Biochemistry (Moscow)

, Volume 78, Issue 6, pp 627–637

Biogenesis, evolution, and functions of plant microRNAs



This review focuses on the biological role of one class of plant small RNAs, ∼22-nt microRNAs (miRNAs). The majority of plant miRNA targets are genes encoding the effector factors of cell signaling pathways. The regulation of their expression is necessary for both ontogenesis and rapid response of plants to biotic and abiotic stress factors. We also summarized current views on the biogenesis and evolution of plant miRNAs as well as the techniques used for their investigation.

Key words

microRNA stress plant 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Voinnet, O. (2009) Cell, 136, 669–687.PubMedCrossRefGoogle Scholar
  2. 2.
    Zhang, B., Pan, X., Cannon, C. H., Cobb, G. P., and Anderson, T. A. (2006) Plant J., 46, 243–259.PubMedCrossRefGoogle Scholar
  3. 3.
    Lee, Y., Kim, M., Han, J., Yeom, K. H., Lee, S., Baek, S. H., and Kim, V. N. (2004) EMBO J., 23, 4051–4060.PubMedCrossRefGoogle Scholar
  4. 4.
    Kim, V. N. (2005) Nat. Rev. Mol. Cell Biol., 6, 376–385.PubMedCrossRefGoogle Scholar
  5. 5.
    Vazquez, F., Blevins, T., Ailhas, J., Boller, T., and Meins, F., Jr. (2008) Nucleic Acids Res., 36, 6429–6438.PubMedCrossRefGoogle Scholar
  6. 6.
    Fang, Y., and Spector, D. L. (2007) Curr. Biol., 17, 818–823.PubMedCrossRefGoogle Scholar
  7. 7.
    Yu, B., Bi, L., Zheng, B., Ji, L., Chevalier, D., Agarwal, M., Ramachandran, V., Li, W., Lagrange, T., Walker, J. C., and Chen, X. (2008) Proc. Natl. Acad. Sci. USA, 105, 10073–10078.PubMedCrossRefGoogle Scholar
  8. 8.
    Kurihara, Y., Takashi, Y., and Watanabe, Y. (2006) RNA, 12, 206–212.PubMedCrossRefGoogle Scholar
  9. 9.
    Yang, L., Liu, Z., Lu, F., Dong, A., and Huang, H. (2006) Plant J., 47, 841–850.PubMedCrossRefGoogle Scholar
  10. 10.
    Lobbes, D., Rallapalli, G., Schmidt, D. D., Martin, C., and Clarke, J. (2006) EMBO Rep., 7, 1052–1058.PubMedCrossRefGoogle Scholar
  11. 11.
    Xie, Z., Allen, E., Fahlgren, N., Calamar, A., Givan, S. A., and Carrington, J. C. (2005) Plant Physiol., 138, 2145–2154.PubMedCrossRefGoogle Scholar
  12. 12.
    Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R. W., Steward, R., and Chen, X. (2005) Science, 307, 932–935.PubMedCrossRefGoogle Scholar
  13. 13.
    Li, J., Yang, Z., Yu, B., Liu, J., and Chen, X. (2005) Curr. Biol., 15, 1501–1507.PubMedCrossRefGoogle Scholar
  14. 14.
    Park, M. Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H., and Poethig, R. S. (2005) Proc. Natl. Acad. Sci. USA, 102, 3691–3696.PubMedCrossRefGoogle Scholar
  15. 15.
    Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B., and Bartel, D. P. (2002) Genes Dev., 16, 1616–1626.PubMedCrossRefGoogle Scholar
  16. 16.
    Matranga, C., Tomari, Y., Shin, C., Bartel, D. P., and Zamore, P. D. (2005) Cell, 123, 607–620.PubMedCrossRefGoogle Scholar
  17. 17.
    Chapman, E. J., and Carrington, J. C. (2007) Nat. Rev. Genet., 8, 884–896.PubMedCrossRefGoogle Scholar
  18. 18.
    Schwarz, D. S., Hutvagner, G., Du, T., Xu, Z., Aronin, N., and Zamore, P. D. (2003) Cell, 115, 199–208.PubMedCrossRefGoogle Scholar
  19. 19.
    Jones-Rhoades, M. W., and Bartel, D. P. (2004) Mol. Cell, 14, 787–799.PubMedCrossRefGoogle Scholar
  20. 20.
    Bohmert, K., Camus, I., Bellini, C., Bouchez, D., Caboche, M., and Benning, C. (1998) EMBO J., 17, 170–180.PubMedCrossRefGoogle Scholar
  21. 21.
    Humphreys, D. T., Westman, B. J., Martin, D. I., and Preiss, T. (2005) Proc. Natl. Acad. Sci. USA, 102, 16961–16966.PubMedCrossRefGoogle Scholar
  22. 22.
    Baumberger, N., and Baulcombe, D. C. (2005) Proc. Natl. Acad. Sci. USA, 102, 11928–11933.PubMedCrossRefGoogle Scholar
  23. 23.
    Beitzinger, M., Peters, L., Zhu, J. Y., Kremmer, E., and Meister, G. (2007) RNA Biol., 4, 76–84.PubMedCrossRefGoogle Scholar
  24. 24.
    Wang, Y., Juranek, S., Li, H., Sheng, G., Wardle, G. S., Tuschl, T., and Patel, D. J. (2009) Nature, 461, 754–761.PubMedCrossRefGoogle Scholar
  25. 25.
    Iki, T., Yoshikawa, M., Nishikiori, M., Jaudal, M. C., Matsumoto-Yokoyama, E., Mitsuhara, I., Meshi, T., and Ishikawa, M. (2010) Mol. Cell, 39, 282–291.PubMedCrossRefGoogle Scholar
  26. 26.
    Yuan, Y. R., Pei, Y., Ma, J. B., Kuryavyi, V., Zhadina, M., Meister, G., Chen, H. Y., Dauter, Z., Tuschl, T., and Patel, D. J. (2005) Mol. Cell, 19, 405–419.PubMedCrossRefGoogle Scholar
  27. 27.
    Cenik, E. S., and Zamore, P. D. (2011) Curr. Biol., 21, R446–R449.PubMedCrossRefGoogle Scholar
  28. 28.
    Ghildiyal, M., and Zamore, P. D. (2009) Nat. Rev. Genet., 10, 94–108.PubMedCrossRefGoogle Scholar
  29. 29.
    Bartel, D. P. (2004) Cell, 116, 281–297.PubMedCrossRefGoogle Scholar
  30. 30.
    Iwai, N., and Naraba, H. (2005) Biochem. Biophys. Res. Commun., 331, 1439–1444.PubMedCrossRefGoogle Scholar
  31. 31.
    Pillai, R. S., Artus, C. G., and Filipowicz, W. (2004) RNA, 10, 1518–1525.PubMedCrossRefGoogle Scholar
  32. 32.
    Aleman, L. M., Doench, J., and Sharp, P. A. (2007) RNA, 13, 385–395.PubMedCrossRefGoogle Scholar
  33. 33.
    Haley, B., and Zamore, P. D. (2004) Nat. Struct. Mol. Biol., 11, 599–606.PubMedCrossRefGoogle Scholar
  34. 34.
    Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Cell, 120, 15–20.PubMedCrossRefGoogle Scholar
  35. 35.
    Kiriakidou, M., Tan, G. S., Lamprinaki, S., De Planell-Saguer, M., Nelson, P. T., and Mourelatos, Z. (2007) Cell, 129, 1141–1151.PubMedCrossRefGoogle Scholar
  36. 36.
    Dunoyer, P., Lecellier, C. H., Parizotto, E. A., Himber, C., and Voinnet, O. (2004) Plant Cell, 16, 1235–1250.PubMedCrossRefGoogle Scholar
  37. 37.
    Kawashima, C. G., Yoshimoto, N., Maruyama-Nakashita, A., Tsuchiya, Y. N., Saito, K., Takahashi, H., and Dalmay, T. (2009) Plant J., 57, 313–321.PubMedCrossRefGoogle Scholar
  38. 38.
    Xie, Z., Kasschau, K. D., and Carrington, J. C. (2003) Curr. Biol., 13, 784–789.PubMedCrossRefGoogle Scholar
  39. 39.
    Vaucheret, H., Vazquez, F., Crete, P., and Bartel, D. P. (2004) Genes Dev., 18, 1187–1197.PubMedCrossRefGoogle Scholar
  40. 40.
    Ramachandran, V., and Chen, X. (2008) Science, 321, 1490–1492.PubMedCrossRefGoogle Scholar
  41. 41.
    Kennedy, S., Wang, D., and Ruvkun, G. (2004) Nature, 427, 645–649.PubMedCrossRefGoogle Scholar
  42. 42.
    Chatterjee, S., and Grosshans, H. (2009) Nature, 461, 546–549.PubMedCrossRefGoogle Scholar
  43. 43.
    Kai, Z. S., and Pasquinelli, A. E. (2010) Nat. Struct. Mol. Biol., 17, 5–10.PubMedCrossRefGoogle Scholar
  44. 44.
    Franco-Zorrilla, J. M., Valli, A., Todesco, M., Mateos, I., Puga, M. I., Rubio-Somoza, I., Leyva, A., Weigel, D., Garcia, J. A., and Paz-Ares, J. (2007) Nat. Genet., 39, 1033–1037.PubMedCrossRefGoogle Scholar
  45. 45.
    Salmena, L., Poliseno, L., Tay, Y., Kats, L., and Pandolfi, P. P. (2011) Cell, 146, 353–358.PubMedCrossRefGoogle Scholar
  46. 46.
    Allen, E., and Howell, M. D. (2010) Semin. Cell Dev. Biol., 21, 798–804.PubMedCrossRefGoogle Scholar
  47. 47.
    Anantharaman, V., Koonin, E. V., and Aravind, L. (2002) Nucleic Acids Res., 30, 1427–1464.PubMedCrossRefGoogle Scholar
  48. 48.
    Buchon, N., and Vaury, C. (2006) Heredity (Edinb.), 96, 195–202.CrossRefGoogle Scholar
  49. 49.
    Axtell, M. J., and Bowman, J. L. (2008) Trends Plant Sci., 13, 343–349.PubMedCrossRefGoogle Scholar
  50. 50.
    Martin, R. C., Liu, P. P., Goloviznina, N. A., and Nonogaki, H. (2010) J. Exp. Bot., 61, 2229–2234.PubMedCrossRefGoogle Scholar
  51. 51.
    Arazi, T. (2012) Plant Mol. Biol., 80, 55–65.PubMedCrossRefGoogle Scholar
  52. 52.
    Molnar, A., Schwach, F., Studholme, D. J., Thuenemann, E. C., and Baulcombe, D. C. (2007) Nature, 447, 1126–1129.PubMedCrossRefGoogle Scholar
  53. 53.
    Arteaga-Vazquez, M., Caballero-Perez, J., and Vielle-Calzada, J. P. (2006) Plant Cell, 18, 3355–3369.PubMedCrossRefGoogle Scholar
  54. 54.
    Palatnik, J. F., Wollmann, H., Schommer, C., Schwab, R., Boisbouvier, J., Rodriguez, R., Warthmann, N., Allen, E., Dezulian, T., Huson, D., Carrington, J. C., and Weigel, D. (2007) Dev. Cell, 13, 115–125.PubMedCrossRefGoogle Scholar
  55. 55.
    Warthmann, N., Das, S., Lanz, C., and Weigel, D. (2008) Mol. Biol. Evol., 25, 892–902.PubMedCrossRefGoogle Scholar
  56. 56.
    Moldovan, D., Spriggs, A., Yang, J., Pogson, B. J., Dennis, E. S., and Wilson, I. W. (2010) J. Exp. Bot., 61, 165–177.PubMedCrossRefGoogle Scholar
  57. 57.
    Beauclair, L., Yu, A., and Bouche, N. (2010) Plant J., 62, 454–462.PubMedCrossRefGoogle Scholar
  58. 58.
    Fahlgren, N., Howell, M. D., Kasschau, K. D., Chapman, E. J., Sullivan, C. M., Cumbie, J. S., Givan, S. A., Law, T. F., Grant, S. R., Dangl, J. L., and Carrington, J. C. (2007) PLoS One, 2, e219.PubMedCrossRefGoogle Scholar
  59. 59.
    Omelyantchuk, N. A., Kuznetsova, T. N., and Katokhin, A. V. (2005) in Informatsionnyi Vestnik VOGiS, pp. 440–450.Google Scholar
  60. 60.
    Allen, E., Xie, Z., Gustafson, A. M., Sung, G. H., Spatafora, J. W., and Carrington, J. C. (2004) Nat. Genet., 36, 1282–1290.PubMedCrossRefGoogle Scholar
  61. 61.
    Dunoyer, P., Himber, C., Ruiz-Ferrer, V., Alioua, A., and Voinnet, O. (2007) Nat. Genet., 39, 848–856.PubMedCrossRefGoogle Scholar
  62. 62.
    De Meaux, J., Hu, J. Y., Tartler, U., and Goebel, U. (2008) Proc. Natl. Acad. Sci. USA, 105, 8994–8999.PubMedCrossRefGoogle Scholar
  63. 63.
    Felippes, F. F., Schneeberger, K., Dezulian, T., Huson, D. H., and Weigel, D. (2008) RNA, 14, 2455–2459.PubMedCrossRefGoogle Scholar
  64. 64.
    Piriyapongsa, J., and Jordan, I. K. (2008) RNA, 14, 814–821.PubMedCrossRefGoogle Scholar
  65. 65.
    Niwa, R., and Slack, F. J. (2007) Curr. Opin. Genet. Dev., 17, 145–150.PubMedCrossRefGoogle Scholar
  66. 66.
    Mallory, A. C., Bartel, D. P., and Bartel, B. (2005) Plant Cell, 17, 1360–1375.PubMedCrossRefGoogle Scholar
  67. 67.
    Guo, H. S., Xie, Q., Fei, J. F., and Chua, N. H. (2005) Plant Cell, 17, 1376–1386.PubMedCrossRefGoogle Scholar
  68. 68.
    Mallory, A. C., Dugas, D. V., Bartel, D. P., and Bartel, B. (2004) Curr. Biol., 14, 1035–1046.PubMedCrossRefGoogle Scholar
  69. 69.
    McHale, N. A., and Koning, R. E. (2004) Plant Cell, 16, 1730–1740.PubMedCrossRefGoogle Scholar
  70. 70.
    Chen, X. (2004) Science, 303, 2022–2025.PubMedCrossRefGoogle Scholar
  71. 71.
    Baranenko, V. V. (2006) Tsitologiya, 48, 465–474.Google Scholar
  72. 72.
    Sunkar, R., Li, Y. F., and Jagadeeswaran, G. (2012) Trends Plant Sci., 17, 196–203.PubMedCrossRefGoogle Scholar
  73. 73.
    Trindade, I., Capitao, C., Dalmay, T., Fevereiro, M. P., and Santos, D. M. (2010) Planta, 231, 705–716.PubMedCrossRefGoogle Scholar
  74. 74.
    Li, W. X., Oono, Y., Zhu, J., He, X. J., Wu, J. M., Iida, K., Lu, X. Y., Cui, X., Jin, H., and Zhu, J. K. (2008) Plant Cell, 20, 2238–2251.PubMedCrossRefGoogle Scholar
  75. 75.
    Zhao, B., Liang, R., Ge, L., Li, W., Xiao, H., Lin, H., Ruan, K., and Jin, Y. (2007) Biochem. Biophys. Res. Commun., 354, 585–590.PubMedCrossRefGoogle Scholar
  76. 76.
    Lv, D. K., Bai, X., Li, Y., Ding, X. D., Ge, Y., Cai, H., Ji, W., Wu, N., and Zhu, Y. M. (2010) Gene, 459, 39–47.PubMedCrossRefGoogle Scholar
  77. 77.
    Ding, D., Zhang, L., Wang, H., Liu, Z., Zhang, Z., and Zheng, Y. (2009) Ann. Bot., 103, 29–38.PubMedCrossRefGoogle Scholar
  78. 78.
    Xin, M., Wang, Y., Yao, Y., Song, N., Hu, Z., Qin, D., Xie, C., Peng, H., Ni, Z., and Sun, Q. (2011) BMC Plant Biol., 11, 61.PubMedCrossRefGoogle Scholar
  79. 79.
    Kantar, M., Unver, T., and Budak, H. (2010) Funct. Integr. Genom., 10, 493–507.CrossRefGoogle Scholar
  80. 80.
    Pashkovskii, P. P., Ryazanskii, S. S., Radyukina, N. L., Gvozdev, V. A., and Kuznetsov, Vl. V. (2010) Rus. J. Plant Physiol., 57, 707–714.CrossRefGoogle Scholar
  81. 81.
    Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O., and Jones, J. D. (2006) Science, 312, 436–439.PubMedCrossRefGoogle Scholar
  82. 82.
    Chapman, E. J., and Estelle, M. (2009) Annu. Rev. Genet., 43, 265–285.PubMedCrossRefGoogle Scholar
  83. 83.
    Vidal, E. A., Araus, V., Lu, C., Parry, G., Green, P. J., Coruzzi, G. M., and Gutierrez, R. A. (2010) Proc. Natl. Acad. Sci. USA, 107, 4477–4482.PubMedCrossRefGoogle Scholar
  84. 84.
    Gifford, M. L., Dean, A., Gutierrez, R. A., Coruzzi, G. M., and Birnbaum, K. D. (2008) Proc. Natl. Acad. Sci. USA, 105, 803–808.PubMedCrossRefGoogle Scholar
  85. 85.
    Hsieh, L. C., Lin, S. I., Shih, A. C., Chen, J. W., Lin, W. Y., Tseng, C. Y., Li, W. H., and Chiou, T. J. (2009) Plant Physiol., 151, 2120–2132.PubMedCrossRefGoogle Scholar
  86. 86.
    Pant, B. D., Buhtz, A., Kehr, J., and Scheible, W. R. (2008) Plant J., 53, 731–738.PubMedCrossRefGoogle Scholar
  87. 87.
    Pant, B. D., Musialak-Lange, M., Nuc, P., May, P., Buhtz, A., Kehr, J., Walther, D., and Scheible, W. R. (2009) Plant Physiol., 150, 1541–1555.PubMedCrossRefGoogle Scholar
  88. 88.
    Liang, G., and Yu, D. (2010) Plant Signal. Behav., 5, 1257–1259.PubMedCrossRefGoogle Scholar
  89. 89.
    Burkhead, J. L., Reynolds, K. A., Abdel-Ghany, S. E., Cohu, C. M., and Pilon, M. (2009) New Phytol., 182, 799–816.PubMedCrossRefGoogle Scholar
  90. 90.
    Pashkovsky, P. P., and Radyukina, N. L. (2011) Vestnik Tomsk. Univer. Biol., 3, 147–151.Google Scholar
  91. 91.
    Abdel-Ghany, S. E., and Pilon, M. (2008) J. Biol. Chem., 283, 15932–15945.PubMedCrossRefGoogle Scholar
  92. 92.
    Jagadeeswaran, G., Saini, A., and Sunkar, R. (2009) Planta, 229, 1009–1014.PubMedCrossRefGoogle Scholar
  93. 93.
    Ameres, S. L., Martinez, J., and Schroeder, R. (2007) Cell, 130, 101–112.PubMedCrossRefGoogle Scholar
  94. 94.
    Maksymiec, W. (2007) Acta Physiol. Plant., 29, 177–187.CrossRefGoogle Scholar
  95. 95.
    Ding, Y., Chen, Z., and Zhu, C. (2011) J. Exp. Bot., 62, 3563–3573.PubMedCrossRefGoogle Scholar
  96. 96.
    Chen, L., Wang, T., Zhao, M., Tian, Q., and Zhang, W. H. (2012) Planta, 235, 375–386.PubMedCrossRefGoogle Scholar
  97. 97.
    Huang, S. Q., Peng, J., Qiu, C. X., and Yang, Z. M. (2009) J. Inorg. Biochem., 103, 282–287.PubMedCrossRefGoogle Scholar
  98. 98.
    Kim, T. H., Park, J. H., Kim, M. C., and Cho, S. H. (2008) J. Plant Physiol., 165, 345–349.PubMedCrossRefGoogle Scholar
  99. 99.
    Ruiz-Ferrer, V., and Voinnet, O. (2009) Annu. Rev. Plant Biol., 60, 485–510.PubMedCrossRefGoogle Scholar
  100. 100.
    Zhang, W., Gao, S., Zhou, X., Chellappan, P., Chen, Z., Zhou, X., Zhang, X., Fromuth, N., Coutino, G., Coffey, M., and Jin, H. (2011) Plant Mol. Biol., 75, 93–105.PubMedCrossRefGoogle Scholar
  101. 101.
    Berezikov, E. (2011) Nat. Rev. Genet., 12, 846–860.PubMedCrossRefGoogle Scholar
  102. 102.
    Castoldi, M., Schmidt, S., Benes, V., Noerholm, M., Kulozik, A. E., Hentze, M. W., and Muckenthaler, M. U. (2006) RNA, 12, 913–920.PubMedCrossRefGoogle Scholar
  103. 103.
    Shi, R., and Chiang, V. L. (2005) Biotechniques, 39, 519–525.PubMedCrossRefGoogle Scholar
  104. 104.
    Brautigam, A., and Gowik, U. (2010) Plant Biol. (Stuttg.), 12, 831–841.CrossRefGoogle Scholar
  105. 105.
    Zhang, Y., Jiang, W. K., and Gao, L. Z. (2011) PLoS One, 6, e28073.PubMedCrossRefGoogle Scholar
  106. 106.
    Studholme, D. J. (2012) Brief Funct. Genom., 11, 71–85.CrossRefGoogle Scholar
  107. 107.
    Zhang, L., Hou, D., Chen, X., Li, D., Zhu, L., Zhang, Y., Li, J., Bian, Z., Liang, X., Cai, X., Yin, Y., Wang, C., Zhang, T., Zhu, D., Zhang, D., Xu, J., Chen, Q., Ba, Y., Liu, J., Wang, Q., Chen, J., Wang, J., Wang, M., Zhang, Q., Zhang, J., Zen, K., and Zhang, C. Y. (2012) Cell Res., 22, 107–126.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2013

Authors and Affiliations

  1. 1.Timiryazev Institute of Plant PhysiologyRussian Academy of SciencesMoscowRussia
  2. 2.Institute of Molecular GeneticsRussian Academy of SciencesMoscowRussia

Personalised recommendations