Abstract
DNA methylation is the most important epigenetic regulatory strategy that is involved in various biological processes, including environmental stress response. In the present study, the potential contribution of DNA methylation-mediated gene regulation in a high-temperature-tolerant strain of Pyropia haitanensis (Z-61) was investigated by using the methylation-sensitive amplification polymorphism (MSAP) assay. With high temperature, the level of global DNA methylation (5-mC) in Z-61 decreased from 2.21% (control) to 1.36% (12 h) and 0.60% (144 h). MSAP analysis indicated that the total methylation ratio (%) decreased from 30.19% (control) to 15.82% (12 h) and 16.89% (144 h) and that the demethylation of fully methylated fragments was the main contributor of the DNA methylation alterations. A total of 55 polymorphic bands representing fragments that were generated during methylation/demethylation events in different samples were randomly selected and sequenced, of which 29 fragments were situated within a gene, whereas the others were located within noncoding regions or promoters. The 29 MSAP fragments consisted of 18 fragments that were highly expressed as indicated by RNA-seq analysis and 11 genes that exhibited either very low or no expression at all time points. BLASTN analysis indicated that the methylated fragments situated within genes are homologous to those involved in numerous processes, including abiotic stress response, programmed cell death, photosynthesis, energy metabolism, signal transduction, protein synthesis, and transposon activation. To the best of our knowledge, this is the first report on changes in methylation patterns in macroalgae under environmental stress, and our findings provide insights into the elucidation of the mechanism underlying stress adaptation in P. haitanensis.
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References
Abraham M, Jonathan G, Vera AF (2006) Repetitive proline-rich proteins in the extracellular matrix of the plant cell. Physiol Plant 81:273–279
Alina 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 Plant 121:472–480
Blouin NA, Brodie JA, Grossma AC, Xu P, Brawley SH (2010) Porphyra: a marine crop shaped by stress. Trends Plant Sci 16:29–37
Chen CS, Ji DH, Xie CT, Xu Y, Liang Y, Zhen YJ, Shi XZ, Wang FX, Zhao LM (2008) Preliminary study on selecting the high temperature resistance strains and economic traits of Porphyra haitanensis. Acta Oceanol Sinica 30:100–106 (in Chinese with English abstract)
Chen CS, Dai ZZ, Xu Y, Ji DH, Xie CT (2016) Cloning, expression, and characterization of carbonic anhydrase genes from Pyropia haitanensis (Bangiales, Rhodophyta). J Appl Phycol 28:1403–1417
Choi CS, 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
Davison IR, Pearson GA (1996) Stress tolerance in intertidal seaweeds. J Phycol 32:197–211
Duncan RF, Hershey JW (1989) Protein synthesis and protein phosphorylation during heat stress, recovery, and adaptation. J Cell Biol 109:1467–1481
Harrison A, Parle-McDermott A (2011) DNA methylation: a timeline of methods and applications. Frontn Genet 2:74
Henderson IR, Jacobsen SE (2007) Epigenetic inheritance in plants. Nature 447:418–424
Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1105
Ji DH, Li B, Xu Y, Chen CS, Xie CT (2015) Cloning and quantitative analysis of five heat shock protein 70 genes from Pyropia haitanensis. J Appl Phycol 27:499–509
Johnston JW, Benson EE, Harding K (2009) Cryopreservation induces temporal DNA methylation epigenetic changes and differential transcriptional activity in Ribes germplasm. Plant Physiol Biochem 47:123–131
Kapuy O, Lizák B, Stiller I, Bánhegyi G (2014) A systems biological perspective of cellular stress-directed programmed cell death. Comp Molec Biosci 4:28–34
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, Fedman M, Levy AA (2003) Transcriptional activation of retro-transposons alters the expression of adjacent genes in wheat. Nat Genet 33:102–106
Kim MY, Zilberman D (2014) DNA methylation as a system of plant genomic immunity. Trends Plant Sci 19:320–326.
Kumar G, Rattan UK, Singh AK (2016) Chilling-mediated DNA methylation changes during dormancy and its release reveal the importance of epigenetic regulation during winter dormancy in apple (Malus x domestica Borkh). PLoS One 11:e0149934
Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220
McClelland M, Nelson M, Raschke E (1994) Effect of site-specific modification on restriction endonucleases and DNA modification methyl-transferases. Nucleic Acid Res 22:3640–3659
Mirouze M, Paszkowski J (2011) Epigenetic contribution to stress adaptation in plants. Curr Opin Plant Biol 14:267–274
Pan YJ, Wang WS, Zhao XQ, Zhu LH, Fu BY, Li ZK (2011) DNA methylation alterations of rice in response to cold stress. Plant Omics J 7:364–369
Portis E, Acquadro A, Comino C, Lanteri S (2004) Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP). Plant Sci 166:169–178
Rantong G, Gunawardena AH (2015) Programmed cell death: genes involved in signaling, regulation, and execution in plants and animals. Botany 93:193–210
Reinders J, Wulff BB, Mirouze M, Marí-Ordóñez 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
Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiol Plant 120:179–186
Sanchez DH, Paszkowski J (2014) Heat-induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene. PLoS Genet 10:e1004806
Santos AP, Ferreira L, Maroco J, Oliveira MM (2011) Abiotic stress and induced DNA hypomethylation cause interphase chromatin structural changes in rice rDNA loci. Cytogenet Genome Res 132:297–303
Shan XH, Wang XY, Yang G, Ying W, SZ S, Li SP, Liu HK, Yuan YP (2013) 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
Sirisha VL, Sinha M, D'Souza JS (2014) Menadione-induced caspase-dependent programmed cell death in the green chlorophyte Chlamydomonas reinhardtii. J Phycol 50:587–601
Sun W, Van MM, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9
Wang WL, Lin YH, Teng F, Ji DH, Xu Y, Chen CS, Xie CT (2018) Comparative transcriptome analysis between heat-tolerant and sensitive Pyropia haitanensis strains in response to high temperature stress. Algal Res 29:104–112
Xie CT, Li B, Xu Y, Ji DH, Chen CS (2013) Characterization of the global transcriptome for Pyropia haitanensis (Bangiales, Rhodophyta) and development of cSSR markers. BMC Genomics 14:107
Xu Y, Chen CS, Ji DH, Hang N, Xie CT (2014) Proteomic profile analysis of Pyropia haitanensis in response to high-temperature stress. J Appl Phycol 26:607–618
Xu K, Xu Y, Ji DH, Xie J, Chen CS, Xie CT (2016a) Proteomic analysis of the economic seaweed Pyropia haitanensis in response to desiccation. Algal Res 19:198–206
Xu Y, Chen CS, Ji DH, Xu K, Xie XX, Xie CT (2016b) Developing a core collection of Pyropia haitanensis using simple sequence repeat markers. Aquaculture 452:351–356
Yan HH, Kikuchi S, Neumann P, Zhang WL, Wu YF, Chen F, Jiang JM (2010a) Genome-wide mapping of cytosine methylation revealed dynamic DNA methylation patterns associated with genes and centromeres in rice. Plant J 63:353–365
Yan XH, Lv F, Liu CJ, Zheng YF (2010b) Selection and characterization of a high-temperature tolerant strain of Porphyra haitanensis Chang et Zheng (Bangiales, Rhodophyta). J Appl Phycol 22:511–516
Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2006) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69
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We thank LetPub (www.LetPub.com) for its linguistic assistance during the preparation of this manuscript.
Funding
The Natural Science Foundation of Fujian Province, China (Grant No. 2014J07006) and the National Natural Science Foundation of China (Grant No. 41276177) supported this study.
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Chaotian Xie and Changsheng Chen designed the experiment; Chenjia Yu, Yan Xu, and Dehua Ji participated in sample collection, experimentation, and bioinformatics analysis; Chenjia Yu and Wenlei Wang processed the data, Chenjia Yu prepared the manuscript, and Chaotian Xie and Kai Xu revised the manuscript.
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Yu, C., Xu, K., Wang, W. et al. Detection of changes in DNA methylation patterns in Pyropia haitanensis under high-temperature stress using a methylation-sensitive amplified polymorphism assay. J Appl Phycol 30, 2091–2100 (2018). https://doi.org/10.1007/s10811-017-1363-4
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DOI: https://doi.org/10.1007/s10811-017-1363-4