol. Direct 14:7
    [Google Scholar]
  165. Yoo BC, Kragler F, Varkonyi-Gasic E, Haywood V, Archer-Evans S et al. 2004. A systemic small RNA signaling system in plants. Plant Cell 16:1979–2000
    [Google Scholar]
  166. Yu Y, Jia T, Chen X 2017. The ‘how’ and ‘where’ of plant microRNAs. New Phytol 216:1002–17
    [Google Scholar]
  167. Yu Y, Zhou Y, Zhang Y, Chen Y 2018. Grass phasiRNAs and male fertility. Sci. China Life Sci. 61:148–54
    [Google Scholar]
  168. Zhai J, Bischof S, Wang H, Feng S, Lee T-F et al. 2015a. A one precursor one siRNA model for Pol IV–dependent siRNA biogenesis. Cell 163:445–55
    [Google Scholar]
  169. Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD et al. 2011. MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–53
    [Google Scholar]
  170. Zhai J, Zhang H, Arikit S, Huang K, Nan G-L et al. 2015b. Spatiotemporally dynamic, cell-type–dependent premeiotic and meiotic phasiRNAs in maize anthers. PNAS 112:3146–51
    [Google Scholar]
  171. Zhang C, Li G, Wang J, Fang J 2012. Identification of trans-acting siRNAs and their regulatory cascades in grapevine. Bioinformatics 28:2561–68
    [Google Scholar]
  172. Zhang G, Duan A, Zhang J, He C 2017. Genome-wide analysis of long non-coding RNAs at the mature stage of sea buckthorn (Hippophae rhamnoides Linn) fruit. Gene 596:130–36
    [Google Scholar]
  173. Zhang H, Chen X, Wang C, Xu Z, Wang Y et al. 2013. Long non-coding genes implicated in response to stripe rust pathogen stress in wheat (Triticum aestivum L.). Mol. Biol. Rep. 40:6245–53
    [Google Scholar]
  174. Zhang L, Yao L, Zhang N, Yang J, Zhu X et al. 2018. Lateral root development in potato is mediated by Stu-mi164 regulation of NAC transcription factor. Front. Plant Sci. 9:383
    [Google Scholar]
  175. Zhang W, Han Z, Guo Q, Liu Y, Zheng Y et al. 2014. Identification of maize long non-coding RNAs responsive to drought stress. PLOS ONE 9:e98958
    [Google Scholar]
  176. Zhang XO, Wang HB, Zhang Y, Lu X, Chen LL, Yang L 2014. Complementary sequence–mediated exon circularization. Cell 159:134–47
    [Google Scholar]
  177. Zhang YC, Chen YQ. 2013. Long noncoding RNAs: new regulators in plant development. Biochem. Biophys. Res. Commun. 436:111–14
    [Google Scholar]
  178. Zhang YC, Liao JY, Li ZY, Yu Y, Zhang JP et al. 2014. Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol 15:512
    [Google Scholar]
  179. Zhang Z, Zheng Y, Ham BK, Zhang S, Fei Z, Lucas WJ 2019. Plant lncRNAs are enriched in and move systemically through the phloem in response to phosphate deficiency. J. Integr. Plant Biol. 61:492–508
    [Google Scholar]
  180. Zhao T, Wang L, Li S, Xu M, Guan X, Zhou B 2017. Characterization of conserved circular RNA in polyploid Gossypium species and their ancestors. FEBS Lett 591:3660–69
    [Google Scholar]
  181. Zhao W, Cheng Y, Zhang C, You Q, Shen X et al. 2017. Genome-wide identification and characterization of circular RNAs by high throughput sequencing in soybean. Sci. Rep. 7:5636
    [Google Scholar]
  182. Zhao X, Li J, Lian B, Gu H, Li Y, Qi Y 2018. Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA. Nat. Commun. 9:5056
    [Google Scholar]
  183. Zhou M, Palanca AMS, Law JA 2018. Locus-specific control of the de novo DNA methylation pathway in Arabidopsis by the CLASSY family. Nat. Genet. 50:865–73
    [Google Scholar]
  184. Zhu QH, Stephen S, Taylor J, Helliwell CA, Wang MB 2014. Long noncoding RNAs responsive to Fusarium oxysporum infection in Arabidopsis thaliana. New Phytol 201:574–84
    [Google Scholar]
  185. Zuo J, Wang Q, Han C, Ju Z, Cao D et al. 2017. SRNAome and degradome sequencing analysis reveals specific regulation of sRNA in response to chilling injury in tomato fruit. Physiol. Plant 160:142–54
    [Google Scholar]
  186. Zuo J, Wang Q, Zhu B, Luo Y, Gao L 2016. Deciphering the roles of circRNAs on chilling injury in tomato. Biochem. Biophys. Res. Commun. 479:132–38
    [Google Scholar]
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