Biologia plantarum 2019, 63:343-353 | DOI: 10.32615/bp.2019.040

Gibberellin A3 mediated decreased transcriptional rate, mRNA stability and non-competitive inhibition of DNA methyltransferases in tobacco

R. Manoharlal*, G.V.S. Saiprasad, V. Kaikala
Corporate R&D (Agrisciences), ITC Limited, ITC Life Science and Technology Centre (LSTC), Peenya Industrial Area, Bengaluru-560058, Karnataka, India

The present work aims to examine the underlying molecular mechanism(s) for the reduced transcriptions and activities of DNA methyltransferases (NtDNMTs) by gibberellin A3 (GA3) in tobacco (Nicotiana tabacum L). Nuclear run-on and cordycepin chase assays demonstrated a significant reduction in the transcriptional rate and transcript half-lives of NtMET1 and NtCMT3 by GA3. Lineweaver-Burk plot analysis revealed a non-competitive mode of inhibition of NtDNMTs activity by GA3. Taken together, both in vivo and in vitro studies clearly demonstrated the altered transcriptional and post-transcriptional regulation as a mechanism of inhibition in expression and activity of NtDNMTs by GA3.

Keywords: Nicotiana tabacum, nuclear run-on, transcriptional and post-transcriptional regulation

Accepted: January 9, 2019; Prepublished online: January 9, 2019; Published: January 19, 2019Show citation

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Manoharlal, R., Saiprasad, G.V.S., & Kaikala, V. (2019). Gibberellin A3 mediated decreased transcriptional rate, mRNA stability and non-competitive inhibition of DNA methyltransferases in tobacco. Biologia plantarum, 63(1), 343-353. doi: 10.32615/bp.2019.040.
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    References

    1. Adams, R., Rinaldi, A., Seivwright, C.: Microassay for DNA methyltransferase. - J. biochem. biophys. Methods 22: 19-22, 1991. Go to original source...
    2. Ahmad, F., Huang, X., Lan, H.X., Huma, T., Bao, Y.M., Huang, J., Zhang, H.S.: Comprehensive gene expression analysis of the DNA (cytosine-5) methyltransferase family in rice (Oryza sativa L.). - Genet. mol. Res. 13: 5159-5172, 2014. Go to original source...
    3. Arase, S., Kasai, M., Kanazawa, A.: In planta assays involving epigenetically silenced genes reveal inhibition of cytosine methylation by genistein. - Plant Methods 8: 10. 2012. Go to original source...
    4. Bartels, A., Han, Q., Nair, P., Stacey, L., Gaynier, H., Mosley, M., Huang, Q., Pearson, J., Hsieh, T., An, Y., Xiao, W.: Dynamic DNA methylation in plant growth and development. - Int. J. mol. Sci. 19: 21-44, 2018. Go to original source...
    5. Belinsky, S.A., Nikula, K.J., Baylin, S.B., Issa, J.: Increased cytosine DNA-methyltransferase activity is target-cell-specific and an early event in lung cancer. - Proc. nat. Acad. Sci. USA. 93: 4045-4050, 1996. Go to original source...
    6. Brian, P.W., Hemming, H.G., Lowe, D.: Inhibition of rooting of cuttings by gibberellic acid. - Ann. Bot. 24: 407-419, 1960. Go to original source...
    7. Cao, L., Yu, N., Li, J., Qi, Z., Wang, D., Chen, L.: Heritability and reversibility of DNA methylation induced by in vitro grafting between Brassica juncea and B. oleracea. - Sci. Rep. 6: 27233, 2016. Go to original source...
    8. Fang, M.Z., Wang, Y., Ai, N., Hou, Z., Sun, Y., Lu, H., Welsh, W., Yang, C.S.: Tea polyphenol (-)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. - Cancer Res. 63: 7563-7570, 2003.
    9. Gao, Z., Meng, C., Gao, H., Li, Y., Zhang, X., Xu, D., Zhou, S., Liu, B., Su, Y., Ye, N.: Carotenoid genes transcriptional regulation for astaxanthin accumulation in fresh water unicellular alga Haematococcus pluvialis by gibberellin A3 (GA3). - Ind. J. Biochem. Biophys. 50: 548-553, 2013.
    10. Gubler, F., Chandler, P.M., White, R.G., Llewellyn, D.J., Jacobsen, J.V.: Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. - Plant Physiol. 129: 191-200, 2002. Go to original source...
    11. Gutiérrez, R.A., Ewing, R.M., Cherry, J.M., Green, P.J.: Identification of unstable transcripts in Arabidopsis by cDNA microarray analysis: rapid decay is associated with a group of touch-and specific clock-controlled genes. - Proc. nat. Acad. Sci. USA. 99: 11513-11518, 2002. Go to original source...
    12. Hamilton, R.H., Künsch, U., Temperli, A.: Simple rapid procedures for isolation of tobacco leaf nuclei. - Anal. Biochem. 49: 48-57, 1972. Go to original source...
    13. Hauvermale, A.L., Ariizumi, T., Steber, C.M.: Gibberellin Signaling: A theme and variations on DELLA repression. - Plant Physiol. 160: 83-92, 2012. Go to original source...
    14. Hedden, P., Phillips, A.L.: Gibberellin metabolism: new insights revealed by the genes. - Trends Plant Sci. 5: 523-530, 2000. Go to original source...
    15. Jennings, R.: Gibberellin antagonism by material from a brown alga. - New Phytol. 68: 683-688, 1969. Go to original source...
    16. Jones, W.K., Grupp, I.L., Doetschman, T., Grupp, G., Osinska, H., Hewett, T.E., Boivin, G., Gulick, J., Ng, W.A., Robbins, J.: Ablation of the murine α myosin heavy chain gene leads to dosage effects and functional deficits in the heart. - J. clin. Invest. 98: 1906, 1996.
    17. Kalantidis, K., Psaradakis, S., Tabler, M., Tsagris, M.: The Occurrence of CMV-specific short rnas in transgenic tobacco expressing virus-derived double-stranded RNA is indicative of resistance to the virus. - Mol. Plant-Microbe Interact. 15: 826-833, 2002. Go to original source...
    18. Kanazawa, A., O'Dell, M., Hellens, R.P., Hitchin, E., Metzlaff, M.: Mini-scale method for nuclear run-on transcription assay in plants. - Plant mol. Biol. Rep. 18: 377-383, 2000. Go to original source...
    19. Kim, H., Yano, A., Wada, Y., Sano, H.: Properties of a tobacco DNA methyltransferase, NtMET1 and its involvement in chromatin movement during cell division. - Ann. Bot. 99: 845-856, 2007. Go to original source...
    20. Kumar, S., Chandra, G.R., Albaugh, G.P., Muthukrishnan, S.: Regulation of the expression of α-amylase gene by sodium butyrate. - Plant mol. Biol. 5: 269-279, 1985. Go to original source...
    21. Kyo, M., Hattori, S., Yamaji, N., Pechan, P., Fukui, H.: Cloning and characterization of cDNAs associated with the embryogenic dedifferentiation of tobacco immature pollen grains. - Plant Sci. 164: 1057-1066, 2003. Go to original source...
    22. Lidder, P., Gutiérrez, R.A., Salomé, P.A., McClung, C.R., Green, P.J.: Circadian control of messenger RNA stability. Association with a sequence-specific messenger RNA decay pathway. - Plant Physiol. 138: 2374-2385, 2005. Go to original source...
    23. Liu, H., Wu, Y., Cao, A., Mao, B., Zhao, B., Wang, J.: Genome-wide analysis of DNA methylation during ovule development of female-sterile rice fsv1. - G3: Genes Genomes Genet. 7: 3621-3635, 2017. Go to original source...
    24. López de Silanes, I., Gorospe, M., Taniguchi, H., Abdelmohsen, K., Srikantan, S., Alaminos, M., Berdasco, M., Urdinguio, R.G., Fraga, M.F., Jacinto, F.V., Esteller, M.: The RNA-binding protein HuR regulates DNA methylation through stabilization of DNMT3b mRNA. - Nucl. Acids Res. 37: 2658-2671, 2009.
    25. Manoharlal, R., Saiprasad, G.V.S., Thambrahalli, A., Madhavakrishna, K.: Dissecting the transcriptional networks underlying the gibberellin response in Nicotiana tabacum. - Biol. Plant. 62: 647-662, 2018b. Go to original source...
    26. Manoharlal, R., Saiprasad, G.V.S., Ullagaddi, C., Kovařík, A.: Gibberellin A3 as an epigenetic determinant of global DNA hypo-methylation in tobacco. - Biol. Plant. 62: 11-23, 2018a. Go to original source...
    27. Meijón, M., Jesús Cañal, M., Valledor, L., Rodríguez, R., Feito, I.: Epigenetic and physiological effects of gibberellin inhibitors and chemical pruners on the floral transition of azalea. - Physiol. Plant. 141: 276-288, 2011. Go to original source...
    28. Meilan, L., Qiaomei, W., Zhujun, Z., Guangwen, Z.: Studies on the changes of DNA methylation level, GA content and protein in non-heading Chinese cabbage during vernalization. - Acta hort. sin. 29: 353-357, 2002.
    29. Narsai, R., Gouil, Q., Secco, D., Srivastava, A., Karpievitch, Y.V., Liew, L.C., Lister, R., Lewsey, M.G., Whelan, J.: Extensive transcriptomic and epigenomic remodelling occurs during Arabidopsis thaliana germination. - Genome Biol. 18: 172, 2017. Go to original source...
    30. Nolan, R.C., Ho, T.D.: Hormonal regulation of α-amylase expression in barley aleurone layers the effects of gibberellic acid removal and abscisic acid and phaseic acid treatments. - Plant Physiol. 88: 588-593, 1988. Go to original source...
    31. Park, S., Chung, P.J., Juntawong, P., Bailey-Serres, J., Kim, Y.S., Jung, H., Bang, S.W., Kim, Y., Do Choi, Y., Kim, J.: Posttranscriptional control of photosynthetic mRNA decay under stress conditions requires 3' and 5' untranslated regions and correlates with differential polysome association in rice. - Plant Physiol. 159: 1111-1124, 2012. Go to original source...
    32. Richards, D.E., King, K.E., Ait-Ali, T., Harberd, N.P.: How gibberellin regulates plant growth and development: a molecular genetic analysis of gibberellin signaling. - Annu. Rev. Plant Physiol. Plant mol. Biol. 52: 67-88, 2001. Go to original source...
    33. Shi, L., Olszewski, N.E.: Gibberellin and abscisic acid regulate GAST1 expression at the level of transcription. - Plant mol. Biol. 38: 1053-1060, 1998. Go to original source...
    34. Sun, T., Gubler, F.: Molecular mechanism of gibberellin signaling in plants. - Annu. Rev. Plant Biol. 55: 197-223, 2004. Go to original source...
    35. Thomas, S.G., Sun, T.P.: Update on gibberellin signaling. A tale of the tall and the short. - Plant Physiol. 135: 668-676, 2004. Go to original source...
    36. Turco, G.M., Kajala, K., Kunde-Ramamoorthy, G., Ngan, C., Olson, A., Deshphande, S., Tolkunov, D., Waring, B., Stelpflug, S., Klein, P.: DNA methylation and gene expression regulation associated with vascularization in Sorghum bicolor. - New Phytol. 214: 1213-1229, 2017. Go to original source...
    37. Vanyushin, B.F., Ashapkin, V.V.: DNA methylation in higher plants: past, present and future. - Biochim. biophys. Acta. 1809: 360-368, 2011.
    38. Vlasova, T.I., Demidenko, Z.N., Kirnos, M.D., Vanyushin, B.F.: In vitro DNA methylation by wheat nuclear cytosine DNA methyltransferase: effect of phytohormones. - Gene 157: 279-281, 1995. Go to original source...
    39. Wada, Y., Ohya, H., Yamaguchi, Y., Koizumi, N., Sano, H.: Preferential de novo methylation of cytosine residues in non-CpG sequences by a domains rearranged DNA methyltransferase from tobacco plants. - J. biol. Chem. 278: 42386-42393, 2003. Go to original source...
    40. Wolfraim, L.A., Langis, R., Tyson, H., Dhindsa, R.S.: cDNA sequence, expression, and transcript stability of a cold acclimation-specific gene, cas18, of alfalfa (Medicago falcata) cells. - Plant Physiol. 101: 1275-1282, 1993. Go to original source...
    41. Xu, J., Chua, N.: Arabidopsis decapping 5 is required for mRNA decapping, P-body formation, and translational repression during postembryonic development. - Plant Cell 21: 3270-3279, 2009. Go to original source...
    42. Yung, K.H., Mann, J.D.: Inhibition of early steps in the gibberellin-activated synthesis of α-amylase. - Plant Physiol. 42: 195-200, 1967. Go to original source...

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