Abstract
Gracilariopsis lemaneiformis is an economically important agarophyte, which contains high quality gel and shows a high growth rate. Wild population of G. lemaneiformis displayed resident divergence, though with a low genetic diversity as was revealed by amplified fragment length polymorphism (AFLP) and simple sequence repeat (SSR) analyses. In addition, different strains of G. lemaneiformis are diverse in morphology. The highly inconsistence between genetic background and physiological characteristics recommends strongly to the regulation at epigenetic level. In this study, the DNA methylation change in G. lemaneiformis among different generation branches and under different temperature stresses was assessed using methylation sensitive amplified polymorphism (MSAP) technique. It was shown that DNA methylation level among different generation branches was diverse. The full and total methylated DNA level was the lowest in the second generation branch and the highest in the third generation. The total methylation level was 61.11%, 60.88% and 64.12% at 15°C, 22°C and 26°C, respectively. Compared with the control group (22°C), the fully methylated and totally methylated ratios were increased in both experiment groups (15°C and 26°C). All of the cytosine methylation/demethylation transform (CMDT) was further analyzed. High temperature treatment could induce more CMDT than low temperature treatment did.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Aina, R., Sgorbati, S., Santagostino, A., Labra, M., Ghiani, A., and Citterio, S., 2004. Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiologia Plantarum, 121 (3): 472–480.
Angers, B., Castonguay, E., and Massicotte, R., 2010. Environmentally induced phenotypes and DNA methylation: How to deal with unpredictable conditions until the next generation and after. Molecular Ecology, 19 (7): 1283–1295.
Bassam, B. J., Caetanoanollés, G., and Gresshoff, P. M., 1991. Fast and sensitive silver staining of DNA in polyacrylamide gels. Analytical Biochemistry, 196 (1): 80–83.
Baurens, F. C., Bonnot, F., Bienvenu, D., Causse, S., and Legavre, T., 2012. Using SD-AFLP and MSAP to assess CCGG methylation in the banana genome. Plant Molecular Biology Reporter, 21 (4): 339–348.
Bender, J., 1998. Cytosine methylation of repeated sequences in eukaryotes: The role of DNA pairing. Trends in Biochemical Sciences, 23 (7): 252–256.
Boyko, A., and Kovalchuk, I., 2011. Genetic and epigenetic effects of plant-pathogen interactions: An evolutionary perspective. Molecular Plant, 4 (6): 1014–1023.
Chakrabarty, D., Yu, K. W., and Paek, K. Y., 2003. Detection of DNA methylation changes during somatic embryogenesis of Siberian ginseng (Eleuterococcus senticosus). Plant Science, 165 (1): 61–68.
Chen, X., Ma, Y., Chen, F., Song, W., and Zhang, L., 2009. Analysis of DNA methylation patterns of PLBs derived from Cymbidium hybridium based on MSAP. Plant Cell, Tissue and Organ Culture (PCTOC), 98 (1): 67–77.
Choi, C., S., and Sano, H., 2007. Abiotic-stress induces demethylation and transcriptional activation of a gene encoding a glycerophosphodiesterase-like protein in tobacco plants. Molecular Genetics and Genomics, 277 (5): 589–600.
Dhar, M. S., Pethe, V. V., Gupta, V. S., and Ranjekar, P. K., 1990. Predominance and tissue specificity of adenine methylation in rice. Theoretical and Applied Genetics, 80 (3): 402–408.
Ding, H. Y., Sui, Z. H., Zhong, J., Zhou, W., and Wang, Z. X., 2012. Analysis and comparison on genetic diversity of haploid and diploid Gracilaria lemaneiformis polulations from different places of Qingdao by AFLP. Periodical of Ocean University of China, 42: 99–105.
Dyachenko, O. V., Zakharchenko, N. S., Shevchuk, T. V., Bohnert, H. J., Cushman, J. C., and Buryanov, Y. I., 2006. Effect of hypermethylation of CCWGG sequences in DNA of Mesembryanthemum crystallinum plants on their adaptation to salt stress. Biochemistry, 71 (4): 461–465.
Fieldes, M. A., Schaeffer, S. M., Krech, M. J., and Brown, J. C. L., 2005. DNA hypomethylation in 5-azacytidine-induced early-flowering lines of flax. Theoretical and Applied Genetics, 111 (1): 136–149.
Finnegan, E. J., Lawrence, G. J., Dennis, E. S., and Ellis, J. G., 1993. Behaviour of modified Ac elements in flax callus and regenerated plants. Plant Molecular Biology, 22 (4): 625–633.
González-Leija, J. A., Hernández-Garibay, E., Pacheco-Ruíz, I., Guardado-Puentes, J., Espinoza-Avalos, J., López-Vivas, J. M., and Bautista-Alcantar, J., 2009. Optimization of the yield and quality of agar from Gracilariopsis lemaneiformis (Gracilariales) from the Gulf of California using an alkaline treatment. Journal of Applied Phycology, 21 (3): 321–326.
Iqbal, K., Jin, S. G., Pfeifer, G. P., and Szabó, P. E., 2011. Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proceedings of the National Academy of Sciences, 108 (9): 3642–3647.
Iwase, Y., Shiraya, T., and Takeno, K., 2010. Flowering and dwarfism induced by DNA demethylation in Pharbitis nil. Physiologia Plantarum, 139 (1): 118–127.
Kay, A., 2001. Detection of DNA methylation changes in micropropagated banana plants using methylation-sensitive amplification polymorphism (MSAP). Plant Science, 161 (2): 359–367.
Kimatu, J. N., Diarso, M., Song, C., Agboola, R. S., Pang, J., Xin, Q., and Bao, L., 2011. DNA cytosine methylation alterations associated with aluminium toxicity and low pH in Sorghum bicolor. African Journal of Agricultural Research, 6 (19): 4579–4593.
Lukens, L. N., and Zhan, S., 2007. The plant genome’s methylation status and response to stress: Implications for plant improvement. Current Opinion in Plant Biology, 10 (3): 317–322.
Lund, G., Messing, J., and Viotti, A., 1995. Endosperm-specific demethylation and activation of specific alleles of a-tubulin genes of Zea mays L. Molecular Genetics and Genomics, 246 (6): 716–722.
Ma, K., Zhang, Z., Wang, S., Song, Y., and Zhang, D., 2012. Optimization of MSAP system and preliminary analysis of DNA methylation in Populus tomentosa. Journal of Northeast Forestry University, 40 (12): 1–7.
Mazumder, S., Ghosal, P. K., Pujol, C. A., Carlucci, M. A. J., Damonte, E. B., and Ray, B., 2003. Isolation, chemical investigation and antiviral activity of polysaccharides from Gracilaria corticata (Gracilariaceae, Rhodophyta). International Journal of Biological Macromolecules, 31 (1): 87–95.
Mcclelland, M., Nelson, M., and Raschke, E., 1994. Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Research, 21 (13): 3139–3154.
Melo, M. R. S., Feitosa, J. P. A., Freitas, A. L. P., and Paula, R. C. M. D., 2002. Isolation and characterization of soluble sulfated polysaccharide from the red seaweed Gracilaria cornea. Carbohydrate Polymers, 49 (4): 491–498.
Meng, F. R., Li, Y., Yin, J., Liu, H., Chen, X., Ni, Z. F., and Sun, Q. X., 2012. Analysis of DNA methylation during the germination of wheat seeds. Biologia Plantarum, 56 (2): 269–275.
Messeguer, R., Ganal, M. W., Steffens, J. C., and Tanksley, S. D., 1991. Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Molecular Biology, 16 (5): 753–770.
Pang, Q., Sui, Z., Kang, K. H., Kong, F., and Zhang, X., 2010. Application of SSR and AFLP to the analysis of genetic diversity in Gracilariopsis lemaneiformis (Rhodophyta). Journal of Applied Phycology, 22 (5): 607–612.
Pflugmacher., and Steinberg., 1997. Activity of Phase I and Phase II detoxication enzymes in aquatic macrophytes. Journal of Applied Botany Angewandte Botanik, 71 (5-6): 144-146.
Portis, E., Acquadro, A., Comino, C., and Lanteri, S., 2004. Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP). Plant Science, 166 (1): 169–178.
Qu, J, Q., Wang, X., Liu, C., Li, X. L., Zhang, X. L., and Liu, T., 2013. Preliminary analysis of DNA methylation of Saccharina japonica with MSAP. Periodical of Ocean University of China, 43 (10): 54–59.
Ren, X. Y., Zhang, X. C., and Sui, Z. H., 2006. Identification of phase relative genes in tetrasporophytes and female gametophytes of Gracilaria/Gracilariopsis lemaneiformis (Gracilariales, Rhodophyta). Electronic Journal of Biotechnology, 9 (2): 127–132.
Reynalópez, G. E., Simpson, J., and Ruizherrera, J., 1997. Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Molecular Genetics and Genomics, 253 (6): 703–710.
Ronemus, M. J., Galbiati, M., Ticknor, C., Chen, J., and Dellaporta, S. L., 1996. Demethylation-induced developmental pleiotropy in Arabidopsis. Science, 273 (5275): 654–657.
Santelices, B., and Doty, M. S., 1989. A review of Gracilaria farming. Aquaculture, 78 (2): 95–133.
Shan, X., Wang, X., Yang, G., Wu, Y., Su, S., Li, S., Liu, H., and Yuan, Y., 2013. Analysis of the DNA methylation of maize (Zea mays L.) in response to cold stress based on methylationsensitive amplified polymorphisms. Journal of Plant Biology, 56 (1): 32–38.
Sui, Z., 2005. Study of the benthic marine algae on the Liaoning Huanghai and Bohai sea coasts. Transaction of Oceanology & Limnology, 2005 (3): 57–65.
Tanaka, H., Masuta, C., Uehara, K., Kataoka, J., Koiwai, A., and Noma, M., 1997. Morphological changes and hypomethylation of DNA in transgenic tobacco expressing antisense RNA of the S-adenosyl-l-homocysteine hydrolase gene. Plant Molecular Biology, 35 (6): 981–986.
Vyskot, B., Koukalová, B., Kovarík, A., Sachambula, L., Reynolds, D., and Bezdek, M., 1995. Meiotic transmission of a hypomethylated repetitive DNA family in tobacco. Theoretical and Applied Genetics, 91 (4): 659–664.
Wang, J., Sui, Z., Hu, Y., Zhou, W., Wei, H., Du, Q., Niaz, Z., Peng, C., Mi, P., and Que, Z., 2016. Assessment of photosynthetic performance, carboxylase activities, and ATP content during tetrasporic development in Gracilariopsis lemaneiformis (Gracilariaceae, Rhodophyta). Journal of Applied Phycology, 28 (5): 1–14.
Wang, W. S., Pan, Y. J., Zhao, X. Q., Dwivedi, D., Zhu, L. H., Ali, J., Fu, B. Y., and Li, Z. K., 2011. Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). Journal of Experimental Botany, 62 (6): 1951–1960.
Wang, Z., Sui, Z., Hu, Y. Y., Zhang, S., Pan, Y., and Ju, H. R., 2014. A comparison of different Gracilariopsis lemaneiformis (Rhodophyta) parts in biochemical characteristics, protoplast formation and regeneration. Journal of Ocean University of China, 13 (4): 671–676.
Wang, Z., Wang, G., Niu, J., Wang, W., and Peng, G., 2010. Optimization of conditions for tetraspore release and assessment of photosynthetic activities for different generation branches of Gracilaria lemaneiformis Bory. Chinese Journal of Oceanology and Limnology, 28 (4): 738–748.
Xiong, L. Z., Xu, C. G., Maroof, M. A. S., and Zhang, Q., 1999. Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Molecular Genetics and Genomics, 261 (3): 439–446.
Xu, M. L., Li, X. Q., and Korban, S. S., 2000. AFLP-based detection of DNA methylation. Plant Molecular Biology Reporter, 18 (4): 361–368.
Ye, N., Wang, H., and Wang, G., 2006. Formation and early development of tetraspores of Gracilaria lemaneiformis (Gracilaria, Gracilariaceae) under laboratory conditions. Aquaculture, 254 (1): 219–226.
Yu, Y., Yang, X., Wang, H., Shi, F., Liu, Y., Liu, J., Liu, L., Wang, D., and Liu, B., 2013. Cytosine methylation alteration in natural populations of Leymus chinensis induced by multiple abiotic stresses. PLoS One, 8 (2): e55772.
Zhang, M., Kimatu, J, N., Xu, K., and Bao, L., 2010. DNA cytosine methylation in plant development. Journal of Genetics and Genomics, 37 (1): 1–12.
Zhang, X., and Fei, X., 2008. The varieties registered by Chinese Aquaculture Varieties Approving Committeee □ the cultivar 981 of Gp. lemaneiformis and its cultivation techniques. lemaneiformis and its cultivation techniques. Scientific Fish Farming, 6: 21–22.
Zhang, X., Qin, S., Ma, J., and Xu, P., 2004. The Genetics of Marine Algae. Agricultural Press of China, Beijing, 335pp.
Zhou, J., Gregurick, S. K., Krueger, S., and Schwarz, F. P., 2006. Conformational changes in Single-Strand DNA as a function of temperature by SANS. Biophysical Journal, 90 (2): 544–551.
Zhou, W., Hu, Y., Sui, Z., Fu, F., and Wang, J., Chang, L., Guo, W., and Li, B., 2013. Genome survey sequencing and genetic background characterization of Gracilariopsis lemaneiformis (Rhodophyta) based on Next-Generation sequencing. PLoS One, 8 (7): 374–374.
Zou, D., Xia, J., and Yang, Y., 2004. Photosynthetic use of exogenous inorganic carbon in the agarophyte Gracilaria lemaneiformis (Rhodophyta). Aquaculture, 237 (1): 421–431.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (No. 31372529), the Fundamental Research Funds for the Central Universities (No. 201762016) and China Agriculture Research System (No. CARS-50).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Peng, C., Sui, Z., Zhou, W. et al. Analysis of DNA Methylation of Gracilariopsis lemaneiformis Under Temperature Stress Using the Methylation Sensitive Amplification Polymorphism (MSAP) Technique. J. Ocean Univ. China 17, 623–631 (2018). https://doi.org/10.1007/s11802-018-3426-9
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-018-3426-9