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The role of microRNA in abiotic stress response in plants

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Abstract

Regulation of gene expression via microRNA is the key mechanism of response to biotic and abiotic stresses in plants. There are a lot of experimental data on the biological function of microRNAs in response to different stresses in various plant species. This review contains up-to-date information on molecular mechanisms of microRNA action in plants in response to abiotic stresses, including drought, salinity, mineral nutrient deficiency or imbalance.

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References

  1. Sunkar R. 2010. MicroRNAs with macro-effects on plant stress responses. Semin. Cell Dev. Biol. 21, 805–811.

    Article  CAS  PubMed  Google Scholar 

  2. Mathur S., Agrawal D., Jajoo A. 2014. Photosynthesis: Response to high temperature stress. J. Photochem. Photobiol. B. 137, 116–126.

    Article  CAS  PubMed  Google Scholar 

  3. Suzuki N., Rivero R.M., Shulaev V., Blumwald E., Mittler R. 2014. Abiotic and biotic stress combinations. New Phytol. 203, 32–43.

    Article  PubMed  Google Scholar 

  4. Sunkar R., Li Y.F., Jagadeeswaran G. 2012. Functions of microRNAs in plant stress responses. Trends Plant Sci. 17, 196–203.

    Article  CAS  PubMed  Google Scholar 

  5. Khraiwesh B., Zhu J.K., Zhu J. 2012. Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta. 1819, 137–148.

    Article  CAS  PubMed  Google Scholar 

  6. Zhang B. 2015. MicroRNA: A new target for improving plant tolerance to abiotic stress. J. Exp. Bot. 66, 1749–1761.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Axtell M.J., Westholm J.O., Lai E.C. 2011. Vive la difference: Biogenesis and evolution of microRNAs in plants and animals. Genome Biol. 12, 221.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Cuperus J.T., Fahlgren N., Carrington J.C. 2011. Evolution and functional diversification of MIRNA genes. Plant Cell. 23, 431–442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Voinnet O. 2009. Origin, biogenesis, and activity of plant microRNAs. Cell. 136, 669–687.

    Article  CAS  PubMed  Google Scholar 

  10. Carrington J.C., Ambros V. 2003. Role of microRNAs in plant and animal development. Science. 301, 336–338.

    Article  CAS  PubMed  Google Scholar 

  11. Bartel D.P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116, 281–297.

    Article  CAS  PubMed  Google Scholar 

  12. Lee Y., Kim M., Han J., Yeom K.H., Lee S., Baek S.H., Kim V.N. 2004). MicroRNA genes are transcribed by RNA polymerase II. EMBO J. 23, 4051–4060.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. He L., Hannon G.J. 2004. MicroRNAs: Small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522–531.

    Article  CAS  PubMed  Google Scholar 

  14. Grigg S.P., Canales C., Hay A., Tsiantis M. 2005. SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature. 437, 1022–1026.

    Article  CAS  PubMed  Google Scholar 

  15. 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, 206–212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Dong Z., Han M.H., Fedoroff N. 2008. The RNAbinding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc. Natl. Acad. Sci. U. S. A. 105, 9970–9975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Llave C., Kasschau K.D., Rector M.A., Carrington J.C. 2002. Endogenous and silencing-associated small RNAs in plants. Plant Cell. 14, 1605–1619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Mette M.F., van der Winden J., Matzke M., Matzke A.J. 2002. Short RNAs can identify new candidate transposable element families in Arabidopsis. Plant Physiol. 130, 6–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. 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, 1484–1495.

    Article  CAS  PubMed  Google Scholar 

  20. Reinhart B.J., Weinstein E.G., Rhoades M.W., Bartel B., Bartel D.P. 2002. MicroRNAs in plants. Genes Dev. 16, 1616–1626.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhang Z., Yu J., Li D., Zhang Z., Liu F., Zhou X., Wang T., Ling Y., Su Z. 2010. PMRD: Plant microRNA database. Nucleic Acids Res. 38, D806–D813.

    Article  CAS  PubMed  Google Scholar 

  22. Zhang B.H., Pan X.P., Wang Q.L., Cobb G.P., Anderson T.A. 2005. Identification and characterization of new plant microRNAs using EST analysis. Cell Res. 15, 336–360.

    Article  PubMed  Google Scholar 

  23. Sunkar R., Jagadeeswaran G. 2008. In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol. 8, 37.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Sun X., Zhang Y., Zhu X., Korir N.K., Tao R., Wang C., Fang J. 2014. Advances in identification and validation of plant microRNAs and their target genes. Physiol. Plant. 152, 203–218.

    Article  CAS  PubMed  Google Scholar 

  25. Ma X., Tang Z., Qin J., Meng Y. 2015. The use of highthroughput sequencing methods for plant microRNA research. RNA Biol. 12, 709–719.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Liu C.G., Calin G.A., Volinia S., Croce C.M. 2008. MicroRNA expression profiling using microarrays. Nat. Protoc. 3, 563–578.

    Article  CAS  PubMed  Google Scholar 

  27. Song C., Fang J., Wang C., Guo L., Nicholas K.K., Ma Z. 2010. MiR-RACE, a new efficient approach to determine the precise sequences of computationally identified trifoliate orange (Poncirus trifoliata) microRNAs. PLoS ONE. 5, e10861.

    Article  Google Scholar 

  28. Wang T., Chen L., Zhao M., Tian Q., Zhang W.H. 2011. Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics. 12, 367.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Eldem V., Celikkol Akcay U., Ozhuner E., Bakir Y., Uranbey S., Unver T. 2012. Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by high-throughput deep sequencing. PLoS ONE. 7, e50298.

    Article  Google Scholar 

  30. Melnikova N.V., Belenikin M.S., Bolsheva N.L., Dmitriev A.A., Speranskaya A.S., Krinitsina A.A., Samatadze T.E., Amosova A.V., Muravenko O.V., Zelenin A.V., Kudryavtseva A.V. 2014. Flax inorganic phosphate deficiency responsive miRNAs. J. Agr. Sci. 6, 156–160.

    Google Scholar 

  31. Barrera-Figueroa B.E., Gao L., Diop N.N., Wu Z., Ehlers J.D., Roberts P.A., Close T.J., Zhu J.K., Liu R. 2011. Identification and comparative analysis of drought-associated microRNAs in two cowpea genotypes. BMC Plant Biol. 11, 127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kumar R. 2014. Role of microRNAs in biotic and abiotic stress responses in crop plants. Appl. Biochem. Biotechnol. 174, 93–115.

    Article  CAS  PubMed  Google Scholar 

  33. Shiroguchi K., Jia T.Z., Sims P.A., Xie X.S. 2012. Digital RNA sequencing minimizes sequence-dependent bias and amplification noise with optimized singlemolecule barcodes. Proc. Natl. Acad. Sci. U. S. A. 109, 1347–1352.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Krasnov G.S., Oparina N.Yu., Dmitriev A.A., Kudryavtseva A.V., Anedchenko E.A., Kondrat’eva T.T., Zabarovsky E.R., Senchenko V.N. 2011. RPN1, a new reference gene for quantitative data normalization in lung and kidney cancer. Mol. Biol. (Moscow). 45 (2), 211–220.

    Article  CAS  Google Scholar 

  35. Benes V., Castoldi M. 2010. Expression profiling of microRNA using real-time quantitative PCR, how to use it and what is available. Methods. 50, 244–249.

    Article  CAS  PubMed  Google Scholar 

  36. Shukla L.I., Chinnusamy V., Sunkar R. 2008. The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim. Biophys. Acta. 1779, 743–748.

    Article  CAS  PubMed  Google Scholar 

  37. Jones-Rhoades M.W., Bartel D.P. 2004. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell. 14, 787–799.

    Article  CAS  PubMed  Google Scholar 

  38. Panda S.K., Sunkar R. 2015. Nutrient- and other stress-responsive microRNAs in plants: Role for thiolbased redox signaling. Plant Signal. Behav. 10, e1010916.

    Google Scholar 

  39. Paul S., Datta S.K., Datta K. 2015. miRNA regulation of nutrient homeostasis in plants. Front. Plant Sci. 6, 232.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Kulcheski F.R., Correa R., Gomes I.A., de Lima J.C., Margis R. 2015. NPK macronutrients and microRNA homeostasis. Front. Plant Sci. 6, 451.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Matthewman C.A., Kawashima C.G., Huska D., Csorba T., Dalmay T., Kopriva S. 2012. miR395 is a general component of the sulfate assimilation regulatory network in Arabidopsis. FEBS Lett. 586, 3242–3248.

    Article  CAS  PubMed  Google Scholar 

  42. Kawashima C.G., Matthewman C.A., Huang S., Lee B.R., Yoshimoto N., Koprivova A., Rubio-Somoza I., Todesco M., Rathjen T., Saito K., Takahashi H., Dalmay T., Kopriva S. 2011. Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J. 66, 863–876.

    Article  CAS  PubMed  Google Scholar 

  43. Jagadeeswaran G., Li Y.F., Sunkar R. 2014. Redox signaling mediates the expression of a sulfate-deprivationinducible microRNA395 in Arabidopsis. Plant J. 77, 85–96.

    Article  CAS  PubMed  Google Scholar 

  44. Melnikova N.V., Dmitriev A.A., Belenikin M.S., Speranskaya A.S., Krinitsina A.A., Rachinskaia O.A., Lakunina V.A., Krasnov G.S., Snezhkina A.V., Sadritdinova A.F., Uroshlev L.A., Koroban N.V., Samatadze T.E., Amosova A.V., Zelenin A.V., et al. 2015. Excess fertilizer responsive miRNAs revealed in Linum usitatissimum L. Biochimie. 109, 36–41.

    Article  CAS  PubMed  Google Scholar 

  45. Sunkar R., Zhu J.K. 2004. Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell. 16, 2001–2019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Pant B.D., Buhtz A., Kehr J., Scheible W.R. 2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53, 731–738.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Branscheid A., Sieh D., Pant B.D., May P., Devers E.A., Elkrog A., Schauser L., Scheible W.R., Krajinski F. 2010. Expression pattern suggests a role of MiR399 in the regulation of the cellular response to local Pi increase during arbuscular mycorrhizal symbiosis. Mol. Plant Microbe Interact. 23, 915–926.

    Article  CAS  PubMed  Google Scholar 

  48. Liang G., Ai Q., Yu D. 2015. Uncovering miRNAs involved in crosstalk between nutrient deficiencies in Arabidopsis. Sci. Rep. 5, 11813.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Ariel F., Romero-Barrios N., Jegu T., Benhamed M., Crespi M. 2015. Battles and hijacks: Noncoding transcription in plants. Trends Plant Sci. 20, 362–371.

    Article  CAS  PubMed  Google Scholar 

  50. Lauressergues D., Couzigou J.M., Clemente H.S., Martinez Y., Dunand C., Becard G., Combier J.P. 2015. Primary transcripts of microRNAs encode regulatory peptides. Nature. 520, 90–93.

    Article  CAS  PubMed  Google Scholar 

  51. Krannich C.T., Maletzki L., Kurowsky C., Horn R. 2015. Network candidate genes in breeding for drought tolerant crops. Int. J. Mol. Sci. 16, 16378–16400.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Rajwanshi R., Chakraborty S., Jayanandi K., Deb B., Lightfoot D.A. 2014. Orthologous plant microRNAs: microregulators with great potential for improving stress tolerance in plants. Theor. Appl. Genet. 127, 2525–2543.

    Article  CAS  PubMed  Google Scholar 

  53. Ding Y., Tao Y., Zhu C. 2013. Emerging roles of microRNAs in the mediation of drought stress response in plants. J. Exp. Bot. 64, 3077–3086.

    Article  CAS  PubMed  Google Scholar 

  54. Ferdous J., Hussain S.S., Shi B.J. 2015. Role of microRNAs in plant drought tolerance. Plant Biotechnol. J. 13, 293–305.

    Article  CAS  PubMed  Google Scholar 

  55. Giacomelli J.I., Weigel D., Chan R.L., Manavella P.A. 2012. Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol. 195, 766–773.

    Article  CAS  PubMed  Google Scholar 

  56. Zhang N., Yang J., Wang Z., Wen Y., Wang J., He W., Liu B., Si H., Wang D. 2014. Identification of novel and conserved microRNAs related to drought stress in potato by deep sequencing. PLoS ONE. 9, e95489.

    Article  Google Scholar 

  57. Liu P.P., Montgomery T.A., Fahlgren N., Kasschau K.D., Nonogaki H., Carrington J.C. 2007. Repression of AUXIN RESPONSE FACTOR10 by microRNA160 is critical for seed germination and post-germination stages. Plant J. 52, 133–146.

    Article  CAS  PubMed  Google Scholar 

  58. Boualem A., Laporte P., Jovanovic M., Laffont C., Plet J., Combier J.P., Niebel A., Crespi M., Frugier F. 2008. MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J. 54, 876–887.

    Article  CAS  PubMed  Google Scholar 

  59. Trindade I., Capitao C., Dalmay T., Fevereiro M.P., Santos D.M. 2010. miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta. 231, 705–716.

    Article  CAS  PubMed  Google Scholar 

  60. Shamimuzzaman M., Vodkin L. 2012. Identification of soybean seed developmental stage-specific and tissuespecific miRNA targets by degradome sequencing. BMC Genomics. 13, 310.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Kantar M., Lucas S.J., Budak H. 2011. miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta. 233, 471–484.

    Article  CAS  PubMed  Google Scholar 

  62. Liu Q., Zhang Y.C., Wang C.Y., Luo Y.C., Huang Q.J., Chen S.Y., Zhou H., Qu L.H., Chen Y.Q. 2009. Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Lett. 583, 723–728.

    Article  CAS  PubMed  Google Scholar 

  63. Szabados L., Savoure A. 2010. Proline: A multifunctional amino acid. Trends Plant Sci. 15, 89–97.

    Article  CAS  PubMed  Google Scholar 

  64. Li W.X., Oono Y., Zhu J., He X.J., Wu J.M., Iida K., Lu X.Y., Cui X., Jin H., Zhu J.K. 2008. The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell. 20, 2238–2251.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zhao B., Liang R., Ge L., Li W., Xiao H., Lin H., Ruan K., Jin Y. 2007. Identification of drought-induced microRNAs in rice. Biochem. Biophys. Res. Commun. 354, 585–590.

    Article  CAS  PubMed  Google Scholar 

  66. 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. 33, 403–409.

    Article  CAS  PubMed  Google Scholar 

  67. Liu H.H., Tian X., Li Y.J., Wu C.A., Zheng C.C. 2008. Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA. 14, 836–843.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Budak H., Kantar M., Bulut R., Akpinar B.A. 2015. Stress responsive miRNAs and isomiRs in cereals. Plant Sci. 235, 1–13.

    Article  CAS  PubMed  Google Scholar 

  69. Golldack D., Li C., Mohan H., Probst N. 2014. Tolerance to drought and salt stress in plants: Unraveling the signaling networks. Front. Plant Sci. 5, 151.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Reyes J.L., Chua N.H. 2007. ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J. 49, 592–606.

    Article  CAS  PubMed  Google Scholar 

  71. Chaves M.M., Oliveira M.M. 2004. Mechanisms underlying plant resilience to water deficits: Prospects for water-saving agriculture. J. Exp. Bot. 55, 2365–2384.

    Article  CAS  PubMed  Google Scholar 

  72. Si J., Zhou T., Bo W., Xu F., Wu R. 2014. Genomewide analysis of salt-responsive and novel microRNAs in Populus euphratica by deep sequencing. BMC Genet. 15, Suppl. 1, S6.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Song J.B., Gao S., Sun D., Li H., Shu X.X., Yang Z.M. 2013. miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. BMC Plant Biol. 13, 210.

    Article  PubMed  PubMed Central  Google Scholar 

  74. Song J.B., Huang S.Q., Dalmay T., Yang Z.M. 2012. Regulation of leaf morphology by microRNA394 and its target leaf curling responsiveness. Plant Cell Physiol. 53, 1283–1294.

    Article  CAS  PubMed  Google Scholar 

  75. Lu X., Guan Q., Zhu J. 2013. Downregulation of CSD2 by a heat-inducible miR398 is required for thermotolerance in Arabidopsis. Plant Signal. Behav. 8, e24952.

    Article  Google Scholar 

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Correspondence to N. V. Melnikova.

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Original Russian Text © N.V. Koroban, A.V. Kudryavtseva, G.S. Krasnov, A.F. Sadritdinova, M.S. Fedorova, A.V. Snezhkina, N.L. Bolsheva, O.V. Muravenko, A.A. Dmitriev, N.V. Melnikova, 2016, published in Molekulyarnaya Biologiya, 2016, Vol. 50, No. 3, pp. 387–394.

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Koroban, N.V., Kudryavtseva, A.V., Krasnov, G.S. et al. The role of microRNA in abiotic stress response in plants. Mol Biol 50, 337–343 (2016). https://doi.org/10.1134/S0026893316020102

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