Plant Molecular Biology

, Volume 80, Issue 1, pp 17–36 | Cite as

MicroRNAs and their diverse functions in plants

Article

Abstract

microRNAs (miRNAs) are an extensive class of newly identified small RNAs, which regulate gene expression at the post-transcriptional level by mRNA cleavage or translation inhibition. Currently, there are 3,070 miRNAs deposited in the public available miRNA database; these miRNAs were obtained from 43 plant species using both computational (comparative genomics) and experimental (direct cloning and deep sequencing) approaches. Like other signaling molecules, plant miRNAs can also be moved from one tissue to another through the vascular system. These mobile miRNAs may play an important role in plant nutrient homeostasis and response to environmental biotic and abiotic stresses. In addition, miRNAs also control a wide range of biological and metabolic processes, including developmental timing, tissue-specific development, and stem cell maintenance and differentiation. Currently, a majority of plant miRNA-related researches are purely descriptive, and provide no further detailed mechanistic insight into miRNA-mediated gene regulation and other functions. To better understand the function and regulatory mechanisms of plant miRNAs, more strategies need to be employed to investigate the functions of miRNAs and their associated signaling pathways and gene networks. Elucidating the evolutionary mechanism of miRNAs is also important. It is possible to develop a novel miRNA-based biotechnology for improving plant yield, quality and tolerance to environmental biotic and abiotic stresses besides focusing on basic genetic studies.

Keywords

microRNAs Gene regulation Identification Evolution Plants Functions Stresses 

Supplementary material

11103_2011_9817_MOESM1_ESM.doc (872 kb)
Supplementary material 1 (DOC 872 kb)

References

  1. Achard P, Herr A, Baulcombe DC, Harberd NP (2004) Modulation of floral development by a gibberellin-regulated microRNA. Development 131:3357–3365PubMedCrossRefGoogle Scholar
  2. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:758–762PubMedCrossRefGoogle Scholar
  3. Addo-Quaye C, Snyder JA, Park YB, Li YF, Sunkar R, Axtell MJ (2009) Sliced microRNA targets and precise loop-first processing of MIR319 hairpins revealed by analysis of the Physcomitrella patens degradome. RNA 15:2112–2121PubMedCrossRefGoogle Scholar
  4. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: an analysis of the cup-shaped cotyledon mutant. Plant Cell 9:841–857PubMedCrossRefGoogle Scholar
  5. Allen E, Xie Z, Gustafson AM, Sung GH, Spatafora JW, Carrington JC (2004) Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36:1282–1290PubMedCrossRefGoogle Scholar
  6. Aprile A, Mastrangelo AM, De Leonardis AM, Galiba G, Roncaglia E, Ferrari F, De Bellis L, Turchi L, Giuliano G, Cattivelli L (2009) Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics 10:279PubMedCrossRefGoogle Scholar
  7. Arazi T, Talmor-Neiman M, Stav R, Riese M, Huijser P, Baulcombe DC (2005) Cloning and characterization of micro-RNAs from moss. Plant J 43:837–848PubMedCrossRefGoogle Scholar
  8. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741PubMedCrossRefGoogle Scholar
  9. Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13:343–349PubMedCrossRefGoogle Scholar
  10. Bartel DP (2007) MicroRNAs: Genomics, biogenesis, mechanism, and function (Reprinted from Cell, vol 116, pg 281–297, 2004). Cell 131:11–29Google Scholar
  11. Billoud B, De Paepe R, Baulcombe D, Boccara M (2005) Identification of new small non-coding RNAs from tobacco and Arabidopsis. Biochimie 87:905–910PubMedCrossRefGoogle Scholar
  12. Bonnet E, He Y, Billiau K, Van de Peer Y (2010) TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics 26:1566–1568PubMedCrossRefGoogle Scholar
  13. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190PubMedCrossRefGoogle Scholar
  14. 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 53:739–749PubMedCrossRefGoogle Scholar
  15. Bushati N, Cohen SM (2007) MicroRNA functions. Annu Rev Cell Dev Biol 23:175–205PubMedCrossRefGoogle Scholar
  16. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, Campilho A, Sebastian J, Bowman JL, Helariutta Y, Benfey PN (2010) Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465:316–321PubMedCrossRefGoogle Scholar
  17. Carthew RW, Sontheimer EJ (2009) Origins and mechanisms of miRNAs and siRNAs. Cell 136:642–655PubMedCrossRefGoogle Scholar
  18. Chen XM (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025PubMedCrossRefGoogle Scholar
  19. Chen XM (2005) microRNA biogenesis and function in plants. FEBS Lett 579:5923–5931PubMedCrossRefGoogle Scholar
  20. Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332PubMedCrossRefGoogle Scholar
  21. Chitwood DH, Timmermans MCP (2010) Small RNAs are on the move. Nature 467:415–419PubMedCrossRefGoogle Scholar
  22. Creighton CJ, Reid JG, Gunaratne PH (2009) Expression profiling of microRNAs by deep sequencing. Brief Bioinform 10:490–497PubMedCrossRefGoogle Scholar
  23. De Felippes FF, Schneeberger K, Dezulian T, Huson DH, Weigel D (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14:2455–2459PubMedCrossRefGoogle Scholar
  24. Dezulian T, Remmert M, Palatnik JF, Weigel D, Huson DH (2006) Identification of plant microRNA homologs. Bioinformatics 22:359–360PubMedCrossRefGoogle Scholar
  25. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445PubMedCrossRefGoogle Scholar
  26. Ding D, Zhang LF, Wang H, Liu ZJ, Zhang ZX, Zheng YL (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38PubMedCrossRefGoogle Scholar
  27. Du TG, Schmid M, Jansen RP (2007) Why cells move messages: the biological functions of mRNA localization. Semin Cell Dev Biol 18:171–177PubMedCrossRefGoogle Scholar
  28. Elbashir SM, Lendeckel W, Tuschl T (2001) RNA interference is mediated by 21-and 22-nucleotide RNAs. Genes Dev 15:188–200PubMedCrossRefGoogle Scholar
  29. Fahlgren N, Howell MD, Kasschau KD, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Law TF, Grant SR, Dangl JL, Carrington JC (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2:e219PubMedCrossRefGoogle Scholar
  30. Fahlgren N, Jogdeo S, Kasschau KD, Sullivan CM, Chapman EJ, Laubinger S, Smith LM, Dasenko M, Givan SA, Weigel D, Carrington JC (2010) MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22:1074–1089PubMedCrossRefGoogle Scholar
  31. Faller M, Guo F (2008) MicroRNA biogenesis: there’s more than one way to skin a cat. Biochim Biophys Acta Gene Regul Mech 1779:663–667CrossRefGoogle Scholar
  32. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9:102–114PubMedCrossRefGoogle Scholar
  33. Floyd SK, Bowman JL (2004) Gene regulation: ancient microRNA target sequences in plants. Nature 428:485–486PubMedCrossRefGoogle Scholar
  34. Frazier TP, Xie FL, Freistaedter A, Burklew CE, Zhang BH (2010) Identification and characterization of microRNAs and their target genes in tobacco (Nicotiana tabacum). Planta 232:1289–1308PubMedCrossRefGoogle Scholar
  35. Frazier TP, Sun GL, Burklew CE, Zhang BH (2011) Salt and drought stresses iInduce the aberrant expression of microRNA genes in tobacco. Mol Biotechnol. doi:10.1007/s12033-011-9387-5 PubMedGoogle Scholar
  36. German MA, Pillay M, Jeong DH, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, De Paoli E, Lu C, Schroth G, Meyers BC, Green PJ (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26:941–946PubMedCrossRefGoogle Scholar
  37. German MA, Luo SJ, Schroth G, Meyers BC, Green PJ (2009) Construction of parallel analysis of RNA ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat Protoc 4:356–362PubMedCrossRefGoogle Scholar
  38. Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276PubMedCrossRefGoogle Scholar
  39. Gregory BD, O’Malley RC, Lister R, Urich MA, Tonti-Filippini J, Chen H, Millar AH, Ecker JR (2008) A link between RNA metabolism and silencing affecting Arabidopsis development. Dev Cell 14:854–866PubMedCrossRefGoogle Scholar
  40. Griffiths-Jones S, Saini HK, van Dongen S, Enright AJ (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res 36:D154–D158PubMedCrossRefGoogle Scholar
  41. Guo L, Lu ZH (2010) The fate of miRNA* strand through evolutionary analysis: implication for degradation as merely carrier strand or potential regulatory molecule? PLoS One 5:e11387PubMedCrossRefGoogle Scholar
  42. 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 17:1376–1386PubMedCrossRefGoogle Scholar
  43. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499PubMedCrossRefGoogle Scholar
  44. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531PubMedCrossRefGoogle Scholar
  45. He SM, Yang Z, Skogerbo G, Ren F, Cui HL, Zhao HT, Chen RS, Zhao Y (2008) The properties and functions of virus encoded microRNA, siRNA, and other small noncoding RNAs. Crit Rev Microbiol 34:175–188PubMedCrossRefGoogle Scholar
  46. Hinas A, Reimegard J, Wagner EG, Nellen W, Ambros VR, Soderbom F (2007) The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res 35:6714–6726PubMedCrossRefGoogle Scholar
  47. Jagadeeswaran G, Saini A, Sunkar R (2009) Biotic and abiotic stress down-regulate miR398 expression in Arabidopsis. Planta 229:1009–1014PubMedCrossRefGoogle Scholar
  48. Jia XY, Wang WX, Ren LG, Chen QJ, Mendu V, Willcut B, Dinkins R, Tang XQ, Tang GL (2009) Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Mol Biol 71:51–59PubMedCrossRefGoogle Scholar
  49. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14:787–799PubMedCrossRefGoogle Scholar
  50. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53PubMedCrossRefGoogle Scholar
  51. Jung JH, Seo PJ, Park CM (2009) MicroRNA biogenesis and function in higher plants. Plant Biotechnol Rep 3:111–126CrossRefGoogle Scholar
  52. Kanehira A, Yamada K, Iwaya T, Tsuwamoto R, Kasai A, Nakazono M, Harada T (2010) Apple phloem cells contain some mRNAs transported over long distances. Tree Genet Genomes 6:635–642CrossRefGoogle Scholar
  53. Kidner CA (2010) The many roles of small RNAs in leaf development. J Genet Genomics 37:13–21PubMedCrossRefGoogle Scholar
  54. Kim M, Canio W, Kessler S, Sinha N (2001) Developmental changes due to long-distance movement of a homeobox fusion transcript in tomato. Science 293:287–289PubMedCrossRefGoogle Scholar
  55. Kim S, Yang JY, Xu J, Jang IC, Prigge MJ, Chua NH (2008) Two cap-binding proteins CBP20 and CBP80 are involved in processing primary MicroRNAs. Plant Cell Physiol 49:1634–1644PubMedCrossRefGoogle Scholar
  56. Kim VN, Han J, Siomi MC (2009) Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol 10:126–139PubMedCrossRefGoogle Scholar
  57. Kreps JA, Wu YJ, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130:2129–2141PubMedCrossRefGoogle Scholar
  58. Kurihara Y, Watanabe Y (2004) Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc Natl Acad Sci USA 101:12753–12758PubMedCrossRefGoogle Scholar
  59. Kurihara Y, Takashi Y, Watanabe Y (2006) The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12:206–212PubMedCrossRefGoogle Scholar
  60. Kurihara Y, Matsui A, Hanada K, Kawashima M, Ishida J, Morosawa T, Tanaka M, Kaminuma E, Mochizuki Y, Matsushima A, Toyoda T, Shinozaki K, Seki M (2009) Genome-wide suppression of aberrant mRNA-like noncoding RNAs by NMD in Arabidopsis. Proc Natl Acad Sci USA 106:2453–2458PubMedCrossRefGoogle Scholar
  61. Kutter C, Schob H, Stadler M, Meins F Jr, Si-Ammour A (2007) MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19:2417–2429PubMedCrossRefGoogle Scholar
  62. Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854PubMedCrossRefGoogle Scholar
  63. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN (2004) MicroRNA genes are transcribed by RNA polymerase II. EMBO J 23:4051–4060PubMedCrossRefGoogle Scholar
  64. Leung AKL, Sharp PA (2010) MicroRNA functions in stress responses. Mol Cell 40:205–215PubMedCrossRefGoogle Scholar
  65. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20PubMedCrossRefGoogle Scholar
  66. Li J, Yang Z, Yu B, Liu J, Chen X (2005) Methylation protects miRNAs and siRNAs from a 3′-end uridylation activity in Arabidopsis. Curr Biol 15:1501–1507PubMedCrossRefGoogle Scholar
  67. Liang G, Yang F, Yu D (2010) MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62:1046–1057PubMedGoogle Scholar
  68. Lin WC, Li SC, Shin JW, Hu SN, Yu XM, Huang TY, Chen SC, Chen HC, Chen SJ, Huang PJ, Gan RR, Chiu CH, Tang P (2009) Identification of microRNA in the protist Trichomonas vaginalis. Genomics 93:487–493PubMedCrossRefGoogle Scholar
  69. Liu B, Li PC, Li X, Liu CY, Cao SY, Chu CC, Cao XF (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 139:296–305PubMedCrossRefGoogle Scholar
  70. Liu PP, Montgomery TA, Fahlgren N, Kasschau KD, Nonogaki H, Carrington JC (2007) Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J 52:133–146PubMedCrossRefGoogle Scholar
  71. Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843PubMedCrossRefGoogle Scholar
  72. Liu QP, Feng Y, Zhu ZJ (2009) Dicer-like (DCL) proteins in plants. Funct Integr Genomics 9:277–286PubMedCrossRefGoogle Scholar
  73. Llave C, Xie Z, Kasschau KD, Carrington JC (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056PubMedCrossRefGoogle Scholar
  74. Lobbes D, Rallapalli G, Schmidt DD, Martin C, Clarke J (2006) SERRATE: a new player on the plant microRNA scene. EMBO Rep 7:1052–1058PubMedCrossRefGoogle Scholar
  75. Lu SF, Sun YH, Shi R, Clark C, Li LG, Chiang VL (2005) Novel and mechanical stress-responsive microRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203PubMedCrossRefGoogle Scholar
  76. Lu C, Kulkarni K, Souret FF, MuthuValliappan R, Tej SS, Poethig RS, Henderson IR, Jacobsen SE, Wang W, Green PJ, Meyers BC (2006) MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res 16:1276–1288PubMedCrossRefGoogle Scholar
  77. Ma ZR, Coruh C, Axtell MJ (2010) Arabidopsis lyrata small RNAs: transient MIRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell 22:1090–1103PubMedCrossRefGoogle Scholar
  78. Mallory A, Vaucheret H (2010) Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22:3879–3889PubMedCrossRefGoogle Scholar
  79. Mallory AC, Dugas DV, Bartel DP, Bartel B (2004) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046PubMedCrossRefGoogle Scholar
  80. Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375PubMedCrossRefGoogle Scholar
  81. Matsui A, Ishida J, Morosawa T, Mochizuki Y, Kaminuma E, Endo TA, Okamoto M, Nambara E, Nakajima M, Kawashima M, Satou M, Kim JM, Kobayashi N, Toyoda T, Shinozaki K, Seki M (2008) Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant Cell Physiol 49:1135–1149PubMedCrossRefGoogle Scholar
  82. Matts J, Jagadeeswaran G, Roe BA, Sunkar R (2010) Identification of microRNAs and their targets in switchgrass, a model biofuel plant species. J Plant Physiol 167:896–904PubMedCrossRefGoogle Scholar
  83. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen XM, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi YJ, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhui JK (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190PubMedCrossRefGoogle Scholar
  84. Millar AA, Waterhouse PM (2005) Plant and animal microRNAs: similarities and differences. Funct Integr Genomics 5:129–135PubMedCrossRefGoogle Scholar
  85. Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126–1129PubMedCrossRefGoogle Scholar
  86. Montgomery TA, Howell MD, Cuperus JT, Li DW, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC (2008) Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133:128–141PubMedCrossRefGoogle Scholar
  87. Moxon S, Schwach F, Dalmay T, MacLean D, Studholme DJ, Moulton V (2008) A toolkit for analysing large-scale plant small RNA datasets. Bioinformatics 24:2252–2253PubMedCrossRefGoogle Scholar
  88. Murchison EP, Hannon GJ (2004) miRNAs on the move: miRNA biogenesis and the RNAi machinery. Curr Opin Cell Biol 16:223–229PubMedCrossRefGoogle Scholar
  89. Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JDG (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439PubMedCrossRefGoogle Scholar
  90. Notaguchi M, Abe M, Kimura T, Daimon Y, Kobayashi T, Yamaguchi A, Tomita Y, Dohi K, Mori M, Araki T (2008) Long-distance, graft-transmissible action of Arabidopsis FLOWERING LOCUS T protein to promote flowering. Plant Cell Physiol 49:1645–1658PubMedCrossRefGoogle Scholar
  91. Palatnik JF, Allen E, Wu XL, Schommer C, Schwab R, Carrington JC, Weigel D (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263PubMedCrossRefGoogle Scholar
  92. Palatnik JF, Wollmann H, Schommer C, Schwab R, Boisbouvier J, Rodriguez R, Warthmann N, Allen E, Dezulian T, Huson D, Carrington JC, Weigel D (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13:115–125PubMedCrossRefGoogle Scholar
  93. Pan X, Zhang B, San Francisco M, Cobb GP (2007) Characterizing viral microRNAs and its application on identifying new microRNAs in viruses. J Cell Physiol 211:10–18PubMedCrossRefGoogle Scholar
  94. Pang MX, Woodward AW, Agarwal V, Guan XY, Ha M, Ramachandran V, Chen XM, Triplett BA, Stelly DM, Chen ZJ (2009) Genome-wide analysis reveals rapid and dynamic changes in miRNA and siRNA sequence and expression during ovule and fiber development in allotetraploid cotton (Gossypium hirsutum L.). Genome Biol 10:R122PubMedCrossRefGoogle Scholar
  95. Pant BD, Buhtz A, Kehr J, Scheible WR (2008) MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738PubMedCrossRefGoogle Scholar
  96. Pantaleo V, Szittya G, Moxon S, Miozzi L, Moulton V, Dalmay T, Burgyan J (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62:960–976PubMedGoogle Scholar
  97. Park W, Li JJ, Song RT, Messing J, Chen XM (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12:1484–1495PubMedCrossRefGoogle Scholar
  98. Park MY, Wu G, Gonzalez-Sulser A, Vaucheret H, Poethig RS (2005) Nuclear processing and export of microRNAs in Arabidopsis. Proc Natl Acad Sci USA 102:3691–3696PubMedCrossRefGoogle Scholar
  99. Pfeffer S, Zavolan M, Grasser FA, Chien MC, Russo JJ, Ju JY, John B, Enright AJ, Marks D, Sander C, Tuschl T (2004) Identification of virus-encoded microRNAs. Science 304:734–736PubMedCrossRefGoogle Scholar
  100. Piriyapongsa J, Jordan IK (2008) Dual coding of siRNAs and miRNAs by plant transposable elements. RNA 14:814–821PubMedCrossRefGoogle Scholar
  101. Ramachandran V, Chen X (2008) Degradation of microRNAs by a family of exoribonucleases in Arabidopsis. Science 321:1490–1492PubMedCrossRefGoogle Scholar
  102. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626PubMedCrossRefGoogle Scholar
  103. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520PubMedCrossRefGoogle Scholar
  104. Rubio-Somoza I, Weigel D (2011) MicroRNA networks and developmental plasticity in plants. Trends Plant Sci 16:258–264PubMedCrossRefGoogle Scholar
  105. Ruiz-Medrano R, Xoconostle-Cazares B, Lucas WJ (1999) Phloem long-distance transport of CmNACP mRNA: implications for supracellular regulation in plants. Development 126:4405–4419PubMedGoogle Scholar
  106. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527PubMedCrossRefGoogle Scholar
  107. Siomi H, Siomi MC (2010) Posttranscriptional regulation of MicroRNA biogenesis in animals. Mol Cell 38:323–332PubMedCrossRefGoogle Scholar
  108. Song L, Han MH, Lesicka J, Fedoroff N (2007) Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body. Proc Natl Acad Sci USA 104:5437–5442PubMedCrossRefGoogle Scholar
  109. Song Q-X, Liu Y-F, Hu X-Y, Zhang W-K, Ma B, Chen S-Y, Zhang J-S (2011) Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol 11:5PubMedCrossRefGoogle Scholar
  110. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019PubMedCrossRefGoogle Scholar
  111. Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17:1397–1411PubMedCrossRefGoogle Scholar
  112. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25PubMedCrossRefGoogle Scholar
  113. Tang GL (2010) Plant microRNAs: an insight into their gene structures and evolution. Semin Cell Dev Biol 21:782–789PubMedCrossRefGoogle Scholar
  114. Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122PubMedCrossRefGoogle Scholar
  115. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687PubMedCrossRefGoogle Scholar
  116. Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17:2204–2216PubMedCrossRefGoogle Scholar
  117. Wei B, Cai T, Zhang R, Li A, Huo N, Li S, Gu YQ, Vogel J, Jia J, Qi Y, Mao L (2009) Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct Integr Genomics 9:499–511PubMedCrossRefGoogle Scholar
  118. Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Development 132:3657–3668PubMedCrossRefGoogle Scholar
  119. Willmann MR, Poethig RS (2007) Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol 10:503–511PubMedCrossRefGoogle Scholar
  120. Xie Z (2010) Piecing the puzzle together: genetic requirements for miRNA biogenesis in Arabidopsis thaliana. Methods Mol Biol 592:1–17PubMedCrossRefGoogle Scholar
  121. Xie F, Zhang B (2010) Target-align: a tool for plant microRNA target identification. Bioinformatics (in press). doi: 10.1093/bioinformatics/btq568
  122. Xie Q, Guo H-S, Dallman G, Fang S, Weissman AM, Chua N-H (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419:167–170PubMedCrossRefGoogle Scholar
  123. Xie ZX, Kasschau KD, Carrington JC (2003) Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation. Curr Biol 13:784–789PubMedCrossRefGoogle Scholar
  124. Xie FL, Huang SQ, Guo K, Xiang AL, Zhu YY, Nie L, Yang ZM (2007) Computational identification of novel microRNAs and targets in Brassica napus. FEBS Lett 581:1464–1474PubMedCrossRefGoogle Scholar
  125. Xoconostle-Cazares B, Yu X, Ruiz-Medrano R, Wang HL, Monzer J, Yoo BC, McFarland KC, Franceschi VR, Lucas WJ (1999) Plant paralog to viral movement protein that potentiates transport of mRNA into the phloem. Science 283:94–98PubMedCrossRefGoogle Scholar
  126. Yu B, Wang H (2010) Translational inhibition by microRNAs in plants. Prog Mol Subcell Biol 50:41–57PubMedCrossRefGoogle Scholar
  127. Yu B, Yang ZY, Li JJ, Minakhina S, Yang MC, Padgett RW, Steward R, Chen XM (2005) Methylation as a crucial step in plant microRNA biogenesis. Science 307:932–935PubMedCrossRefGoogle Scholar
  128. Yu B, Bi L, Zheng BL, Ji LJ, Chevalier D, Agarwal M, Ramachandran V, Li WX, Lagrange T, Walker JC, Chen XM (2008) The FHA domain proteins DAWDLE in Arabidopsis and SNIP1 in humans act in small RNA biogenesis. Proc Natl Acad Sci USA 105:10073–10078PubMedCrossRefGoogle Scholar
  129. Yu HP, Song CN, Jia QD, Wang C, Li F, Nicholas KK, Zhang XY, Fang JG (2011) Computational identification of microRNAs in apple expressed sequence tags and validation of their precise sequences by miR-RACE. Physiol Plant 141:56–70PubMedCrossRefGoogle Scholar
  130. Zeller G, Henz SR, Widmer CK, Sachsenberg T, Ratsch G, Weigel D, Laubinger S (2009) Stress-induced changes in the Arabidopsis thaliana transcriptome analyzed using whole-genome tiling arrays. Plant J 58:1068–1082PubMedCrossRefGoogle Scholar
  131. Zhang YJ (2005) miRU: an automated plant miRNA target prediction server. Nucleic Acids Res 33:W701–W704PubMedCrossRefGoogle Scholar
  132. Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15:336–360PubMedCrossRefGoogle Scholar
  133. Zhang BH, Pan XP, Cobb GP, Anderson TA (2006a) Plant microRNA: a small regulatory molecule with big impact. Dev Biol 289:3–16PubMedCrossRefGoogle Scholar
  134. Zhang BH, Pan XP, Cox SB, Cobb GP, Anderson TA (2006b) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63:246–254PubMedCrossRefGoogle Scholar
  135. Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2006c) Computational identification of microRNAs and their targets. Comput Biol Chem 30:395–407PubMedCrossRefGoogle Scholar
  136. Zhang BH, Wang QL, Pan XP (2007a) MicroRNAs and their regulatory roles in animals and plants. J Cell Physiol 210:279–289PubMedCrossRefGoogle Scholar
  137. Zhang BH, Wang QL, Wang KB, Pan XP, Liu F, Guo TL, Cobb GP, Anderson TA (2007b) Identification of cotton microRNAs and their targets. Gene 397:26–37PubMedCrossRefGoogle Scholar
  138. Zhang JG, Zeng R, Chen JS, Liu X, Liao QS (2008) Identification of conserved microRNAs and their targets from Solanum lycopersicum Mill. Gene 423:1–7PubMedCrossRefGoogle Scholar
  139. Zhang YQ, Chen DL, Tian HF, Zhang BH, Wen JF (2009) Genome-wide computational identification of microRNAs and their targets in the deep-branching eukaryote Giardia lamblia. Comput Biol Chem 33:391–396PubMedCrossRefGoogle Scholar
  140. Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett (in press)Google Scholar
  141. Zhao BT, Liang RQ, Ge LF, Li W, Xiao HS, Lin HX, Ruan KC, Jin YX (2007a) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590PubMedCrossRefGoogle Scholar
  142. Zhao T, Li GL, Mi SJ, Li S, Hannon GJ, Wang XJ, Qi YJ (2007b) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21:1190–1203PubMedCrossRefGoogle Scholar
  143. Zhou M, Gu L, Li P, Song X, Wei L, Chen Z, Cao X (2010) Degradome sequencing reveals endogenous small RNA targets in rice (Oryza sativa L ssp. indica). Front Biol China 5:67–90Google Scholar
  144. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273PubMedCrossRefGoogle Scholar
  145. Zhu JK (2008) Reconstituting plant miRNA biogenesis. Proc Natl Acad Sci USA 105:9851–9852PubMedCrossRefGoogle Scholar
  146. Zhu C, Ding Y, Liu H (2011) MiR398 and plant stress responses. Physiol Plant 143:1–9Google Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of BiologyEast Carolina UniversityGreenvilleUSA

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