Biologia plantarum 62:647-662, 2018 | DOI: 10.1007/s10535-018-0809-0

Dissecting the transcriptional networks underlying the gibberellin response in Nicotiana tabacum

R. Manoharlal1,*, G. V. S. Saiprasad1, A. Thambrahalli1, K. Madhavakrishna1
1 ITC Life Science and Technology Centre, Peenya Industrial Area, Bengaluru, Karnataka, India

The present work examines global transcriptional and limited metabolic profiling to dissect the signalling pathways associated with gibberellin A3 (GA3) induced alterations in tobacco (Nicotiana tabacum L.) under field conditions. Our microarray analysis revealed that GA3 foliar application elicited 7 032 differentially expressed genes (DEGs) with 3 507 and 3 525 genes displaying up- and down-regulation, respectively. These DEGs broadly belong to diverse metabolic pathways: GA signalling and homeostasis, ethylene and auxin biosyntheses, saccharide metabolism, glycolysistricarboxylic acid cycle, terpenoid biosynthesis, shikimate-phenylpropanoid pathway, S-adenosyl methionine cycle, fatty acid biosynthesis, cell wall metabolism, oxidative stress, DNA repair, and stress responses. Transcription validation of representative DEGs was confirmed by real-time quantitative PCR. A relative enhancement in cellular acetyl-CoA pool corroborated with a concomitant increase and decrease in transcriptions as well as activities of histone acetyltransferases and histone deacetylases, respectively. Phytochemical analysis shows an enhanced content of total sugars, reducing sugars, total flavonoids, and phenolics with a concomitant decrease of the content of starch, chlorophylls a and b, and carotenoids. Gas chromatography with mass spectrometry analysis revealed the presence of 30 differential metabolites, mostly belonging to terpenoid biosynthesis pathway.

Keywords: differentially expressed genes; GC-MS; HPLC; microarray; Nicotiana tabacum
Subjects: transcriptional regulation; gibberelins; gene expression; microarray; saccharides; chlorophyll; carotenoids; phenolics; tobacco
Species: Nicotiana tabacum

Received: August 8, 2017; Revised: February 4, 2018; Accepted: February 12, 2018; Published: August 1, 2018Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Manoharlal, R., Saiprasad, G.V.S., Thambrahalli, A., & Madhavakrishna, K. (2018). Dissecting the transcriptional networks underlying the gibberellin response in Nicotiana tabacum. Biologia plantarum, 62(4), 647-662. doi: 10.1007/s10535-018-0809-0.
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

    Supplementary files

    Download filebpl-201804-0005_S1.pdf

    File size: 1.45 MB

    References

    1. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Straeten, D., Peng, J., Harberd, N.P.: Integration of plant responses to environmentally activated phytohormonal signals. - Science 311: 91-94, 2006. Go to original source...
    2. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., Genschik, P.: The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. - Plant Cell 20: 2117-2129, 2008a. Go to original source...
    3. Achard, P., Renou, J., Berthomé, R., Harberd, N.P., Genschik, P.: Plant DELLAs restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. - Curr. Biol. 18: 656-660, 2008b. Go to original source...
    4. Agius, F., Kapoor, A., Zhu, J.K.: Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. - Proc. nat. Acad. Sci. USA 103: 11796-11801, 2006. Go to original source...
    5. Baenas, N., García-Viguera, C., Moreno, D.A.: Elicitation: a tool for enriching the bioactive composition of foods. - Molecules 19: 13541-13563. 2014. Go to original source...
    6. Bailey-Serres, J., Mittler, R.: The roles of reactive oxygen species in plant cells. - Plant Physiol. 141: 311-311, 2006. Go to original source...
    7. Banerjee, A., Wu, Y., Banerjee, R., Li, Y., Yan, H., Sharkey, T.D.: Feedback inhibition of deoxy-D-xylulose-5-phosphate synthase regulates the methylerythritol 4-phosphate pathway. - J. biol. Chem. 288: 16926-16936. 2013. Go to original source...
    8. Colebrook, E.H., Thomas, S.G., Phillips, A.L., Hedden, P.: The role of gibberellin signalling in plant responses to abiotic stress. - J. exp. Biol. 217: 67-75. 2014. Go to original source...
    9. Corbineau, F., Xia, Q., Bailly, C., El-Maarouf-Bouteau, H.: Ethylene, a key factor in the regulation of seed dormancy. - Front. Plant. Sci. 5: ??-??, 2014.
    10. Cordoba, E., Salmi, M., León, P.: Unravelling the regulatory mechanisms that modulate the MEP pathway in higher plants. - J. exp. Bot. 60: 2933-2943, 2009. Go to original source...
    11. Dennis, D.T., Greyson, M.F.: Fructose 6-phosphate metabolism in plants. - Physiol. Plant. 69: 395-404, 1987. Go to original source...
    12. Disch, A., Hemmerlin, A., Rohmer, M.: Mevalonate-derived isopentenyl diphosphate is the biosynthetic precursor of ubiquinone prenyl side chain in tobacco BY-2 cells. - Biochem. J. 331: 615-621, 1998. Go to original source...
    13. Dubois, M., Skirycz, A., Claeys, H., Maleux, K., Dhondt, S., De Bodt, S., Bossche, R.V., De Milde, L., Yoshizumi, T., Matsui, M.: ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. - Plant Physiol. 162: 319-332, 2013. Go to original source...
    14. Dugardeyn, J., Van den Bussche, F., Van der Straeten, D.: To grow or not to grow: what can we learn on ethylenegibberellin cross-talk by in silico gene expression analysis?. - J. exp. Bot. 59: 1-16, 2008. Go to original source...
    15. Fatland, B.L., Nikolau, B.J., Wurtele, E.S.: Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. - Plant Cell 17: 182-203, 2005. Go to original source...
    16. Finnegan, E.J., Kovac, K.A.: Plant DNA methyltransferases. - Plant mol. Biol. 43: 189-201, 2000. Go to original source...
    17. Frigerio, M., Alabadi, D., Pérez-Gómez, J., García-Cárcel, L., Phillips, A.L., Hedden, P., Blázquez, M.A.: Transcriptional regulation of gibberellin metabolism genes by auxin signaling in Arabidopsis. - Plant Physiol. 142: 553-563, 2006. Go to original source...
    18. Fujita, M., Fujita, Y., Maruyama, K., Seki, M., Hiratsu, K., Ohme-Takagi, M., Tran, L.P., Yamaguchi-Shinozaki, K., Shinozaki, K.: A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. - Plant J. 39: 863-876, 2004. Go to original source...
    19. Fuks, F.: DNA methylation and histone modifications: teaming up to silence genes. - Curr. Opin. Genet. Dev. 15: 490-495, 2005. Go to original source...
    20. Galdieri, L., Vancura, A.: Acetyl-CoA carboxylase regulates global histone acetylation. - J. biol. Chem. 287: 23865-23876, 2012. Go to original source...
    21. Guevara-García, A., San Román, C., Arroyo, A., Cortés, M.E., De la Luz Gutiérrez-Nava, M., León, P.: Characterization of the Arabidopsis clb6 mutant illustrates the importance of posttranscriptional regulation of the methyl-D-erythritol 4- phosphate pathway. - Plant Cell 17: 628-643, 2005. Go to original source...
    22. Gupta, R., Chakrabarty, S.K.: Gibberellic acid in plant: still a mystery unresolved. - Plant Signal. Behav. 8: e25504. 2013. Go to original source...
    23. Hansen, J., Møller, I.: Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. - Anal. Biochem. 68: 87-94, 1975. Go to original source...
    24. 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...
    25. Hedden, P., Phillips, A.L.: Gibberellin metabolism: new insights revealed by the genes. - Trends Plant Sci. 5: 523-530, 2000. Go to original source...
    26. Herrmann, K.M.: The shikimate pathway: early steps in the biosynthesis of aromatic compounds. - Plant Cell 7: 907, 1995. Go to original source...
    27. Inaba, Y., Brotherton, J.E., Ulanov, A., Widholm, J.M.: Expression of a feedback insensitive anthranilate synthase gene from tobacco increases free tryptophan in soybean plants. - Plant Cell Rep. 26: 1763-1771, 2007. Go to original source...
    28. Kant, M., Jonckheere, W., Knegt, B., Lemos, F., Liu, J., Schimmel, B., Villarroel, C., Ataide, L., Dermauw, W., Glas, J.: Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. - Ann. Bot. 115: 1015-1051. 2015. Go to original source...
    29. Kasote, D.M., Katyare, S.S., Hegde, M.V., Bae, H.: Significance of antioxidant potential of plants and its relevance to therapeutic applications. - Int. J. biol. Sci. 11: 982-991. 2015. Go to original source...
    30. Kawaguchi, A., Bloch, K.: Inhibition of glucose 6-phosphate dehydrogenase by palmitoyl coenzyme A. - J. biol. Chem. 249: 5793-5800, 1974.
    31. Keyes, G., Sorrells, M.E., Setter, T.L.: Gibberellic acid regulates cell wall extensibility in wheat (Triticum aestivum L.). - Plant Physiol. 92: 242-245, 1990. Go to original source...
    32. Kim, D., Jeong, S.W., Lee, C.Y.: Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. - Food Chem. 81: 321-326, 2003. Go to original source...
    33. Kim, D.S., Hwang, B.K.: An important role of the pepper phenylalanine ammonia-lyase gene (PAL1) in salicylic aciddependent signalling of the defence response to microbial pathogens. - J. exp. Bot. 65: 2295-2306. 2014. Go to original source...
    34. Kolbe, A., Tiessen, A., Schluepmann, H., Paul, M., Ulrich, S., Geigenberger, P.: Trehalose 6-phosphate regulates starch synthesis via posttranslational redox activation of ADPglucose pyrophosphorylase. - Proc. nat. Acad. Sci. USA 102: 11118-11123, 2005. Go to original source...
    35. Lange, B.M., Rujan, T., Martin, W., Croteau, R.: Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. - Proc. nat. Acad. Sci. USA 97: 13172-13177, 2000. Go to original source...
    36. Lata, C., Prasad, M.: Role of DREBs in regulation of abiotic stress responses in plants. - J. exp. Bot. 62: 4731-4748. 2011. Go to original source...
    37. Laule, O., Fürholz, A., Chang, H., Zhu, T., Wang, X., Heifetz, P.B., Gruissem, W., Lange, M.: Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. - Proc. nat. Acad. Sci. USA 100: 6866-6871, 2003. Go to original source...
    38. Laware, S.L.: Sequential extraction of plant metabolites. - Int. J. Curr. Microbiol. appl. Sci. 4: 33-38, 2015.
    39. Li, Z., Niu, S., Yuan, H., Li, W.: Gibberellins affect tobacco growth and development in a dose dependent manner through genes involved in metabolic processes. - Plant mol. Biol. Rep. 33: 1259-1269. 2015. Go to original source...
    40. Lichtenthaler, H.K., Wellburn, A.R.: Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. - Biochem. Soc. Trans. 11: 591-592, 1983. Go to original source...
    41. Lindroth, A.M., Cao, X., Jackson, J.P., Zilberman, D., McCallum, C.M., Henikoff, S., Jacobsen, S.E.: Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. - Science 292: 2077-2080, 2001. Go to original source...
    42. Mabiki, F.P., Magadula, J.J., Mdegela, R.H., Mosha, R.D.: Optimization of extraction conditions and phytochemical screening of root extract of Synadenium glaucescens Pax. - Int. J. Chem. 5: 103, 2013. Go to original source...
    43. Magome, H., Yamaguchi, S., Hanada, A., Kamiya, Y., Oda, K.: The DDF1 transcriptional activator upregulates expression of a gibberellin-activating gene, GA2ox7, under highsalinity stress in Arabidopsis. - Plant J. 56: 613-626, 2008. Go to original source...
    44. Manoharlal, R., Saiprasad, G.V.S., Ullagaddi, C., Kovařík, A.: Gibberellin A3 (GA3) as an epigenetic determinant of global DNA hypo-methylation in tobacco. - Biol. Plant. 62: 11-23, 2018. Go to original source...
    45. Manova, V., Gruszka, D.: DNA damage and repair in plantsfrom models to crops. - Front. Plant. Sci. 6: 1-26, 2015. Go to original source...
    46. Mansouri, H., Asrar, Z., Amarowicz, R.: The response of terpenoids to exogenous gibberellic acid in Cannabis sativa L. at vegetative stage. - Acta Physiol. Plant. 33: 1085-1091. 2011. Go to original source...
    47. Miller, G., Shulaev, V., Mittler, R.: Reactive oxygen signaling and abiotic stress. - Physiol. Plant. 133: 481-489, 2008. Go to original source...
    48. Miller, G.L.: Use of dinitrosalicylic acid reagent for determination of reducing sugar. - Anal. Chem. 31: 426-428, 1959. Go to original source...
    49. Mustroph, A., Sonnewald, U., Biemelt, S.: Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana. -FEBS Lett. 581: 2401-2410, 2007. Go to original source...
    50. Nemhauser, J.L., Hong, F., Chory, J.: Different plant hormones regulate similar processes through largely non overlapping transcriptional responses. - Cell 126: 467-475, 2006. Go to original source...
    51. Nishiuchi, S., Yamauchi, T., Takahashi, H., Kotula, L., Nakazono, M.: Mechanisms for coping with submergence and waterlogging in rice. - Rice 5: 2, 2012. Go to original source...
    52. O'Neill, D.P., Ross, J.J.: Auxin regulation of the gibberellin pathway in pea. - Plant Physiol. 130: 1974-1982, 2002.
    53. Phukan, U.J., Jeena, G.S., Shukla, R.K.: WRKY transcription factors: molecular regulation and stress responses in plants. - Front. Plant. Sci. 7: 760, 2016. Go to original source...
    54. Poirier, Y., Antonenkov, V.D., Glumoff, T., Hiltunen, J.K.: Peroxisomal β-oxidation-A metabolic pathway with multiple functions. - Biochim. biophys Acta 1763: 1413-1426, 2006. Go to original source...
    55. Richard, O., Paquet, N., Haudecoeur, E., Charrier, B.: Organization and expression of the GSK3/Shaggy kinase gene family in the moss Physcomitrella patens suggest early gene multiplication in land plants and an ancestral response to osmotic stress. - J. mol. Evol. 61: 99-113, 2005. Go to original source...
    56. 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...
    57. Rodwell, V.W., Beach, M.J., Bischoff, K.M., Bochar, D.A., Darnay, B.G., Friesen, J.A., Gill, J.F., Hedl, M., Jordan- Starck, T., Kennelly, P.J.: 3-Hydroxy-3-methylglutaryl-CoA reductase. - Meth. Enzymol. 324: 259, 2000. Go to original source...
    58. Rohmer, M.: The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. - Nat. Prod. Rep. 16: 565-574, 1999. Go to original source...
    59. Ross, J.J., O'Neill, D.P., Smith, J.J., Kerckhoffs, L.H.J., Elliott, R.C.: Evidence that auxin promotes gibberellin A1 biosynthesis in pea. - Plant J. 21: 547-552, 2000. Go to original source...
    60. Sauter, M., Moffatt, B., Saechao, M.C., Hell, R., Wirtz, M.: Methionine salvage and S-adenosylmethionine: essential links between sulfur, ethylene and polyamine biosynthesis. - Biochem. J. 451: 145-154, 2013. Go to original source...
    61. Silva, L., Pezzini, B.R., Soares, L.: Spectrophotometric determination of the total flavonoid content in Ocimum basilicum L. (Lamiaceae) leaves. - Pharmacogn. Mag. 11: 96,2015.
    62. Speranzini, V., Pilotto, S., Sixma, T.K., Mattevi, A.: Touch, act and go: landing and operating on nucleosomes. - EMBO J. 35: 376-388, 2016. Go to original source...
    63. Sun, T.P., Gubler, F.: Molecular mechanism of gibberellin signaling in plants. - Annu. Rev. Plant Biol. 55: 197-223, 2004. Go to original source...
    64. Tamang, B.G., Fukao, T.: Plant adaptation to multiple stresses during submergence and following desubmergence. - Int. J. mol. Sci. 16: 30164-30180,F 2015. Go to original source...
    65. 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...
    66. Tumaney, A.W., Ohlrogge, J.B., Pollard, M.: Acetyl coenzyme A concentration in plant tissues. - J. Plant Physiol. 161: 485-488, 2004. Go to original source...
    67. Verma, V., Ravindran, P., Kumar, P.P.: Plant hormonemediated regulation of stress responses. - BMC Plant Biol. 16: 1, 2016. Go to original source...
    68. Wang, G., Que, F., Xu, Z., Wang, F., Xiong, A.: Exogenous gibberellin altered morphology, anatomic and transcriptional regulatory networks of hormones in carrot root and shoot. - BMC Plant Biol. 15: 1, 2015. Go to original source...
    69. Wolbang, C.M., Ross, J.J.: Auxin promotes gibberellin biosynthesis in decapitated tobacco plants. - Planta 214: 153-157, 2001. Go to original source...
    70. Zhang, J., Jia, W., Yang, J., Ismail, A.M.: Role of ABA in integrating plant responses to drought and salt stresses. - Field Crops Res. 97: 111-119, 2006. Go to original source...
    71. Zhao, Y.: The roles of YUCCA genes in local auxin biosynthesis and plant development. - In: Pua, E., Davey, M. (ed.: Plant Developmental Biology - Biotechnological Perspectives. Vol. 2. Pp. 227-235. Springer, Berlin - Heidelberg 2010. Go to original source...

    Return to the content