biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 59:99-105, 2015 | DOI: 10.1007/s10535-014-0472-z

Brassinosteroid enhances cytokinin-induced anthocyanin biosynthesis in Arabidopsis seedlings

L. B. Yuan1,2, Z. H. Peng1,2, T. T. Zhi1,2, Z. Zho1,2, Y. Liu1,2, Q. Zhu3, X. Y. Xiong1,3, C. M. Ren1,2,*
1 Hunan Provincial Key Laboratory of Crop Germplasm Innovation and Utilization, Hunan Agricultural University, Changsha, P.R. China
2 College of Bioscience and Biotechnology, Hunan Agricultural University, Changsha, P.R. China
3 College of Horticulture and Landscape, Hunan Agricultural University, Changsha, P.R. China

To investigate whether brassinosteroids (BR) affects cytokinin (CK)-induced anthocyanin biosynthesis, seedlings of the Arabidopsis dwarf4 (dwf4) mutants including partially suppressing coi1 (psc1) and dwf4-102, which are defective in the BR biosynthesis, and the brassinosteroid-insensitive 1-4 (bri1-4) mutant defective in BR signalling were used for the analysis of CK-induced anthocyanin accumulation and the expression of anthocyanin biosynthetic genes and WD-repeat/Myb/bHLH transcription factors. The results show that the CK-induced anthocyanin accumulation was remarkably reduced in dwf4 and bri1-4 mutants, but distinctly increased in the wild type (WT) treated with BR. Moreover, the CK-induced expressions of the late anthocyanin biosynthetic genes including dihydroflavonol reductase, leucoanthocyanidin dioxygenase, and UDP-glucose: flavonoid-3-O-glucosyl transferase were significantly reduced in bri1-4 and dwf4-102 mutants compared to WT. In addition, the expressions of transcription factors production of anthocyanin pigment 1 (PAP1), glabra 3 (GL3), and enhancer of glabra 3 (EGL3) were induced by CK in WT but not in the bri1-4 and dwf4-102 mutants. These results indicate that BR enhanced the CK-induced anthocyanin biosynthesis by up-regulating the late anthocyanin biosynthetic genes and this regulation might be mediated by the transcription factors PAP1, GL3, and EGL3.

Keywords: anthocyanin biosynthetic genes; BRI1; mutants; PSC1, DWF4; WD-repeat, Myb, bHLH transcription factors
Subjects: brassinosteroids; cytokinins; anthocyanin biosynthesis; anthocyanin accumulation; mutants; gene expression; transcription factor

Received: November 6, 2013; Revised: June 26, 2014; Accepted: July 8, 2014; Published: January 1, 2015  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Yuan, L.B., Peng, Z.H., Zhi, T.T., Zho, Z., Liu, Y., Zhu, Q., Xiong, X.Y., & Ren, C.M. (2015). Brassinosteroid enhances cytokinin-induced anthocyanin biosynthesis in Arabidopsis seedlings. Biologia plantarum, 59(1), 99-105. doi: 10.1007/s10535-014-0472-z
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aza-González, C., Herrera-Isidrón, L., Núñez-Palenius, H.G., Martínez de la Vega, O., Ochoa-Alejo, N.: Anthocyanin accumulation and expression analysis of biosynthesisrelated genes during chili pepper fruit development. - Biol. Plant. 57: 49-55, 2013. Go to original source...
    2. Bajguz, A., Hayat, S.: Effects of brassinosteroids on the plant responses to environmental stresses. - Plant Physiol. Biochem. 47: 1-8, 2009. Go to original source...
    3. Cevahir, G., Yentur, S., Eryilmaz, F., Yilmazer, N.: Influence of brassinosteroids on pigment content of Glycine max L. (soybean) grown in dark and light. - J. appl. biol. Sci 2: 23-28, 2008.
    4. Chen, S.M., Li, C.H., Zhu, X.R., Deng, Y.M., Sun, W., Wang, L.S., Chen F.D., Zhang, Z.: The identification of flavonoids and the expression of genes of anthocyanin biosynthesis in the chrysanthemum flowers. - Biol. Plant. 56: 458-464, 2012. Go to original source...
    5. Choe, S., Dilkes, B.P., Fujioka, S., Takatsuto, S., Sakurai, A., Feldmann, K.A.: The DWF4 gene of Arabidopsis encodes a cytochrome P450 that mediates multiple 22α-hydroxylation steps in brassinosteroid biosynthesis. - Plant Cell 10: 231-243, 1998. Go to original source...
    6. Chory, J., Nagpal, P., Peto, C.A.: Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. - Plant Cell 3: 445-459, 1991. Go to original source...
    7. Choudhary, S.P., Yu, J.Q., Yamaguchi-Shinozaki, K., Shinozaki, K., Tran, L.S.P.: Benefits of brassinosteroid crosstalk. - Trends Plant Sci. 17: 594-605, 2012. Go to original source...
    8. Cooney, L.J., Van Klink, J.W., Hughes, N.M., Perry, N.B., Schaefer, H.M., Menzies, I.J., Gould, K.S.: Red leaf margins indicate increased polygodial content and function as visual signals to reduce herbivory in Pseudowintera colorata. - New Phytol. 194: 488-497, 2012. Go to original source...
    9. Dao, T.T.H., Linthorst, H.J.M., Verpoorte, R.: Chalcone synthase and its functions in plant resistance. - Phytochem. Rev. 10: 397-412, 2011. Go to original source...
    10. Das, P.K., Shin, D.H., Choi, S.B., Park, Y.I.: Sugar-hormone cross-talk in anthocyanin biosynthesis. - Mol. Cells 34: 501-507, 2012a. Go to original source...
    11. Das, P.K., Shin, D.H., Choi, S.B., Yoo, S.D., Choi, G., Park, Y.I.: Cytokinins enhance sugar-induced anthocyanin biosynthesis in Arabidopsis. - Mol. Cells 34: 93-101, 2012b. Go to original source...
    12. Deikman, J., Hammer, P.E.: Induction of anthocyanin accumulation by cytokinins in Arabidopsis thaliana. - Plant Physiol. 108: 47-57, 1995. Go to original source...
    13. Farooq, M., Wahid, A., Basra, S.M.A., Islam-ud-Din.: Improving water relations and gas exchange with brassinosteroids in rice under drought stress. - J. Agron. Crop Sci. 195: 262-269, 2009. Go to original source...
    14. Gendron, J.M., Haque, A., Gendron, N., Chang, T., Asami, T., Wang, Z.Y.: Chemical genetic dissection of brassinosteroidethylene interaction. - Mol. Plant 1: 368-379, 2008. Go to original source...
    15. Gonzalez, A., Zhao, M., Leavitt, J.M., Lloyd A.M.: Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. - Plant J. 53: 814-827, 2008. Go to original source...
    16. Gould, K.S.: Nature's Swiss ar my knife: the diverse protective roles of anthocyanins in leaves. - J. Biomed. Biotechnol. 5: 314-320, 2004. Go to original source...
    17. Gould, K.S., Dudle, D.A., Neufeld, H.S.: Why some stems are red: cauline anthocyanins shield photosystem II against high light stress. - J. exp. Bot. 61: 2707-2717, 2010. Go to original source...
    18. Grotewold, E.: The genetics and biochemistry of floral pigments. - Annu. Rev. Plant Biol. 57: 761-780, 2006. Go to original source...
    19. Guo, J., Hu, X., Duan, R.: Interactive effects of cytokinins, light, and sucrose on the phenotypes and the syntheses of anthocyanins and lignins in cytokinin overproducing transgenic Arabidopsis. - J. Plant Growth Regul. 24: 93-101, 2005. Go to original source...
    20. Hatier, J.H.B., Clearwater, M.J., Gould, K.S.: The Functional significance of black-pigmented leaves: photosynthesis, photoprotection and productivity in Ophiopogon planiscapus 'Nigrescens'. - PLoS ONE 8: e67850, 2013. Go to original source...
    21. Hatier, J.H.B., Gould, K.S.: Foliar anthocyanins as modulators of stress signals. - J. theor. Biol. 253: 625-627, 2008. Go to original source...
    22. Holton, T.A., Cornish, E.C.: Genetics and biochemistry of anthocyanin biosynthesis. - Plant Cell 7: 1071-1083, 1995. Go to original source...
    23. Huang, Y., Han, C., Peng, W., Peng, Z., Xiong, X., Zhu, Q., Gao, B., Xie, D., Ren, C.: Brassinosteroid negatively regulates jasmonate inhibition of root growth in Arabidopsis. - Plant Signal. Behav. 5: 140-142, 2010. Go to original source...
    24. Jenkins, G.I., Long, J.C., Wade, H.K., Shenton, M.R., Bibikova, T.N.: UV and blue light signalling: pathways regulating chalcone synthase gene expression in Arabidopsis. - New Phytol. 151: 121-131, 2001. Go to original source...
    25. Jeong, S.W., Das, P.K., Jeoung, S.C., Song, J.Y., Lee, H.K., Kim, Y.K., Kim, W.J., Park, Y.I., Yoo, S.D., Choi, S.B., Choi, G., Park, Y.I.: Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. - Plant Physiol. 154: 1514-1531, 2010. Go to original source...
    26. Koes, R.E., Quattrocchio, F., Mol, J.N.M.: The flavonoid biosynthetic pathway in plants: function and evolution. - Bioessays 16: 123-132, 1994. Go to original source...
    27. Krishna, P.: Brassinosteroid-mediated stress responses. - J. Plant Growth Regul. 22: 289-297, 2003. Go to original source...
    28. Kwon, Y., Oh, J.E., Noh, H., Hong, S.W., Bhoo, S.H., Lee, H.: The ethylene signaling pathway has a negative impact on sucrose-induced anthocyanin accumulation in Arabidopsis. - J. Plant Res. 124: 193-200, 2011. Go to original source...
    29. Laxmi, A., Paul, L.K., Peters, J.L., Khurana, J.P.: Arabidopsis constitutive photomorphogenic mutant, bls1, displays altered brassinosteroid response and sugar sensitivity. - Plant mol. Biol. 56: 185-201, 2004. Go to original source...
    30. Loreti, E., Povero, G., Novi, G., Solfanelli, C., Alpi, A., Perata, P.: Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. - New Phytol. 179: 1004-1016, 2008. Go to original source...
    31. Luan, L.Y., Zhang, Z.W., Xi, Z.M., Huo, S.-S., Ma, L.N.: Brassinosteroids regulate anthocyanin biosynthesis in the ripening of grape berries. - S. Afr. J. Enol. Viticult. 34: 196-203, 2013. Go to original source...
    32. Luccioni, L.G., Oliverio, K.A., Yanovsky, M.J., Boccalandro, H.E., Casal, J.J.: Brassinosteroid mutants uncover fine tuning of phytochrome signaling. - Plant Physiol. 128: 173-181, 2002. Go to original source...
    33. Mehdy, M.C., Lamb, C.J.: Chalcone isomerase cDNA cloning and mRNA induction by fungal elicitor, wounding and infection. - EMBO J. 6: 1527-1533, 1987. Go to original source...
    34. Nagira, Y., Ikegami, K., Koshiba, T., Ozeki, Y.: Effect of ABA upon anthocyanin synthesis in regenerated Torenia shoots. - J Plant Res. 119: 137-144, 2006. Go to original source...
    35. Nakamoto, D., Ikeura, A., Asami, T., Yamamoto, K.T.: Inhibition of brassinosteroid biosynthesis by either a dwarf4 mutation or a brassinosteroid biosynthesis inhibitor rescues defects in tropic responses of hypocotyls in the Arabidopsis mutant nonphototropic hypocotyl 4. - Plant Physiol. 141: 456-464, 2006. Go to original source...
    36. Noguchi, T., Fujioka, S., Choe, S., Takatsuto, S., Yoshida, S., Yuan, H., Feldmann, K.A., Tax, F.E.: Brassinosteroid insensitive dwarf mutants of Arabidopsis accumulate brassinosteroids. - Plant Physiol. 121: 743-752, 1999. Go to original source...
    37. Pelletier, M.K., Murrell, J.R., Shirley, B.W.: Characterization of flavonol synthase and leucoanthocyanidin dioxygenase genes in Arabidopsis (further evidence for differential regulation of "early" and "late" genes). - Plant Physiol. 113: 1437-1445, 1997. Go to original source...
    38. Peng, Z., Han, C., Yuan, L., Zhang, K., Huang, H., Ren, C.: Brassinosteroid enhances jasmonate-induced anthocyanin accumulation in Arabidopsis seedlings. - J. Integr. Plant Biol. 53: 632-640, 2011. Go to original source...
    39. Qi, T., Song, S., Ren, Q., Wu, D., Huang, H., Chen, Y., Fan, M., Peng, W., Ren, C., Xie, D.: The jasmonate-ZIM-domain proteins interact with the WD-repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. - Plant Cell 23: 1795-1814, 2011. Go to original source...
    40. Ren, C., Han, C., Peng, W., Huang, Y., Peng, Z., Xiong, X., Zhu, Q., Gao, B., Xie, D.: A leaky mutation in DWARF4 reveals an antagonistic role of brassinosteroid in the inhibition of root growth by jasmonate in Arabidopsis. - Plant Physiol. 151: 1412-1420, 2009. Go to original source...
    41. Sasse, J.M.: Physiological actions of brassinosteroids: an update. - J. Plant Growth Regul. 22: 276-288, 2003. Go to original source...
    42. Shan, X., Zhang, Y., Peng, W., Wang, Z., Xie, D.: Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. - J. exp. Bot. 60: 3849-3860, 2009. Go to original source...
    43. Shin, D.H., Choi, M., Kim, K., Bang, G., Cho, M., Choi, S.B., Choi, G., Park, Y.I.: HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis, - FEBS Lett. 587: 1543-1547, 2013. Go to original source...
    44. Solfanelli, C., Poggi, A., Loreti, E., Alpi, A., Perata, P.: Sucrose-specific induction of the anthocyanin biosynthetic pathway in Arabidopsis. - Plant Physiol. 140: 637-646, 2006. Go to original source...
    45. Springob, K., Nakajima, J., Yamazaki, M., Saito, K.: Recent advances in the biosynthesis and accumulation of anthocyanins. - Natur. Prod. Rep. 20: 288-303, 2003. Go to original source...
    46. Symons, G.M., Davies, C., Shavrukov, Y., Dry, I.B., Reid, J.B., Thomas, M.R.: Grapes on steroids. Brassinosteroids are involved in grape berry ripening. - Plant Physiol. 140: 150-158, 2006. Go to original source...
    47. Szekeres, M., Németh, K., Koncz-Kálmán, Z., Mathur, J., Kauschmann, A., Altmann, T., Rédei, G.P., Nagy, F., Schell, J., Koncz, C.: Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. - Cell 85: 171-182, 1996. Go to original source...
    48. Teng, S., Keurentjes, J., Bentsink, L., Koornneef, M., Smeekens, S.: Sucrose-specific induction of anthocyanin biosynthesis in Arabidopsis requires the MYB75/PAP1 gene. - Plant Physiol. 139: 1840-1852, 2005. Go to original source...
    49. Treutter, D.: Significance of flavonoids in plant resistance and enhancement of their biosynthesis. - Plant Biol. 7: 581-591, 2005. Go to original source...
    50. Winkel-Shirley, B.: Biosynthesis of flavonoids and effects of stress. - Curr. Opin. Plant Biol. 5: 218-223, 2002. Go to original source...
    51. Yokota, T.: The structure, biosynthesis and function of brassinosteroids. - Trends Plant Sci. 2: 137-143, 1997. Go to original source...

    Return to the content