Abstract
Maize, a moderately salt sensitive crop, first experiences osmotic stress that cause reduction in plant growth under salt stress. Fluctuation in cell wall elongation is one of the reasons of this reduction. Along with others, two important proteins expansins and xyloglucan endotransglucosylase are involved in regulation of cell wall elasticity, but the role of epigenetic mechanisms in regulating the cell wall related genes is still elusive. The present study was conducted with the aim of understanding the role of DNA methylation in regulating ZmEXPB2 and ZmXET1 genes. One salt sensitive and one salt tolerant maize cultivar was grown under hydroponic conditions at different levels of salt stress: T1 = 1 mM (control), T2 = 100 mM and T3 = 200 mM in three replicates. DNA and RNA were extracted from roots. After bisulfite treatment, Methyl Sensitive PCR was used for the DNA methylation analysis. It was revealed that fragment in promoter of ZmEXPB2 gene showed high level of DNA methylation under T1 in both varieties. Comparison of different stress treatments revealed decrease in DNA methylation with the increase in salt stress, significantly lower methylation appearing in T3. Similarly, the fragment in promoter of ZmXET1 gene also showed high levels of DNA methylation in T1. When different treatments were analysed, this gene significantly hypomethylated at T2 which continued to decrease in T3 in sensitive variety but remain stable in tolerant variety. Although, further in-depth analysis is required, our results demonstrate region-specific and genotype-specific methylation shift in the promoter of the ZmEXPB2 and ZmXET1 genes when subjected to the salt stress confirming the epigenetic regulation of these genes under stress conditions.
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Baek, D., Jiang, J., Chung, J.-S., Wang, B., Chen, J., Xin, Z., Shi, H. 2011. Regulated AtHKT1 gene expression by a distal enhancer element and DNA methylation in the promoter plays an important role in salt tolerance. Plant Cell Physiol. 52:149–161.
Bjornson, M., Dandekar, A., Dehesh, K. 2016. Determinants of timing and amplitude in the plant general stress response. J. Integr. Plant Biol. 58:119–126.
Cedar, H., Bergman, Y. 2009. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 10:295–304.
Chinnusamy, V., Jagendorf, A., Zhu, J.-K. 2005. Understanding and improving salt tolerance in plants. Crop Sci. 45:437–448.
Cho, H.-T., Cosgrove, D.J. 2000. Altered expression of expansin modulates leaf growth and pedicel abscission in Arabidopsis thaliana. Proc. Natl. Acad. Sci. 97:9783–9788.
Choi, C.-S., Sano, H. 2007. Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Mol. Genet. Genomics. 277:589–600.
Choi, D., Lee, Y., Cho, H.-T., Kende, H. 2003. Regulation of expansin gene expression affects growth and development in transgenic rice plants. Plant Cell 15:1386–1398.
Cosgrove, D.J. 2000. Loosening of plant cell walls by expansins. Nature 407:321–326.
Cosgrove, D.J., Li, L.C., Cho, H.-T., Hoffmann-Benning, S., Moore, R.C., Blecker, D. 2002. The growing world of expansins. Plant Cell Physiol. 43:1436–1444.
de Azevedo Neto, A.D., Prisco, J.T., Enéas-Filho, J., Abreu, C.E.B. de, Gomes-Filho, E. 2006. Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ. Exp. Bot. 56:87–94.
El Sayed, H.E.S.A. 2011. Influence of salinity stress on growth parameters, photosynthetic activity and cytological studies of Zea mays, L. plant using hydrogel polymer. Agric. Biol. J. N. Am. 2:907–920.
Fei, Y., Xue, Y., Du, P., Yang, S., Deng, X. 2017. Expression analysis and promoter methylation under osmotic and salinity stress of TaGAPC1 in wheat (Triticum aestivum L). Protoplasma 254:987–996.
Fortmeier, R., Schubert, S. 1995. Salt tolerance of maize (Zea mays L.): the role of sodium exclusion. Plant Cell Environ. 18:1041–1047.
Galvan-Ampudia, C.S., Julkowska, M.M., Darwish, E., Gandullo, J., Korver, R.A., Brunoud, G., Haring, M.A., Munnik, T., Vernoux, T., Testerink, C. 2013. Halotropism is a response of plant roots to avoid a saline environment. Curr. Biol. 23:2044–2050.
Geilfus, C.-M., Ober, D., Eichacker, L.A., Mühling, K.H., Zörb, C. 2015. Down-regulation of ZmEXPB6 (Zea mays β-expansin 6) protein is correlated with salt-mediated growth reduction in the leaves of Z. mays L. J. Biol. Chem. 290:11235–11245.
Geilfus, C.-M., Zörb, C., Neuhaus, C., Hansen, T., Lüthen, H., Mühling, K.H. 2011. Differential transcript expression of wall-loosening candidates in leaves of maize cultivars differing in salt resistance. J. Plant Growth Regul. 30:387–395.
González, R.M., Ricardi, M.M., Iusem, N.D. 2013. Epigenetic marks in an adaptive water stress-responsive gene in tomato roots under normal and drought conditions. Epigenetics 8:864–872.
Khan, A.R., Enjalbert, J., Marsollier, A.-C., Rousselet, A., Goldringer, I., Vitte, C. 2013. Vernalization treatment induces site-specific DNA hypermethylation at the VERNALIZATION-A1 (VRN-A1) locus in hexaploid winter wheat. BMC Plant Biol. 13:209.
Kosová, K., Prášil, I.T., Vítámvás, P. 2013. Protein contribution to plant salinity response and tolerance acquisition. Int. J. Mol. Sci. 14:6757–6789.
Kumar, S., Beena, A.S., Awana, M., Singh, A. 2017. Salt-induced tissue-specific cytosine methylation down-regulates expression of HKT genes in contrasting wheat (Triticum aestivum L.) genotypes. DNA Cell Biol. 36:283–294.
Lee, D.-K., Ahn, J.H., Song, S.-K., Choi, Y.D., Lee, J.S. 2003. Expression of an expansin gene is correlated with root elongation in soybean. Plant Physiol. 131:985–997.
Li, H., Yan, S., Zhao, L., Tan, J., Zhang, Q., Gao, F., Wang, P., Hou, H., Li, L. 2014. Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol. 14:105.
Liu, T., Van Staden, J., Cress, W.A. 2000. Salinity induced nuclear and DNA degradation in meristematic cells of soybean (Glycine max L.) roots. Plant Growth Regul. 30:49–54.
Menezes-Benavente, L., Kernodle, S.P., Margis-Pinheiro, M., Scandalios, J.G. 2004. Salt-induced antioxidant metabolism defenses in maize (Zea mays L.) seedlings. Redox Rep. 9:29–36.
Paszkowski, J., Whitham, S.A. 2001. Gene silencing and DNA methylation processes. Curr. Opin. Plant Biol. 4:123–129.
Paul, A., Dasgupta, P., Roy, D., Chaudhuri, S. 2017. Comparative analysis of histone modifications and DNA methylation at OsBZ8 locus under salinity stress in IR64 and Nonabokra rice varieties. Plant Mol. Biol. 95:63–88
Pecinka, A., Dinh, H.Q., Baubec, T., Rosa, M., Lettner, N., Mittelsten Scheid, O. 2010. Epigenetic regulation of repetitive elements is attenuated by prolonged heat stress in Arabidopsis. Plant Cell. 22:3118–3129.
Pitann, B., Kranz, T., Mühling, K.H. 2009/a. The apoplastic pH and its significance in adaptation to salinity in maize (Zea mays L.): Comparison of fluorescence microscopy and pH-sensitive microelectrodes. Plant Sci. 176:497–504.
Pitann, B., Schubert, S., Mühling, K.H. 2009/b. Decline in leaf growth under salt stress is due to an inhibition of H+-pumping activity and increase in apoplastic pH of maize leaves. J. Plant Nutr. Soil Sci. 172:535–543.
Shahzad, M., Witzel, K., Zörb, C., Mühling, K.H. 2012. Growth-related changes in subcellular ion patterns in maize leaves (Zea mays L.) under salt stress. J. Agron. Crop Sci. 198:46–56.
Song, Y., Ji, D., Li, S., Wang, P., Li, Q., Xiang, F. 2012. The dynamic changes of DNA methylation and histone modifications of salt responsive transcription factor genes in soybean. PLOS One. 7:e41274.
SüMER, A., Zörb, C., Yan, F., Schubert, S. 2004. Evidence of sodium toxicity for the vegetative growth of maize (Zea mays L.) during the first phase of salt stress. J. Appl. Bot. 78:135–139.
Szalai, G., Janda, T. 2009. Effect of salt stress on the salicylic acid synthesis in young maize (Zea mays L.) plants. J. Agron. Crop Sci. 195:165–171.
Takeda, T., Fry, S.C. 2004. Control of xyloglucan endotransglucosylase activity by salts and anionic polymers. Planta 219:722–732.
Vincent, D., Ergül, A., Bohlman, M.C., Tattersall, E.A.R., Tillett, R.L., Wheatley, M.D., Woolsey, R., Quilici, D.R., Joets, J., Schlauch, K., Schooley, D.A., Cushman, J.C., Cramer, G.R. 2007. Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J. Exp. Bot. 58:1873–1892.
Wu, Y., Jeong, B.-R., Fry, S.C., Boyer, J.S. 2005. Change in XET activities, cell wall extensibility and hypocotyl elongation of soybean seedlings at low water potential. Planta 220:593–601.
Xu, R., Wang, Y., Zheng, H., Lu, W., Wu, C., Huang, J., Yan, K., Yang, G., Zheng, C. 2015. Salt-induced transcription factor MYB74 is regulated by the RNA-directed DNA methylation pathway in Arabidopsis. J. Exp. Bot. 66:5997–6008.
Zörb, C., Mühling, K.H., Kutschera, U., Geilfus, C.-M. 2015. Salinity stiffens the epidermal cell walls of saltstressed maize leaves: Is the epidermis growth-restricting? PLOS One. 10:e0118406.
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Communicated by M. Molnár-Láng
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Kaleem, F., Shahzad, M., Shabir, G. et al. Salt Stress Induces Genotype-specific DNA Hypomethylation in ZmEXPB2 and ZmXET1 Genes in Maize. CEREAL RESEARCH COMMUNICATIONS 47, 216–227 (2019). https://doi.org/10.1556/0806.46.2018.70
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DOI: https://doi.org/10.1556/0806.46.2018.70