Skip to main content

Advertisement

Log in

Salt and Drought Stresses Induce the Aberrant Expression of microRNA Genes in Tobacco

  • Research
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

Drought and salinity stresses significantly altered microRNA (miRNA) expression in a dose-dependent manner in tobacco. Salinity stress changed the miRNA expression levels from a 6.86-fold down-regulation to a 616.57-fold up-regulation. Alternatively, miRNAs were down-regulated by 2.68-fold and up-regulated 2810-fold under drought conditions. miR395 was most sensitive to both stresses and was up-regulated by 616 and 2810-folds by 1.00% PEG and 0.171 M NaCl, respectively. Salinity and drought stresses also changed the expression of protein-coding genes [alcohol dehydrogenase (ADH) and alcohol peroxidase (APX)]. The results suggest that miRNAs may play an important role in plant response to environmental abiotic stresses. Further investigation of miRNA-mediated gene regulation may elucidate the molecular mechanism of plant tolerance to abiotic stresses and has the potential to create a miRNA-based biotechnology for improving plant tolerance to drought and salinity stresses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Sunkar, R. (2010). MicroRNAs with macro-effects on plant stress responses. Seminars in Cell and Developmental Biology. p.10.1016/j.semcdb.2010.04.001.

  2. Meehl, G. A., et al. (2005). How much more global warming and sea level rise? Science, 307(5716), 1769–1772.

    Article  CAS  Google Scholar 

  3. Abu-Asab, M. S., et al. (2004). Earlier plant flowering in spring as a response to global warming in the Washington, DC, area. Biodiversity and Conservation, 10(4), 597–612.

    Article  Google Scholar 

  4. Peng, S., et al. (2004). Rice yields decline with higher night temperature from global warming. Proceedings of the National Academy of Sciences, 101(27), 9971–9975.

    Article  CAS  Google Scholar 

  5. Houghton, J. (2005). Global warming. Reports on Progress in Physics, 68(6), 1343–1403.

    Article  Google Scholar 

  6. Bartel, D. P. (2004). MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116(2), 281–297.

    Article  CAS  Google Scholar 

  7. Zhang, B. H., et al. (2006). Plant microRNA: A small regulatory molecule with big impact. Developmental Biology, 289(1), 3–16.

    Article  CAS  Google Scholar 

  8. Aukerman, M. J., & Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell, 15(11), 2730–2741.

    Article  CAS  Google Scholar 

  9. Juarez, M. T., et al. (2004). microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature, 428(6978), 84–88.

    Article  CAS  Google Scholar 

  10. McHale, N. A., & Koning, R. E. (2004). MicroRNA-directed cleavage of Nicoltiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical Meristems. Plant Cell, 16(7), 1730–1740.

    Article  CAS  Google Scholar 

  11. Guo, H. S., et al. (2005). MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. Plant Cell, 17(5), 1376–1386.

    Article  CAS  Google Scholar 

  12. Zhang, B. H., Wang, Q. L., & Pan, X. P. (2007). MicroRNAs and their regulatory roles in animals and plants. Journal of Cellular Physiology, 210(2), 279–289.

    Article  CAS  Google Scholar 

  13. Mallory, A. C., Bartel, D. P., & 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), 1360–1375.

    Article  CAS  Google Scholar 

  14. Liu, Q., et al. (2009). Expression analysis of phytohormone-regulated microRNAs in rice, implying their regulation roles in plant hormone signaling. FEBS Letters, 583(4), 723–728.

    Article  CAS  Google Scholar 

  15. Poethig, S., et al. (2004). Regulation of developmental timing in plants by miRNAs. Developmental Biology, 271(2), 551–552.

    Google Scholar 

  16. Achard, P., et al. (2004). Modulation of floral development by a gibberellin-regulated microRNA. Development, 131(14), 3357–3365.

    Article  CAS  Google Scholar 

  17. Hewezi, T., et al. (2008). Arabidopsis small RNAs and their targets during cyst nematode parasitism. Molecular Plant-Microbe Interactions, 21(12), 1622–1634.

    Article  CAS  Google Scholar 

  18. Sullivan, C. S., & Ganem, D. (2005). MicroRNAs and viral infection. Molecular Cell, 20(1), 3–7.

    Article  CAS  Google Scholar 

  19. Navarro, L., et al. (2006). A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science, 312(5772), 436–439.

    Article  CAS  Google Scholar 

  20. Zhao, B. T., et al. (2007). Identification of drought-induced microRNAs in rice. Biochemical and Biophysical Research Communications, 354(2), 585–590.

    Article  CAS  Google Scholar 

  21. Zhao, B., et al. (2009). Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Molecular Biology, 10, 29.

    Google Scholar 

  22. Huang, S. Q., et al. (2009). Heavy metal-regulated new microRNAs from rice. Journal of Inorganic Biochemistry, 103(2), 282–287.

    Article  CAS  Google Scholar 

  23. Zhou, X. F., et al. (2008). Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms, 1779(11), 780–788.

    Article  CAS  Google Scholar 

  24. Matsui, A., et al. (2008). Arabidopsis transcriptome analysis under drought, cold, high-salinity and ABA treatment conditions using a tiling array. Plant and Cell Physiology, 49(8), 1135–1149.

    Article  CAS  Google Scholar 

  25. Aprile, A., et al. (2009). Transcriptional profiling in response to terminal drought stress reveals differential responses along the wheat genome. BMC Genomics, 10, 279.

    Article  Google Scholar 

  26. Jones-Rhoades, M. W., & Bartel, D. P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Molecular Cell, 14(6), 787–799.

    Article  CAS  Google Scholar 

  27. Sunkar, R., & Zhu, J. K. (2004). Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell, 16(8), 2001–2019.

    Article  CAS  Google Scholar 

  28. Zhang, B. H., et al. (2005). Identification and characterization of new plant microRNAs using EST analysis. Cell Research, 15(5), 336–360.

    Article  Google Scholar 

  29. Gao, P., et al. (2011). osa-MIR393: A salinity- and alkaline stress-related microRNA gene. Molecular Biology Reports, 38(1), 237–242.

    Article  CAS  Google Scholar 

  30. Sunkar, R., Kapoor, A., & Zhu, J.-K. (2006). Posttranscriptional induction of two Cu/Zn superoxide dismutase genes in Arabidopsis is mediated by downregulation of miR398 and important for oxidative stress tolerance. Plant Cell, 18(8), 2051–2065.

    Article  CAS  Google Scholar 

  31. Andrianov, V., et al. (2010). Tobacco as a production platform for biofuel: Overexpression of Arabidopsis DGAT and LEC2 genes increases accumulation and shifts the composition of lipids in green biomass. Plant Biotechnology Journal, 8, 277–287.

    Article  CAS  Google Scholar 

  32. Zhang, B. H., et al. (2006). Computational identification of microRNAs and their targets. Computational Biology and Chemistry, 30(6), 395–407.

    Article  CAS  Google Scholar 

  33. Frazier, T., et al. (2010). Identification and characterization of microRNAs and their target genes in tobacco (Nicotiana tabacum). Planta, 232(6), 1289–1308.

    Article  CAS  Google Scholar 

  34. Lv, D.-K., et al. (2010). Profiling of cold-stress-responsive miRNAs in rice by microarrays. Gene, 459(1–2), 39–47.

    Article  CAS  Google Scholar 

  35. Jia, X. Y., et al. (2009). Differential and dynamic regulation of miR398 in response to ABA and salt stress in Populus tremula and Arabidopsis thaliana. Plant Molecular Biology, 71(1–2), 51–59.

    Article  CAS  Google Scholar 

  36. Ding, D., et al. (2009). Differential expression of miRNAs in response to salt stress in maize roots. Annals of Botany, 103(1), 29–38.

    Article  CAS  Google Scholar 

  37. Kawashima, C. G., et al. (2009). Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant Journal, 57(2), 313–321.

    Article  CAS  Google Scholar 

  38. Lu, X. Y., & Huang, X. L. (2008). Plant miRNAs and abiotic stress responses. Biochemical and Biophysical Research Communications, 368(3), 458–462.

    Article  CAS  Google Scholar 

  39. Chiou, T. J., et al. (2006). Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell, 18(2), 412–421.

    Article  CAS  Google Scholar 

  40. Pant, B. D., et al. (2008). MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant Journal, 53(5), 731–738.

    Article  CAS  Google Scholar 

  41. Fujii, H., et al. (2005). A miRNA involved in phosphate-starvation response in Arabidopsis. Current Biology, 15(22), 2038–2043.

    Article  CAS  Google Scholar 

  42. Chen, C. F., et al. (2005). Real-time quantification of microRNAs by stem-loop RT-PCR. Nucleic Acids Research, 33(20), e179.

    Article  Google Scholar 

  43. Sunkar, R., & Zhu, J. K. (2007). Micro RNAs and short-interfering RNAs in plants. Journal of Integrative Plant Biology, 49(6), 817–826.

    Article  CAS  Google Scholar 

  44. Liu, D., et al. (2009). Ectopic expression of miR396 suppresses GRF target gene expression and alters leaf growth in Arabidopsis. Physiologia Plantarum, 136(2), 223–236.

    Article  CAS  Google Scholar 

  45. Liu, H.-H., et al. (2008). Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA, 14, 836–843.

    Article  CAS  Google Scholar 

  46. Feng-Xi, Y., & Di-Qiu, Y. (2009). Overexpression of Arabidopsis Mir396 enhances drought tolerance in transgenic tobacco plants. Acta Botanica Yunnanica, 31(5), 421–426.

    Google Scholar 

  47. Gao, P., et al. (2010). Over-expression of osa-MIR396c decreases salt and alkali stress tolerance. Planta, 231, 991–1001.

    Article  CAS  Google Scholar 

  48. Lauter, N., et al. (2005). microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proceedings of the National Academy of Sciences of the United States of America, 102(26), 9412–9417.

    Article  CAS  Google Scholar 

  49. Mlotshwa, S., et al. (2006). Floral patterning defects induced by Arabidopsis APETALA2 and microRNA172 expression in Nicotiana benthamiana. Plant Molecular Biology, 61(4–5), 781–793.

    Article  CAS  Google Scholar 

  50. Li, W.-X., et al. (2008). The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. The Plant Cell, 20, 2238–2251.

    Article  CAS  Google Scholar 

  51. Reyes, J. L., & Chua, N. H. (2007). ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant Journal, 49(4), 592–606.

    Article  CAS  Google Scholar 

  52. Phillips, J. R., Dalmay, T., & Bartels, D. (2007). The role of small RNAs in abiotic stress. FEBS Letters, 581(19), 3592–3597.

    Article  CAS  Google Scholar 

  53. Shukla, L. I., Chinnusamy, V., & Sunkar, R. (2008). The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochimica Et Biophysica Acta-Gene Regulatory Mechanisms, 1779(11), 743–748.

    Article  CAS  Google Scholar 

  54. Yamasaki, H., et al. (2007). Regulation of copper homeostasis by micro-RNA in Arabidopsis. Journal of Biological Chemistry, 282(22), 16369–16378.

    Article  CAS  Google Scholar 

  55. Trindade, I., et al. (2010). miR398 and miR408 are up-regulated in response to water deficit in Medicago truncatula. Planta, 231(3), 705–716.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Baohong Zhang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frazier, T.P., Sun, G., Burklew, C.E. et al. Salt and Drought Stresses Induce the Aberrant Expression of microRNA Genes in Tobacco. Mol Biotechnol 49, 159–165 (2011). https://doi.org/10.1007/s12033-011-9387-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-011-9387-5

Keywords

Navigation