Abstract
DNA methylation plays a vital role in tuning gene expression in response to environmental stimuli. Here, methylation-sensitive amplified polymorphisms (MSAP) were used to assess the effect of cold stress on the extent and patterns of DNA methylation in maize seedlings. Overall, cold-induced genome-wide DNA methylation polymorphisms accounted for 32.6 to 34.8% of the total bands at the different treatment time-points. It was demonstrated that the extent and pattern of DNA methylation was induced by cold stress through the cold treatment process and that the demethylation of fully methylated fragments was the main contributor of the DNA methylation alterations. The sequences of 28 differentially amplified fragments relevant to stress were successfully obtained. Under the cold stress, demethylation was detected in most fragments. BLAST results indicate that the homologues of these fragments are involved in many processes, including hormone regulation, cold response, photosynthesis, and transposon activation. The expression analysis demonstrated an increase in the transcription of five demethylated genes. Despite the fact that DNA methylation changes and cold acclimation are not directly associated, our results may indicate that the specific demethylation of genes is an active and rapid epigenetic response to cold in maize during the seedling stage, further elucidating the mechanism of maize adaptation to cold stress.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S (2004) Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plantarum 121:472–480
Ashikawa I (2001) Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars. Plant Mol Biol 45:31–39
Ausin I, Alonso-Blanco C, Jarillo JA, Ruiz-Garcia L, Martinez-Zapater JM (2004) Regulation of flowering time by FVE, a retinoblastoma-associated protein. Nat Genet 36:162–166
Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21
Cao DH, Gao X, Liu J, Kimatu JN, Geng SJ, Wang XP, Zhao J, Shi DC (2011) Methylation sensitive amplified polymorphism (MSAP) reveals that alkali stress triggers more DNA hypomethylation levels in cotton (Gossypium hirsutum L.) roots than salt stress. Afr J Biotechnol 10:18971–18980
Chen C, Marcus A, Li W, Hu Y, Calzada JP, Grossniklaus U, Cyr RJ, Ma H (2002) The Arabidopsis ATK1 gene is required for spindle morphogenesis in male meiosis. Development 129:2401–2409
Cheng C, Daigen M, Hirochika H (2006) Epigenetic regulation of the rice retrotransposon Tos17. Mol Gen Genet 276:378–390
Ciereszko I, Johansson H, Kleczkowski LA (2001) Sucrose and light regulation of a cold-inducible UDP-glucose pyrophosphorylase gene via a hexokinase-independent and abscisic acid-insensitive pathway in Arabidopsis. Biochem J 354:67–72
Dong ZY, Wang YM, Zhang ZJ, Shen Y, Lin XY, Ou XF, Han FP, Liu B (2006) Extent and pattern of DNA methylation alteration in rice lines derived from introgressive hybridization of rice and Zizania latifolia Griseb. Theor Appl Genet 113:196–205
Johnston JW, Benson EE, Harding K (2009) Cryopreservation induces temporal DNA methylation epigenetic changes and differential transcriptional activity in Ribes germplasm. Plant Physiol Bioch 47:123–131
Karan R, Deleon T, Biradar H, Subudhi PK (2012) Salt stress induced variation in DNA methylation pattern and its influence on gene expression in contrasting rice genotypes. Plos One 7:e40203
Kashkush K, Feldman M, Levy AA (2003) Transcriptional activation of retrotransposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106
Kimatu JN, Diarso M, Song CD, Agboola RS, Pang JS, Qi X, Liu B (2011) DNA cytosine methylation alterations associated with aluminium toxicity and low pH in Sorghum bicolor. Afr J Agr Res 6:4579–4593
Kou HP, Li Y, Song XX, Ou XF, Xing SC, Ma J, Von Wettstein D, Liu B (2011) Heritable alteration in DNA methylation induced by nitrogen-deficiency stress accompanies enhanced tolerance by progenies to the stress in rice (Oryza sativa L.). J Plant Physiol 168:1685–1693
Kovarik A, Koukalova B, Bezdek M, Opatrny Z (1997) Hypermethylation of tobacco heterochromatic loci in response to osmotic stress. Theor Appl Genet 95:301–306
Labra M, Ghiani A, Citterio S, Sgorbati S, Sala F, Vannini C, Ruffini-Castiglione M, Bracale M (2002) Analysis of cytosine methylation pattern in response to water deficit in pea root tips. Plant Biol 4:694–699
Li YD, Shan XH, Liu XM, Hu LJ, Guo WL, Liu B (2008) Utility of the methylation-sensitive amplified polymorphism (MSAP) marker for detection of DNA methylation polymorphism and epigenetic population structure in a wild barley species (Hordeum brevisubulatum). Ecol Res 23:927–930
Lu GY, Wu XM, Chen BY, Gao GZ, Xu K (2007) Evaluation of genetic and epigenetic modification in rapeseed (Brassica napus) induced by salt stress. J Integr Plant Biol 49:1599–1607
Lukens LN, Zhan SH (2007) The plant genome’s methylation status and response to stress: implications for plant improvement. Curr Opin Plant Biol 10:317–322
Piao HL, Xuan YH, Park SH, Je BI, Park SJ, Kim CM, Huang J, Wang GK, Kim MJ, Kang SM, Lee IJ, Kwon TR, Kim YH, Yeo US, Yi G, Son D, Han CD (2010) OsCIPK31, a CBL-interacting protein kinase is involved in germination and seedling growth under abiotic stress conditions in rice plants. Mol Cells 30:19–27
Rabinowicz PD, Palmer LE, May BP, Hemann MT, Lowe SW, McCombie WR, Martienssen RA (2003) Genes and transposons are differentially methylated in plants, but not in mammals. Genome Res 13:2658–2664
Reinders J, Wulff BB, Mirouze M, Mari-Ordonez A, Dapp M, Rozhon W, Bucher E, Theiler G, Paszkowski J (2009) Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev 23:939–950
Richard L, Qin LX, Gadal P, Goldberg R (1994) Molecular cloning and characterisation of a putative pectin methylesterase cDNA in Arabidopsis thaliana (L.). Febs Lett 355:135–139
Singh AK, Kumar R, Pareek A, Sopory SK, Singla-Pareek SL (2012) Overexpression of rice CBS domain containing protein improves salinity, oxidative, and heavy metal tolerance in transgenic tobacco. Mol Biotechnol 52:205–216
Steward N, Ito M, Yamaguchi Y, Koizumi N, Sano H (2002) Periodic DNA methylation in maize nucleosomes and demethylation by environmental stress. J Biol Chem 277:37741–37746
Tan MP (2010) Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive amplified polymorphism. Plant Physiol Bioch 48:21–26
Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J 58:778–790
Wang WS, Pan YJ, Zhao XQ, Dwivedi D, Zhu LH, Ali J, Fu BY, Li ZK (2011a) Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot 62:1951–1960
Wang WS, Zhao XQ, Pan YJ, Zhu LH, Fu BY, Li ZK (2011b) DNA methylation changes detected by methylation-sensitive amplified polymorphism in two contrasting rice genotypes under salt stress. J Genet Genomics 38:419–424
Xiong LZ, Xu CG, Maroof MAS, Zhang QF (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet 261:439–446
Yan H, Kikuchi S, Neumann P, Zhang W, Wu Y, Chen F, Jiang J (2010) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J 63:353–365
Zhao XX, Jia EJ, Yang WG, Dong YS, Liu B (2006) DNA methylation polymorphism in a set of elite maize inbred lines revealed by methylation-sensitive ISSR analysis. Cereal Res Commun 34:879–886
Zhao YL, Yu SX, Ye WW, Wang HM, Wang JJ, Fang BX (2010) Study on DNA cytosine methylation of cotton (Gossypium hirsutum L.) genome and its implication for salt tolerance. Agr Sci China 9:783–791
Zhong L, Xu YH, Wang JB (2009) DNA-methylation changes induced by salt stress in wheat Triticum aestivum. Afr J Biotechnol 8:6201–6207
Zhu JH, Dong CH, Zhu JK (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors contributed equally to this work.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Shan, X., Wang, X., Yang, G. et al. Analysis of the DNA methylation of maize (Zea mays L.) in response to cold stress based on methylation-sensitive amplified polymorphisms. J. Plant Biol. 56, 32–38 (2013). https://doi.org/10.1007/s12374-012-0251-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-012-0251-3