Skip to main content

Advertisement

Log in

Computational Identification of MicroRNAs and Their Targets in Cassava (Manihot esculenta Crantz.)

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

Abstract

MicroRNAs (miRNAs) are a newly discovered class of noncoding endogenous small RNAs involved in plant growth and development as well as response to environmental stresses. miRNAs have been extensively studied in various plant species, however, only few information are available in cassava, which serves as one of the staple food crops, a biofuel crop, animal feed and industrial raw materials. In this study, the 169 potential cassava miRNAs belonging to 34 miRNA families were identified by computational approach. Interestingly, mes-miR319b was represented as the first putative mirtron demonstrated in cassava. A total of 15 miRNA clusters involving 7 miRNA families, and 12 pairs of sense and antisense strand cassava miRNAs belonging to six different miRNA families were discovered. Prediction of potential miRNA target genes revealed their functions involved in various important plant biological processes. The cis-regulatory elements relevant to drought stress and plant hormone response were identified in the promoter regions of those miRNA genes. The results provided a foundation for further investigation of the functional role of known transcription factors in the regulation of cassava miRNAs. The better understandings of the complexity of miRNA-mediated genes network in cassava would unravel cassava complex biology in storage root development and in coping with environmental stresses, thus providing more insights for future exploitation in cassava improvement.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.

    Article  CAS  Google Scholar 

  2. Carthew, R. W., & Sontheimer, E. J. (2009). Origins and mechanisms of miRNAs and siRNAs. Cell, 136, 642–655.

    Article  CAS  Google Scholar 

  3. Jones-Rhoades, M. W., Bartel, D. P., & Bartel, B. (2006). MicroRNAs and their regulatory roles in plants. Annual Review plant Biology, 57, 19–53.

    Article  CAS  Google Scholar 

  4. Zhang, B. H., Pan, X. P., Cobb, G. P., & Anderson, T. A. (2006). Plant microRNA: a small regulatory molecule with big impact. Developmental Biology, 289, 3–16.

    Article  CAS  Google Scholar 

  5. Dugas, D. V., & Bartel, B. (2004). MicroRNA regulation of gene expression in plants. Current Opinion in Plant Biology, 7, 512–520.

    Article  CAS  Google Scholar 

  6. Chen, X. (2005). MicroRNA biogenesis and function in plants. FEBS Letters, 579, 5923–5931.

    Article  CAS  Google Scholar 

  7. Cui, X., Xu, S. M., Mu, D. S., & Yang, Z. M. (2009). Genomic analysis of rice microRNA promoters and clusters. Gene, 431, 61–66.

    Article  CAS  Google Scholar 

  8. Lee, Y., Kim, M., Han, J., Yeom, K., Lee, S., et al. (2004). MicroRNA genes are transcribed by RNA polymeraseII. EMBO Journal, 23, 4051–4060.

    Article  CAS  Google Scholar 

  9. Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B., & Bartel, D. P. (2002). Micro-RNAs in plants. Genes and Development, 16, 1616–1626.

    Article  CAS  Google Scholar 

  10. Papp, I., Mette, M. F., Aufsatz, W., Daxinger, L., Schauer, S. E., et al. (2003). Evidence for nuclear processing of plant microRNA and short interfering RNA precursors. Plant Physiology, 132, 1382–1390.

    Article  CAS  Google Scholar 

  11. Park, M. Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H., & Poethig, R. S. (2005). Nuclear processing and export of microRNAs in Arabidopsis. Proceedings National Academy Sciences, 102, 3691–3696.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Adai, A., Johnson, C., & Mlotshwa, S. (2005). Computational prediction of miRNAs in Arabidopsis thaliana. Genome Research, 15, 78–91.

    Article  CAS  Google Scholar 

  14. Zhang, B. H., Pan, X. P., & Anderson, T. A. (2006). Identification of 188 conserved maize microRNAs and their targets. FEBS Letters, 580, 3753–3762.

    Article  CAS  Google Scholar 

  15. Zhang, B. H., Wang, Q. L., Wang, K. B., Pan, X. P., Liu, F., et al. (2007). Identification of cotton microRNAs and their targets. Gene, 397, 26–37.

    Article  CAS  Google Scholar 

  16. Yin, Z., Li, C., Han, X., & Shen, F. (2008). Identification of conserved microRNAs and their target genes in tomato (Lycopersicon esculentum). Gene, 414, 60–66.

    Article  CAS  Google Scholar 

  17. Song, C., Fang, J., Li, X., Liu, H., & Chao, C. T. (2009). Identification and characterization of 27 conserved microRNAs in citrus. Planta, 230, 671–685.

    Article  CAS  Google Scholar 

  18. Xie, F., Frazier, T. P., & Zhang, B. (2011). Identification, characterization and expression analysis of microRNAs and their targets in the potato (Solanum tuberosum). Gene, 473, 8–22.

    Article  CAS  Google Scholar 

  19. Dhandapani, V., Ramchiary, N., Paul, P., Kim, J., Choi, S. H., et al. (2011). Identification of potential microRNAs and their targets in Brassica rapa L. Molecules and Cells, 32, 21–37.

    Article  CAS  Google Scholar 

  20. Li, B., Qin, Y., Duan, H., Yin, W., & Xia, X. (2011). Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. Journal of Experimental Botany. doi:10.1093/jxb/err051.

    Google Scholar 

  21. Meyers, B. C., Axtell, M. J., Bartel, B., Bartel, D. P., Baulcombe, D., et al. (2008). Criteria for annotation of plant microRNAs. Plant Cell, 20, 3186–3190.

    Article  CAS  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 Research, 15, 336–360.

    Article  Google Scholar 

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

    Article  Google Scholar 

  24. Feng, D. J., Jun, W. Y., Feng, F. X., Xia, C. J., Liang, Z., et al. (2010). Prediction of sorghum miRNAs and their targets with computational methods. Chinese Science Bulletin, 55, 1263–1270.

    Article  Google Scholar 

  25. Lu, Y., & Yang, X. (2010). Computational identification of novel microRNAs and their targets in Vigna unguiculata. Comparative and Functional Genomics, 2010, 1–17.

    Article  Google Scholar 

  26. Frazier, T. P., Xie, F., Freistaedter, A., Burklew, C. E., & Zhang, B. (2010). Identification and characterization of microRNAs and their target genes in tobacco (Nicotiana tabacum). Planta, 232, 1289–1308.

    Article  CAS  Google Scholar 

  27. Xie, F., Frazier, T. P., & Zhang, B. (2010). Identification and characterization of microRNAs and their targets in the bioenergy plant switchgrass (Panicum virgatum). Planta, 232, 417–434.

    Article  CAS  Google Scholar 

  28. Bonnet, E., Wuyts, J., Rouze, P., & Van de Peer, Y. (2004). Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences. Bioinformatics, 20, 2911–2917.

    Article  CAS  Google Scholar 

  29. Rhoades, M. W., Reinhart, B. J., Lim, L. P., Burge, C. B., Bartel, B., et al. (2002). Prediction of plant microRNA targets. Cell, 110, 513–520.

    Article  CAS  Google Scholar 

  30. Schwab, R., Palatnik, J. F., Riester, M., Schommer, C., Schmid, M., et al. (2005). Specific effects of microRNAs on the plant transcriptome. Developmental Cell, 8, 517–527.

    Article  CAS  Google Scholar 

  31. Lewis, R., Mendu, V., Mcnear, D., & Tang, G. (2010). Roles of microRNAs in plant abiotic stress. In S. M. Jain & D. S. Brar (Eds.), Molecular techniques in crop improvement (2nd ed., pp. 357–372). Cambridge, MA: Springer.

    Chapter  Google Scholar 

  32. Griffiths-Jones, S. (2006). miRBase: the microRNA sequence database. Methods in Molecular Biology, 342, 129–138.

    CAS  Google Scholar 

  33. Griffiths-Jones, S., Saini, H. K., Van Dongen, S., & Enright, A. J. (2008). miRBase: tools for microRNA genomics. Nucleic Acids Research, 36, D154–D158.

    Article  CAS  Google Scholar 

  34. Hofacker, I. L. (2003). Vienna RNA secondary structure server. Nucleic Acids Research, 31, 3429–3431.

    Article  CAS  Google Scholar 

  35. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Research, 31, 3406–3434.

    Article  CAS  Google Scholar 

  36. Zuker, M., & Stiegler, P. (1981). Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Research, 9, 133–148.

    Article  CAS  Google Scholar 

  37. Dai, X., & Zhao, P. X. (2011). psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research, 39, W155–W159.

    Article  CAS  Google Scholar 

  38. Megraw, M., Baev, V., & Rusinov, V. (2006). MicroRNA promoter element discovery in Arabidopsis. RNA, 12, 1612–1619.

    Article  CAS  Google Scholar 

  39. Meng, Y., Shao, C., & Chen, M. (2011). Toward microRNA-mediated gene regulatory networks in plants. Brief Bioinformatics. doi:10.1093/bib/bbq091.

    Google Scholar 

  40. Zhou, L., Liu, Y., Liu, Z., Kong, D., Duan, M., et al. (2010). Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. Journal of Experimental Botany, 61, 4157–4168.

    Article  CAS  Google Scholar 

  41. Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., et al. (2002). PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30, 325–327.

    Article  CAS  Google Scholar 

  42. Higo, K., Ugawa, Y., Iwamoto, M., & Korenaga, T. (1999). Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nucleic Acids Research, 27, 297–300.

    Article  CAS  Google Scholar 

  43. Zeng, C., Wang, W., Zheng, Y., Chen, X., Bo, W., et al. (2009). Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants. Nucleic Acids Research, 38, 981–995.

    Article  Google Scholar 

  44. Amiteye, S., Corral, J. M., & Sharbel, T. F. (2011). Overview of the potential of microRNAs and their target gene detection for cassava (Manihot esculenta) improvement. African Journal of Biotechnology, 11, 2562–2573.

    Google Scholar 

  45. Unver, T., Parmaksız, İ., & Dündar, E. (2010). Identification of conserved micro-RNAs and their target transcripts in opium poppy (Papaver somniferum L.). Plant Cell Reports, 29, 757–769.

    Article  CAS  Google Scholar 

  46. Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., et al. (2008). Sorting of small RNAs into Arabidopsis Argonaute complexes is directed by the 5′ terminal nucleotide. Cell, 133, 116–127.

    Article  CAS  Google Scholar 

  47. Zhang, B. H., Pan, X. P., & Stellwag, E. J. (2008). Identification of soybean microRNAs and their targets. Planta, 229, 161–182.

    Article  CAS  Google Scholar 

  48. Okamura, K., Hagen, J. W., Duan, H., Tyler, D. M., & Lai, E. C. (2007). The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell, 130, 89–100.

    Article  CAS  Google Scholar 

  49. Ruby, J. G., Jan, C. H., & Bartel, D. P. (2007). Intronic microRNA precursors that bypass Drosha processing. Nature, 448, 83–86.

    Article  CAS  Google Scholar 

  50. Moreno, M. A., Harper, L. C., Krueger, R. W., Dellaporta, S. L., & Freeling, M. (1997). Liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis. Genes and Development, 11, 616–628.

    Article  CAS  Google Scholar 

  51. Peter, M. E. (2010). Targeting of mRNAs by multiple miRNAs: the next step. Oncogene, 29, 2161–2164.

    Article  CAS  Google Scholar 

  52. Yin, Z., & Shen, F. (2010). Identification and characterization of conserved microRNAs and their target genes in wheat (Triticum aestivum). General Molecular Research, 9, 1186–1196.

    Article  CAS  Google Scholar 

  53. Wu, S., Huang, S., Ding, J., Zhao, Y., Liang, L., et al. (2010). Multiple microRNAs modulate p21Cip1/Waf1 expression by directly targeting its 3′ untranslated region. Oncogene, 29, 2302–2308.

    Article  CAS  Google Scholar 

  54. Dubos, C., Stracke, R., Grotewold, E., Weisshaar, B., Martin, C., et al. (2010). MYB transcription factors in Arabidopsis. Trends in Plant Science, 15, 573–581.

    Article  CAS  Google Scholar 

  55. Lin-Wang, K., Bolitho, K., Grafton, K., Kortstee, A., Karunairetnam, S., et al. (2010). An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biology, 10, 50.

    Article  Google Scholar 

  56. Wang, D., Pei, K., Fu, Y., Sun, Z., Li, S., et al. (2007). Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene, 394, 13–24.

    Article  CAS  Google Scholar 

  57. Jofuku, K. D., Boer, B., Montagu, M. V., & Okamuro, J. K. (1994). Control of Arabidopsis flower and seed development by the Homeotic Gene APETALA2. Plant Cell, 6, 1211–1225.

    CAS  Google Scholar 

  58. Mlotshwa, S., Ynag, Z., Kim, Y., & Chen, X. (2006). Floral patterning defects induced by Arabidopsis APETALA2 and microRNA172 expression in Nicotiana benthamiana. Plant Molecular Biology, 61, 781–793.

    Article  CAS  Google Scholar 

  59. Rizhsky, L., Davletova, S., Liang, H., & Mittlers, R. (2004). The zinc finger protein zat12 is required for cytosolic Ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. Journal of Biological Chemistry, 279, 11736–11743.

    Article  CAS  Google Scholar 

  60. Achard, P., Herr, A., Baulcombe, D. C., & Harberd, N. P. (2004). Modulation of floral development by a gibberellin-regulated microRNA. Development, 131, 3357–3365.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was financially supported by Mahidol University. OP was partially supported by Center of Excellence on Agricultural Biotechnology, Science and Technology Postgraduate Education and Research Development Office, Commission on Higher Education, Ministry of Education (AG-BIO/PERDO-CHE), Thailand.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jarunya Narangajavana.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 348 kb)

Supplementary material 2 (XLS 263 kb)

12033_2012_9521_MOESM3_ESM.pdf

Supplement Figure S1 Predicted secondary hairpin structure for 169 cassava miRNAs identified in this study. (PDF 2073 kb)

12033_2012_9521_MOESM4_ESM.tif

Supplement Figure S2 Relative transcript abundance of miR159 in the fibrous and storage root. The relative expression corresponds to the ratio of the transcript abundance of miR159 gene/transcript abundance of the small RNA U6 control gene. Data are means of three independent experiments and SE (n = 9). Different letters indicate values that are significantly different between the transcripts of the fibrous and storage root cDNA samples (Tukey’s test, one-way ANOVA; P < 0.05). (TIFF 677 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Patanun, O., Lertpanyasampatha, M., Sojikul, P. et al. Computational Identification of MicroRNAs and Their Targets in Cassava (Manihot esculenta Crantz.). Mol Biotechnol 53, 257–269 (2013). https://doi.org/10.1007/s12033-012-9521-z

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-012-9521-z

Keywords

Navigation