Plant Molecular Biology

, Volume 80, Issue 1, pp 3–16 | Cite as

Conservation and divergence in plant microRNAs

  • Matthew W. Jones-RhoadesEmail author


MicroRNAs (miRNAs) are a class of small, non-coding RNAs that regulate gene expression in eukaryotic cells. The past decade has seen an explosion in our understanding of the sets of miRNA genes encoded in the genomes in different species of plants and the mechanisms by which miRNAs interact with target RNAs. A subset of miRNA families (and their binding sites in target RNAs) are conserved between angiosperms and basal plants, suggesting they predate the divergence of existing lineages of plants. However, the majority of miRNA families expressed by any given plant species have a narrow phylogenetic distribution. As a group, these “young” miRNAs genes appear to be evolutionarily fluid and lack clearly understood biological function. The goal of this review is to summarize our understanding of the sets of miRNA genes and miRNA targets that exist in various plant species and to discuss hypotheses that explain the patterns of conservation and divergence observed among microRNAs in plants.


Plants MicroRNAs Evolution Conservation 


  1. Adai A, Johnson C, Mlotshwa S et al (2005) Computational prediction of miRNAs in Arabidopsis thaliana. Genome Res 15(1):78–91PubMedCrossRefGoogle Scholar
  2. Addo-Quaye C, Eshoo T, Bartel D, Axtell M (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:1–5CrossRefGoogle 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(12):2112–2121PubMedCrossRefGoogle Scholar
  4. Allen E, Howell MD (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin Cell Dev Biol 21:798–804PubMedCrossRefGoogle 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(12):1282–1290PubMedCrossRefGoogle Scholar
  6. Allen E, Xie Z, Gustafson AM, Carrington JC (2005) MicroRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121(2):207–221PubMedCrossRefGoogle Scholar
  7. Ambros V, Bartel B, Bartel DP et al (2003) A uniform system for microRNA annotation. RNA 9(3):277–279PubMedCrossRefGoogle 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(11):2730–2741PubMedCrossRefGoogle Scholar
  9. Axtell MJ (2008) Evolution of microRNAs and their targets: are all microRNAs biologically relevant? Biochim Biophys Acta 1779(11):725–734PubMedCrossRefGoogle Scholar
  10. Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17(6):1658–1673PubMedCrossRefGoogle Scholar
  11. Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13(7):343–349PubMedCrossRefGoogle Scholar
  12. Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19(6):1750–1769PubMedCrossRefGoogle Scholar
  13. Baker CC, Sieber P, Wellmer F, Meyerowitz EM (2005) The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr Biol 15(4):303–315PubMedCrossRefGoogle Scholar
  14. Barakat A, Wall K, Leebens-Mack J, Wang YJ, Carlson JE, Depamphilis CW (2007) Large-scale identification of microRNAs from a basal eudicot (Eschscholzia californica) and conservation in flowering plants. Plant J 51(6):991–1003PubMedCrossRefGoogle Scholar
  15. Bartel D (2009) MicroRNAs: target recognition and regulatory functions. Cell 136(2):215–233PubMedCrossRefGoogle Scholar
  16. Beauclair L, Yu A, Bouche N (2010) MicroRNA-directed cleavage and translational repression of the copper chaperone for superoxide dismutase mRNA in Arabidopsis. Plant J 62(3):454–462PubMedCrossRefGoogle Scholar
  17. Braun L, Cannella D, Ortet P et al (2010) A complex small RNA repertoire is generated by a plant/fungal-like machinery and effected by a metazoan-like Argonaute in the single-cell human parasite Toxoplasma gondii. PLoS Pathog 6(5):e1000920PubMedCrossRefGoogle Scholar
  18. Brodersen P, Voinnet O (2009) Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 10(2):141–148PubMedCrossRefGoogle Scholar
  19. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320(5880):1185–1190PubMedCrossRefGoogle Scholar
  20. Cerutti H, Casas-Mollano J (2006) On the origin and functions of RNA-mediated silencing: from protists to man. Curr Genet 50(2):81–99PubMedCrossRefGoogle Scholar
  21. Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8(11):884–896PubMedCrossRefGoogle Scholar
  22. Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303(5666):2022–2025PubMedCrossRefGoogle Scholar
  23. Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44PubMedCrossRefGoogle Scholar
  24. Cock J, Sterck L, Rouze P et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465(7298):617–621PubMedCrossRefGoogle Scholar
  25. Dugas D, Bartel B (2008) Sucrose induction of Arabidopsis miR398 represses two Cu/Zn superoxide dismutases. Plant Mol Biol 67:403–417PubMedCrossRefGoogle Scholar
  26. Ehrenreich IM, Purugganan MD (2008) Sequence variation of MicroRNAs and their binding sites in Arabidopsis. Plant Physiol 146(4):1974–1982PubMedCrossRefGoogle Scholar
  27. Fahlgren N, Howell MD, Kasschau KD et al (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS One 2(2):e219PubMedCrossRefGoogle Scholar
  28. Fahlgren N, Jogdeo S, Kasschau KD et al (2010) MicroRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22(4):1074–1089PubMedCrossRefGoogle Scholar
  29. Felippes FF, Schneeberger K, Dezulian T, Huson DH, Weigel D (2008) Evolution of Arabidopsis thaliana microRNAs from random sequences. RNA 14(12):2455–2459PubMedCrossRefGoogle Scholar
  30. Finet C, Timme R, Delwiche C, Marletaz F (2010) Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Curr Biol 20(24):2217–2222PubMedCrossRefGoogle Scholar
  31. Floyd SK, Bowman JL (2004) Gene regulation: ancient microRNA target sequences in plants. Nature 428(6982):485–486PubMedCrossRefGoogle Scholar
  32. Floyd SK, Zalewski CS, Bowman JL (2006) Evolution of class III homeodomain-leucine zipper genes in streptophytes. Genetics 173(1):373–388PubMedCrossRefGoogle Scholar
  33. Franco-Zorrilla J, Valli A, Todesco M et al (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39(8):1033–1037PubMedCrossRefGoogle Scholar
  34. Friedman R, Farh K, Burge C, Bartel D (2009) Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19(1):92–105PubMedCrossRefGoogle Scholar
  35. Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15(22):2038–2043PubMedCrossRefGoogle Scholar
  36. German MA, Pillay M, Jeong DH et al (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26(8):941–946PubMedCrossRefGoogle Scholar
  37. Guddeti S, Zhang DC, Li AL et al (2005) Molecular evolution of the rice miR395 gene family. Cell Res 15(8):631–638PubMedCrossRefGoogle Scholar
  38. 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(5):1376–1386PubMedCrossRefGoogle Scholar
  39. Hinas A, Reimegard J, Wagner E, Nellen W, Ambros V, Soderbom F (2007) The small RNA repertoire of Dictyostelium discoideum and its regulation by components of the RNAi pathway. Nucleic Acids Res 35(20):6714–6726PubMedCrossRefGoogle Scholar
  40. Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14(6):787–799PubMedCrossRefGoogle Scholar
  41. Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53PubMedCrossRefGoogle Scholar
  42. Kasschau KD, Xie Z, Allen E et al (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. Dev Cell 4(2):205–217PubMedCrossRefGoogle Scholar
  43. Klevebring D, Street NR, Fahlgren N et al (2009) Genome-wide profiling of Populus small RNAs. BMC Genomics 10:620PubMedCrossRefGoogle Scholar
  44. Kutter C, Schob H, Stadler M, Meins F, Si-Ammour A (2007) MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19(8):2417–2429PubMedCrossRefGoogle Scholar
  45. Lee H, Li L, Gu W et al (2010) Diverse pathways generate microRNA-like RNAs and dicer-independent small interfering RNAs in fungi. Mol Cell 38(6):803–814PubMedCrossRefGoogle Scholar
  46. Lelandais-Briere C, Naya L, Sallet E et al (2009) Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21(9):2780–2796PubMedCrossRefGoogle Scholar
  47. Li Y, Zheng Y, Addo-Quaye C et al (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J 62(5):742–759PubMedCrossRefGoogle Scholar
  48. Lim LP, Lau NC, Garrett-Engele P et al (2005) Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433(7027):769–773PubMedCrossRefGoogle Scholar
  49. 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(1):133–146PubMedCrossRefGoogle Scholar
  50. Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14(7):1605–1619PubMedCrossRefGoogle Scholar
  51. Lu C, Tej S, Luo S, Haudenschild C, Meyers B, Green P (2005) Elucidation of the small RNA component of the transcriptome. Science 309(5740):1567–1569PubMedCrossRefGoogle Scholar
  52. Lu C, Jeong DH, Kulkarni K et al (2008) Genome-wide analysis for discovery of rice microRNAs reveals natural antisense microRNAs (nat-miRNAs). Proc Natl Acad Sci USA 105(12):4951–4956PubMedCrossRefGoogle Scholar
  53. Ma Z, Coruh C, Axtell MJ (2010) Arabidopsis lyrata small RNAs: transient MIRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell 22(4):1090–1103PubMedCrossRefGoogle Scholar
  54. Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16(4):510–519PubMedCrossRefGoogle Scholar
  55. 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(5):1360–1375PubMedCrossRefGoogle Scholar
  56. Mallory AC, Hinze A, Tucker MR et al (2009) Redundant and specific roles of the ARGONAUTE proteins AGO1 and ZLL in development and small RNA-directed gene silencing. PLoS Genet 5(9):e1000646PubMedCrossRefGoogle Scholar
  57. Meyers BC, Axtell MJ, Bartel B et al (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20(12):3186–3190PubMedCrossRefGoogle Scholar
  58. Mi S, Cai T, Hu Y et al (2008) Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133(1):116–127PubMedCrossRefGoogle Scholar
  59. Molnar A, Schwach F, Studholme D, Thuenemann E, Baulcombe D (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447(7148):1126–1129PubMedCrossRefGoogle Scholar
  60. Nikovics K, Blein T, Peaucelle A et al (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18(11):2929–2945PubMedCrossRefGoogle Scholar
  61. Nodine M, Bartel D (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24(23):2678–2692PubMedCrossRefGoogle Scholar
  62. Palatnik JF, Allen E, Wu X et al (2003) Control of leaf morphogenesis by microRNAs. Nature 425(6955):257–263PubMedCrossRefGoogle Scholar
  63. Palatnik J, Wollmann H, Schommer C et al (2007) Sequence and expression differences underlie functional specialization of Arabidopsis microRNAs miR159 and miR319. Dev Cell 13(1):115–125PubMedCrossRefGoogle Scholar
  64. Pantaleo V, Szittya G, Moxon S et al (2010) Identification of grapevine microRNAs and their targets using high-throughput sequencing and degradome analysis. Plant J 62(6):960–976PubMedGoogle Scholar
  65. Park W, Li J, Song R, Messing J, Chen X (2002) CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol 12(17):1484–1495PubMedCrossRefGoogle Scholar
  66. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20(24):3407–3425PubMedCrossRefGoogle Scholar
  67. Raman S, Greb T, Peaucelle A, Blein T, Laufs P, Theres K (2008) Interplay of miR164, CUP-SHAPED COTYLEDON genes and LATERAL SUPPRESSOR controls axillary meristem formation in Arabidopsis thaliana. Plant J 55(1):65–76PubMedCrossRefGoogle Scholar
  68. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16(13):1616–1626PubMedCrossRefGoogle Scholar
  69. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110(4):513–520PubMedCrossRefGoogle Scholar
  70. Roger A, Hug L (2006) The origin and diversification of eukaryotes: problems with molecular phylogenetics and molecular clock estimation. Philos Trans R Soc Lond B Biol Sci 361(1470):1039–1054PubMedCrossRefGoogle Scholar
  71. Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510PubMedCrossRefGoogle Scholar
  72. Schauer SE, Jacobsen SE, Meinke DW, Ray A (2002) DICER-LIKE1: blind men and elephants in Arabidopsis development. Trends Plant Sci 7(11):487–491PubMedCrossRefGoogle Scholar
  73. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of MicroRNAs on the plant transcriptome. Dev Cell 8(4):517–527PubMedCrossRefGoogle Scholar
  74. Shin H, Shin H, Chen R, Harrison M (2006) Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J 45(5):712–726PubMedCrossRefGoogle Scholar
  75. Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM (2007) Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134(6):1051–1060PubMedCrossRefGoogle Scholar
  76. Song C, Wang C, Zhang C et al (2010) Deep sequencing discovery of novel and conserved microRNAs in trifoliate orange (Citrus trifoliata). BMC Genomics 11:431PubMedCrossRefGoogle Scholar
  77. Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16(8):2001–2019PubMedCrossRefGoogle Scholar
  78. Sunkar R, Girke T, Jain PK, Zhu JK (2005) Cloning and characterization of microRNAs from rice. Plant Cell 17(5):1397–1411PubMedCrossRefGoogle Scholar
  79. Tang G, Reinhart BJ, Bartel DP, Zamore PD (2003) A biochemical framework for RNA silencing in plants. Genes Dev 17(1):49–63PubMedCrossRefGoogle Scholar
  80. 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(7):e1001031PubMedCrossRefGoogle Scholar
  81. Vaucheret H (2008) Plant ARGONAUTES. Trends Plant Sci 13(7):350–358PubMedCrossRefGoogle Scholar
  82. Vaucheret H, Vazquez F, Crete P, Bartel DP (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18(10):1187–1197PubMedCrossRefGoogle Scholar
  83. Vazquez F, Gasciolli V, Crete P, Vaucheret H (2004) The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing. Curr Biol 14(4):346–351PubMedGoogle Scholar
  84. Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136(4):669–687PubMedCrossRefGoogle Scholar
  85. 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(8):2204–2216PubMedCrossRefGoogle Scholar
  86. Xie Z, Johansen LK, Gustafson AM et al (2004) Genetic and functional diversification of small RNA pathways in plants. PLoS Biol 2(5):E104PubMedCrossRefGoogle Scholar
  87. Zhang J, Xu Y, Huan Q, Chong K (2009a) Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10:449PubMedCrossRefGoogle Scholar
  88. Zhang L, Chia JM, Kumari S et al (2009b) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5(11):e1000716PubMedCrossRefGoogle Scholar
  89. Zhao T, Li G, Mi S et al (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21(10):1190–1203PubMedCrossRefGoogle Scholar
  90. Zhao CZ, Xia H, Frazier TP et al (2010) Deep sequencing identifies novel and conserved microRNAs in peanuts (Arachis hypogaea L.). BMC Plant Biol 10:3PubMedCrossRefGoogle Scholar
  91. Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of BiologyKnox CollegeGalesburgUSA

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