Abstract
To investigate the molecular response of ancient plants to heavy metal stress and to explore the feature of DNA methylation in endangered plants after exposure to heavy metals, the Isoetes sinensis, an endangered plant, was stressed with three different concentrations of two heavy metals lead (Pb) and cadmium (Cd), respectively. Then the degrees and the patterns of DNA methylation in the leaves were measured on the 14th day using Methylation Sensitive Amplified Polymorphism (MSAP) technique. The results showed that the DNA methylated profile of I. sinensis was affected by Pb and Cd stress. There was no significant difference in the amount of DNA methylation among control check (CK), Pb stress group, and Cd stress group (CK 46.96%, Pb 48.23%, and Cd 48.1%). However, full-methylation level of Pb stress group (28.34%) and Cd stress group (20.25%) was lower than control (33.91%), in contrast, hemi-methylation level Pb stress group (19.89%) and Cd stress group (27.85%) were higher than control (13.04%). The change of patterns from no methylation or hemi-methylation of internal and external cytosines into full-methylation of internal and external cytosines accounted for a large proportion in enhanced methylation aspects. The full-methylation into no methylation or hemi- or full-methylation of internal and external cytosines occupied most of demethylation. The proportion of DNA methylation (including hypermethylation) by both Pb and Cd stresses is nearly equal (39.04% and 39.71%), but the proportion of DNA demethylation by Cd is higher than that by Pb (46.86% than 33.92%).
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ashikawa I (2001) Surveying CpG methylation at 5'-CCGG in the genomes of rice cultivars. Plant Mol Biol 45:31–39. https://doi.org/10.1023/A:1006457321781
Bender J (1998) Cytosine methylation of repeated sequences in eukaryotes: the role of DNA pairing. Trends Biochem Sci 23:252–256. https://doi.org/10.1016/S0968-0004(98)01225-0
Chen Y-Y, Kong D-R, Huang C-H, Xu Y-X, Li Z-Z (2012) Microsatellite analysis reveals the genetic structure and gene flow of the aquatic quillwort Isoetes sinensis, a critically endangered species in China. Aquat Bot 96:52–57. https://doi.org/10.1016/j.aquabot.2011.09.001
Cicatelli A, Todeschini V, Lingua G, Biondi S, Torrigiani P, Castiglione S (2014) Epigenetic control of heavy metal stress response in mycorrhizal versus non-mycorrhizal poplar plants. Environ Sci Pollut Res 21:1723–1737. https://doi.org/10.1007/s11356-013-2072-4
Ding H, Gao J, Qin C, Ma H, Huang H, Song P, Luo X, Lin H, Shen Y, Pan G, Zhang Z (2014) The dynamics of DNA methylation in maize roots under Pb stress. Int J Mol Sci 15:23537–23554. https://doi.org/10.3390/ijms151223537
Dowen RH, Ecker JR (2012) Widespread dynamic DNA methylation in response to biotic stress. Proc Natl Acad Sci U S A 109:2183–2191. https://doi.org/10.1073/pnas.1209329109
Duruibe JO, Ogwuegbu MOC, Egwurugwu JN (2007) Heavy metal pollution and human biotoxic effects. Int J Phys Sci 2:112–118
Erturk FA, Aydin M, Sigmaz B, Taspinar MS, Arslan E, Agar G, Yagci S (2015a) Effects of As2O3 on DNA methylation, genomic instability, and LTR retrotransposon polymorphism in Zea mays. Environ Sci Pollut Res 22:18601–18606. https://doi.org/10.1007/s11356-015-5426-2
Erturk FA, Agar G, Arslan E, Arslan E, Nardemir G (2015b) Analysis of genetic and epigenetic effects of maize seeds in response to heavy metal (Zn) stress. Environ Sci Pollut Res 22:10291–10297. https://doi.org/10.1007/s11356-014-3886-4
Fu L-K, Jin J-M (1992) China plant Red Data Book—rare and endangered plants. Science Press, Beijing, pp 538–539 (in Chinese)
Ge C-L, Yang X-Y, Liu X-N, Sun J-H, Luo S-S, Wang Z-G (2002) Effects of heavy metal on the DNA methylation level in rice and wheat. Acta Photophysiologica Sinica 28:363–368 (in Chinese)
Gouda EM, Essawy GS, Mahdy EM, Abdel-Mageed HH (2004) DNA fragmentation and DNA-protein cross-links as oxidative damage induced by heavy metals in rats. J Egypt Acad Soc Environ Develop (C-Molecular Biology) 5:59–75
He L-L, Shen H, Wang Y, Wang J-J, Gong Y-Q, Xu L, Liu L-W (2015) Analysis of genomic DNA methylation level in radish under lead stress. J Nucl Agr Sci 29:1278–1284 (in Chinese)
Hei S-M (2011) Effects of heavy metal chromium on the DNA methylation in wheat seedlings. J Anhui Agr Sci 13:7589–7591 (in Chinese). https://doi.org/10.1016/j.ecns.2012.07.070
Lanier C, Bernard F, Dumez S, Leclercq J, Lemière S, Vandenbulcke F, Nesslany F, Platel A, Devred I, Cuny D, Deram A (2016) Combined effect of Cd and Pb spiked field soils on bioaccumulation, DNA damage, and peroxidase activities in Trifolium repens. Environ Sci Pollut Res 23:1755–1767. https://doi.org/10.1007/s11356-015-5414-6
Li Z, Liu Z, Chen R, Li X, Tai P, Gong Z, Jia C, Liu W (2015) DNA damage and genetic methylation changes caused by Cd in Arabidopsis thaliana seedlings. Environ Toxicol Chem 34:2095–2103. https://doi.org/10.1002/etc.3033
Ou X-F, Zhang Y-H, Xu C-M, Lin X-Y, Zang Q, Zhuang T-T, Jiang L-L, von Wettstein D, Liu B (2012) Transgenerational inheritance of modified DNA methylation patterns and enhanced tolerance induced by heavy metal stress in rice (Oryza sativa L.). PLoS One 7:e41143. https://doi.org/10.1371/journal.pone.0041143
Rana SV (2008) Metals and apoptosis: recent developments. J Trace Elem Med Biol 22:262–284. https://doi.org/10.1016/j.jtemb.2008.08.002
Saxena I, Shekhawat GS (2013) Nitric oxide (NO) in alleviation of heavy metal induced phytotoxicity and its role in protein nitration. Nitric Oxide 32:13–20. https://doi.org/10.1016/j.niox.2013.03.004
Singh J, Kalamdhad AS (2011) Effects of heavy metals on soil, plants, human health and aquatic life. Int J Res Chem 1:15–21
Wang J-Y, Gituru WR, Wang Q-F (2006) Ecology and conservation of the endangered quillwort Isoetes sinensis in China. J Nat Hist 39:4069–4079. https://doi.org/10.1080/00222930500505052
Wang H-C, Li J-Q, He Z-C (2007) Irregular meiotic behavior in Isoetes sinensis (Isoetaceae), a rare and endangered fern in China. Caryologia 60:358–363. https://doi.org/10.1080/00087114.2007.10797959
Xiong L-Z, Xu C-G, Maroof MA, Zhang Q-F (1999) Patterns of cytosine methylation in an elicits hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet 26:439–446. https://doi.org/10.1007/s004380050986
Yaish MW (2013) DNA methylation-associated epigenetic changes in stress tolerance of plants. In: Rout GR, Das AB (eds) Molecular Stress Physiology of Plants. Springer, India, pp 427–440. https://doi.org/10.1007/978-81-322-0807-5_17
Yang J-L, Liu L-W, Gong Y-Q, Huang D-Q, Wang F, He L-L (2007) Analysis of genomic DNA methylation level in radish under cadmium stress by methylation sensitve ampolified polymorphism technique. J Plant Physiol Mol Biol 33:219–226 (in Chinese)
Ye Q-G, Li J-Q (2003) Distribution status and causation of endangerment of Isoetes sinesis Palmer in Zhejiang province. J Wuhan Bot Res 3:216–220 (in Chinese)
Zhang K-K, Chen X-Y, Yang P, Guan P (2016) Effects of different concentrations Cd stress on DNA methylation of Tagetes patula. Prata Sci 33(9):1673–1680 (in Chinese)
Zhao Y-L, Ye W-W, Wang J-J (2009) Review of DNA methylation and plant stress-tolerance. Acta Bot Boreali-Occidentalia Sinica 7:1479–1489 (in Chinese)
Funding
This research was supported by the National Science Foundation of China (31170294, 31770350) and the Open Projects of the Key Laboratory of Plant Biology (ZK201201).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Yi-ping Chen
Rights and permissions
About this article
Cite this article
Ding, GH., Guo, DD., Guan, Y. et al. Changes of DNA methylation of Isoetes sinensis under Pb and Cd stress. Environ Sci Pollut Res 26, 3428–3435 (2019). https://doi.org/10.1007/s11356-018-3864-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-018-3864-3