Biologia plantarum 58:491-498, 2014 | DOI: 10.1007/s10535-014-0426-5

Copper stress induces the differential expression of microRNAs in non-heading Chinese cabbage

J. Ren1, J. J. Zhou1, W. K. Duan1, X. M. Song1, T. K. Liu1, X. L. Hou1, Y. Li1,*
1 Horticultural Department, Nanjing Agricultural University, State Key Laboratory of Crop Genetics & Germplasm Enhancement, and Key Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, Nanjing, P.R. China

To gain a deep understanding of the regulatory mechanism of Cu-responsive microRNAs (miRNAs) in non-heading Chinese cabbage (Brassica campestris ssp. chinensis Makino), the transcription of 10 annotated stress-inducible miRNAs and their target genes were investigated in two cultivars Suzhouqing and Wutacai exposed to excess of copper. Results show that these miRNAs were negatively correlated with their target genes under the Cu stress and showed different transcriptions in different tissues and cultivars. The transcriptions of bra-miR1530a and bra-miR1533v were highest in petioles and lowest in roots. Bra-miR1533ah, bra-miR1533m, bra-miR1533t, bra-miR414a, and bra-miR398b had the highest and lowest transcriptions in leaves and roots, respectively. In contrast, the transcription of bra-miR172f was highest in roots and lowest in leaves. Bra-miR1533aj and bra-miR1533d had similar transcriptions in petioles and leaves. The promoter analysis further revealed that seven miRNAs contained the Cu-response element (CuRE). In addition, miRNAs with more CuREs in the 5'-flanking sequences showed a lower expression following the Cu treatment. It imply that CuREs likely played a role in increasing the response to Cu in non-heading Chinese cabbage.

Keywords: Brassica campestris, cis-responsive element; Cu-response element
Subjects: copper; miRNA; cis-responsing element; gene expression; target genes; regulatory mechanism; Chinese cabbage

Received: July 20, 2013; Revised: March 4, 2014; Accepted: March 24, 2014; Published: September 1, 2014Show citation

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Ren, J., Zhou, J.J., Duan, W.K., Song, X.M., Liu, T.K., Hou, X.L., & Li, Y. (2014). Copper stress induces the differential expression of microRNAs in non-heading Chinese cabbage. Biologia plantarum, 58(3), 491-498. doi: 10.1007/s10535-014-0426-5.
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    References

    1. Alonso-Peral, M.M., Li, J., Li, Y., Allen, R.S., Schnippenkoetter, W., Ohms, S., White, R.G., Millar, A.A.: The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. - Plant Physiol. 154: 757-771, 2010. Go to original source...
    2. Bartel, D.P.: MicroRNAs: genomics, biogenesis, mechanism and function. - Cell 116: 281-297, 2004. Go to original source...
    3. Chapman, E.J., Carrington, J.C.: Specialization and evolution of endogenous small RNA pathways. - Nature Rev. Genet. 8: 884-896, 2007. Go to original source...
    4. Chuck, G., Cigan, A.M., Saeteurn, K., Hake, S.: The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. - Nat. Genet. 39: 544-549, 2007. Go to original source...
    5. De Lima, J.C., Loss-Morais, G., Margis, R.: MicroRNAs play critical roles during plant development and in response to abiotic stresses. - Genet. mol. Biol. 35(4 Suppl): 1069-1077, 2012.
    6. Dieterich, C., Grossmann, S., Tanzer, A., Röpcke, S., Arndt, P.F., Stadler, P.F., Vingron, M.: Comparative promoter region analysis powered by CORG. - BMC Genomics 6: 24, 2005. Go to original source...
    7. Ding, D., Zhang, L.F., Wang, H., Liu, Z., Zhang, Z.X., Zheng, Y.L.: Differential expression of miRNAs in response to salt stress in maize roots. - Ann. Bot. 103: 29-38, 2009. Go to original source...
    8. Guo, H.S., Xie, Q., Fei, J.F., Chua, N.H.: MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. - Plant Cell 17: 1376-1386, 2005. Go to original source...
    9. Guo, S.R.: Nutrient solution. - In: Guo, S.R. (ed.): Soilless Cultivation Science. Pp. 111-115. China Agricultural Press, Beijing 2003.
    10. Jones-Rhoades, M.W., Bartel, D.P.: Computational identification of plant microRNAs and their targets, including a stress induced miRNA. - Mol. Cell 14: 787-799, 2004. Go to original source...
    11. Kozomara, A., Griffiths-Jones, S.: MiRBase: annotating high confidence microRNAs using deep sequencing data. - Nucl. Acids Res. 42: D68-D73, 2014. Go to original source...
    12. Ku, H.M., Tan, C.W., Su, Y.S., Chiu, C.Y., Chen, C.T., Jan, F.J.: The effect of water deficit and excess copper on proline metabolism in Nicotiana benthamiana. - Biol. Plant. 56: 337-343, 2012. Go to original source...
    13. Lauter, N., Kampani, A., Carlson, S., Goebel, M., Moose, S.P.: MicroRNA172 down-regulates glossy15 to promote vegetative phase change in maize. - Proc. nat. Acad. Sci. USA. 102: 9412-9417, 2005. Go to original source...
    14. Lescot, M., Dehais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouzé, P., Rombauts, S.: PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. - Nucl. Acids Res. 30: 325-327, 2002. Go to original source...
    15. Li, Y., Song, Y.P., Shi, G.J., Wang, J.J., Hou, X.L.: Response of antioxidant activity to excess copper in two cultivars of Brassica campestris ssp. chinensis Makino. - Acta Physiol. Plant 31: 155-162, 2009. Go to original source...
    16. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method, - Methods 25: 402-408, 2001. Go to original source...
    17. Lu, S.F., Sun, Y.H., Chiang, V.L.: Stress-responsive microRNA in Populus. - Plant J. 55: 131-151, 2008. Go to original source...
    18. Lu, S.F., Sun, Y.H., Shi, R., Clark, C., Li, L., Chiang, V.L.: Novel and mechanical stress-responsive microRNA in Populus trichocarpa that are absent from Arabidopsis. - Plant Cell 17: 2186-2203, 2005. Go to original source...
    19. Lu, S.F., Yang, C.M., Chiang, V.L.: Conservation and diversity of microRNA-associated copper-regulatory networks in Populus trichocarpa. - J. Integr. Plant Biol. 53: 879-891, 2011. Go to original source...
    20. Millar, A.A., Gubler, F.: The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulate genes that redundantly facilitate anther development. - Plant Cell 17: 705-721, 2005. Go to original source...
    21. Min, H.L., Cai, S.J., Rui, Z., Sha, S., Xie, K.B., Xu, Q.S.: Calcium-mediated enhancement of copper tolerance in Elodea canadensis. - Biol. Plant. 57: 365-369, 2013. Go to original source...
    22. Nagae, M., Nakata, M., Takahashi, Y.: Identification of negative cis-acting elements in response to copper in the chloroplastic iron superoxide dismutase gene of the moss Barbula unguiculata. - Plant Physiol. 146: 1687-1696, 2008. Go to original source...
    23. Pant, B.D., Musialak-Lange, M., Nuc, P., May, P., Buhtz, A., Kehr, J., Walther, D., Scheible, W.R.: Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. - Plant Physiol. 150: 1541-1555, 2009. Go to original source...
    24. Quinn, J.M., Barraco, P., Eriksson, M., Merchant, S.: Coordinate copper- and oxygen-responsive Cyc6 and Cpx1 expression in Chlamydomonas is mediated by the same element. - J. biol. Chem. 275: 6080-6089, 2000. Go to original source...
    25. Quinn, J.M., Merchant, S.: Two copper-responsive elements associated with the Chlamydomonas Cyc6 gene function as targets for transcriptional activators. - Plant Cell 7: 623-628, 1995. Go to original source...
    26. Robertus, J.L., Harms, G., Blokzijl, T., Booman, M., Jong, D.D., Imhoff, G.V., Rosati, S., Schuuring, E., Kluin, P., Berg, A.V.D.: Specific expression of miR-17-5p and miR-127 in testicular and central nervous system diffuse large B-cell lymphoma. - Mod. Pathol. 22: 547-555, 2009. Go to original source...
    27. Song, J., Yang, Y.Q., Zhu, S.H., Chen, G.C., Yuan, X.F., Liu, T.T., Yu, X.H., Shi, J.Y.: Spatial distribution and speciation of copper in root tips of cucumber revealed by μ-XRF and of copper in root tips of cucumber revealed by μ-XRF and μ-XANES. - Biol. Plant. 57: 581-586, 2013a. Go to original source...
    28. Song, X.M., Li, Y., Hou, X.L.: Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis). - BMC Genomics 14: 573, 2013b. Go to original source...
    29. Sunkar, R., Chinnusamy, V., Zhu, J., Zhu, J.K.: Small RNAs as big players in plant abiotic stress responses and nutrient deprivation. - Trends Plan Sci. 12: 301-309, 2007. Go to original source...
    30. Sunkar, R., Kapoor, A., Zhu, J.K.: 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: 2051-2065, 2006. Go to original source...
    31. Sunkar, R., Zhou, X., Zheng, Y., Zhang, W.X., Zhu, J.K.: Identification of novel and candidate miRNAs in rice by high throughput sequencing. - BMC Plant Biol. 8: 1-10, 2008. Go to original source...
    32. Wang, J.Y., Hou, X.L., Yang, X.D.: Identification of conserved microRNAs and their targets in Chinese cabbage (Brassica rapa ssp. pekinensis). - Genome 54: 1029-1040, 2011. Go to original source...
    33. Waters, B.M., Mclnturf, S.A., Stein, R.J.: Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arobidopsis thaliana. - J. exp. Bot. 63: 5903-5918, 2012. Go to original source...
    34. Xiao, D., Zhang, N.W., Zhao, J.J., Guusje, B., Hou, X.L.: Validation of reference genes for quantitative PCR normalization in non-heading Chinese cabbage. - Funct. Plant Biol. 39: 342-350, 2012. Go to original source...
    35. Yamasaki, H., Abdel-Ghany S.E., Cohu, C.M., Kobayashi, Y., Shikanai, T., Pilon, M.: Regulation of copper homeostasis by micro-RNA in Arabidopsis. - J. biol. Chem. 282: 16369-16378, 2007. Go to original source...
    36. Yin, Z.J., Li, Y., Han X.L., Shen, F.F.: Genome-wide profiling of miRNAs and other small non-coding RNAs in the Verticillium dahliae -inoculated cotton roots. - PloS ONE 7(4): e35756, 2012. Go to original source...
    37. Zeng, H.Q., Zhu, Y.Y., Huang, S.Q., Yang, Z.M.: Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). - J. Plant Physiol. 167: 1289-1297, 2010. Go to original source...
    38. Zhao, B., Liang, R., Ge, L., Li, W., Xiao, H., Lin, H., Ruan, K., Jin, Y.: Identification of drought-induced microRNAs in rice. - Biochem. biophys. Res. Commun. 354: 585-590, 2007. Go to original source...
    39. Zhou, L., Liu, Y., Liu, Z.C., Kong, D., Duan, M., Luo, L.J.: Genome-wide identification and analysis of droughtresponsive microRNAs in Oryza sativa. - J. Exp. Bot. 61: 4157-4168, 2010. Go to original source...
    40. Zhou, X.F., Wang, G.D., Sutoh, K., Zhu, J.K., Zhang, W.X.: Identification of cold-inducible microRNAs in plants by transcriptome analysis. - BBA 1779: 780-788, 2008. Go to original source...
    41. Zhou, X.F., Wang, G.D., Zhang, W.X.: UV-B responsive microRNA genes in Arabidopsis thaliana. - Mol. syst. Biol. 3: 103-115, 2007. Go to original source...

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