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Whole-genome methylation analysis reveals epigenetic differences in the occurrence and recovery of hyperhydricity in Dendrobium officinale plantlets

  • Plant Tissue Culture
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Abstract

DNA methylation is one of the important contents of epigenetics research, and it is inseparable from the occurrence of various biological processes. To explore the epigenetic mechanism of hyperhydricity development and recovery in Dendrobium officinale, whole-genome bisulfite sequencing was performed to systematically analyze the extent and patterns of cytosine methylation in the normal plantlets (Normal), hyperhydric plantlets (HH), and hyperhydric plantlets cultured with K2SiO3 (HH-Si). The CHH context accounted for the largest proportion of methylated cytosine site in D. officinale. There was no significant difference in the degree of methylation in the CG context among the HH vs. Normal, HH-Si vs. HH, and HH-Si vs. Normal. The methylation level in the CHH context decreased with hyperhydricity, while the exogenous addition of silicon increased the methylation level of hyperhydric plantlets. In addition, 36,944 differentially methylated regions were detected in our study. GO enrichment analysis of differentially methylated genes revealed that various methylation sites were involved in different processes and pathways. In HH vs. Normal and HH-Si vs. HH, CHH-DMGs are closely related to the redox system. A cointegration analysis of transcriptome sequencing and methylation data showed that the expression levels of most differentially expressed genes were positively correlated to the methylation level. Our research provides references for an in-depth understanding of plant oxidative stress response mechanisms, as well as new insights into the epigenetic regulation of gene expression in the occurrence and restoration of hyperhydricity.

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References

  • Ai Y, Jing S, Cheng Z, Song B, Liu J, Zhou J (2021) Horticulture Research DNA methylation affects photoperiodic tuberization in potato (Solanum tuberosum L.) by mediating the expression of genes related to the photoperiod and GA pathways. Hortic Res 8:181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An Y, Goettel W, Han Q, Bartels A, Liu Z, Xiao W (2017) Dynamic changes of genome-wide DNA methylation during soybean seed development. Sci Rep 7:12263

    Article  PubMed  PubMed Central  Google Scholar 

  • Bakir Y, Eldem V, Zararsiz G, Turgay U (2016) Global transcriptome analysis reveals differences in gene expression patterns between nonhyperhydric and hyperhydric peach leaves. Plant Genome-US 9. https://doi.org/10.3835/plantgenome2015.09.0080

  • Casanova E, Moysset L, Trillas MI (2008) Effects of agar concentration and vessel closure on the organogenesis and hyperhydricity of adventitious carnation shoots. J Exp Med 52:1–8

    Google Scholar 

  • Cedar H, Bergman Y (2012) Programming of DNA methylation patterns. Annu Rev Biochem 81:97–117

    Article  CAS  PubMed  Google Scholar 

  • Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng J, Kou S, Zou Q, Li P, Zhang C, Yuan P (2018) DNA methylation and plant stress responses. J Plant Physiol Pathol 6:4. https://doi.org/10.4172/2329-955X.1000182

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Xia X, An L, Liang Y (2017) Reversion of hyperhydricity in pink (Dianthus chinensis L.) plantlets by AgNO3 and its associated mechanism during in vitro culture. Plant Sci 254:1–11

    Article  CAS  PubMed  Google Scholar 

  • Kakutani T, Saze H, Miura A, Inagaki S, Kobayashi A, Nakamura M, Tsukahara S, Fu Y (2012) Genetics of DNA methylation in genes and transposons in Arabidopsis. Genes Genet Syst 87:372–372

    Google Scholar 

  • Kang YJ, Bae A, Shim S, Lee T, Lee J, Satyawan D, Kim MY, Lee S (2017) Genome-wide DNA methylation profile in mung bean. Sci Rep-UK 7:40503

    Article  CAS  Google Scholar 

  • Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Lv C, Lan L, Jiang K, Zhang Y, Li N, Deng C, Gao W (2021) DNA methylation is involved in sexual differentiation and sex chromosome evolution in the dioecious plant garden asparagus. Hortic Res-England 8:198

    Article  CAS  Google Scholar 

  • Li X, Zhu J, Hu F, Ge S, Ye M, Xiang H, Zhang G, Zhang X, Zhang H, Zhang S (2012) Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics 13:300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Wei X, Sheng Z, Jiao G, Tang S, Luo J, Hu P (2017) Polycomb protein OsFIE2 affects plant height and grain yield in rice. PLoS ONE 11. https://doi.org/10.1371/journal.pone.0164748

  • Martienssen RA (2001) DNA methylation and epigenetic inheritance in plants and filamentous fungi. Science 293:1070–1074

    Article  CAS  PubMed  Google Scholar 

  • Meng D, Dubin M, Pei Z, Osborne EJ, Nordborg M (2016) Limited contribution of DNA methylation variation to expression regulation in Arabidopsis thaliana. PLoS Genet 12:e1006141. https://doi.org/10.1371/journal.pgen.1006141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peter M (2015) Epigenetic variation and environmental change. J Exp Bot 12:3541–3548

    Google Scholar 

  • Prabhakaran Soundararajan, Abinaya Manivannan, Yoon S (2017) Exogenous supplementation of silicon improved the recovery of hyperhydric shoots in Dianthus caryophyllus L. by stabilizing the physiology and protein expression. Front Plant Sci 8:738

    Article  Google Scholar 

  • Richards EJ (2011) Natural epigenetic variation in plant species: a view from the field. Curr Opin Plant Biol 14:204–209

    Article  CAS  PubMed  Google Scholar 

  • Sen A, Alikamanoglu S (2013) Antioxidant enzyme activities, malondialdehyde, and total phenolic content of peg-induced hyperhydric leaves in sugar beet tissue culture. In Vitro Cell Dev-Plant 49:396–404

    Article  CAS  Google Scholar 

  • Sivanesan I, Park SW (2014) The role of silicon in plant tissue culture. Front Plant Sci 5:571

    Article  PubMed  PubMed Central  Google Scholar 

  • Sowbiya M, Hao W, Yoo P, Hai J, Byoung J (2017) Proteomic analysis reveals the dynamic role of silicon in alleviation of hyperhydricity in carnation grown in vitro. Int J Mol Sci 19:50

    Article  Google Scholar 

  • Su C, Wang C, He L, Yang C, Wang Y (2014) Shotgun bisulfite sequencing of the Betula platyphylla genome reveals the tree’s DNA methylation patterning. Int J Mol Sci 15:22874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun S, Zhu J, Guo R, Whelan J, Shou H (2021) DNA methylation is involved in acclimation to iron deficiency in rice (Oryza sativa). Plant J 107:727–739

    Article  CAS  PubMed  Google Scholar 

  • Tabart J, Franck T, Kevers C, Dommes J (2015) Effect of polyamines and polyamine precursors on hyperhydricity in micropropagated apple shoots. Plant Cell Tiss Org 120:11–18

    Article  CAS  Google Scholar 

  • Tang M, Xu L, Wang Y, Dong J, Zhang X, Wang K, Ying J, Li C, Liu L (2021) Melatonin-induced DNA demethylation of metal transporters and antioxidant genes alleviates lead stress in radish plants. Hortic Res-England 8:124

    Article  CAS  Google Scholar 

  • Tian J, Cheng Y, Kong X, Liu M, Jiang F, Zhen W (2017) Induction of reactive oxygen species and the potential role of NADPH oxidase in hyperhydricity of garlic plantlets in vitro. Protoplasma 254:379–388

    Article  CAS  PubMed  Google Scholar 

  • Toshiro I, Hajime S, Elliot MM (2003) Whorl-specific expression of the SUPERMAN gene of Arabidopsis is mediated by cis elements in the transcribed region. Curr Biol 13:1524–1530

    Article  Google Scholar 

  • Underwood CJ, Henderson IR, Martienssen RA (2017) Genetic and epigenetic variation of transposable elements in Arabidopsis. Curr Opin Plant Biol 36:135–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valpuesta V, Botella MA (2005) Biosynthesis of L-ascorbic acid in plants: new pathways for an old antioxidant. Trends Plant Sci 9:573–577

    Article  Google Scholar 

  • Wang B, Luo Q, Li Y, Yin L, Zhou N, Li X, Gan J, Dong A (2020) Structural insights into target DNA recognition by R2R3-MYB transcription factors. Nucleic Acids Res 48:460–471

    CAS  PubMed  Google Scholar 

  • Xu J, Zhou S, Gong X, Yi S, Guan Q (2018) Single-base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple. Plant Biotechnol J 16:672–687

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Lang Z, Zhu JK (2018) Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol 19:489–506

    Article  CAS  PubMed  Google Scholar 

  • Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, Mcquinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31:154–159

    Article  CAS  PubMed  Google Scholar 

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Funding

The Guangdong Basic and Applied Basic Research Foundation (2019A1515111043), the Youth Innovative Talents Project by the Educational Department of Guangdong Province (2019KQNCX057), the Special Fund for Science and Technology Innovation Cultivation of Guangdong University Students (special fund for “climbing plan”) (51348227), the Scientific Research Project of the Traditional Chinese Medicine Bureau of Guangdong Province (20202104), the Natural Science Foundation of Zhejiang Province (LY21B060007), and Shandong Qingyu Jiangxing Biotechnology Co., Ltd.(KYY-HX-20210702) supported this study.

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Authors and Affiliations

  1. School of Traditional Chinese Medicine, Guangdong Pharmaceutical University, Guangzhou, 510006, China

    Huiju Zhang, Min Shi, Shuting Su, Sikai Zheng, Miao Wang, Jun Lv, Quan Yang & Hongyang Gao

  2. College of Pharmaceutical Science, Zhejiang University of Technology, Hangzhou, 310014, Zhejiang, China

    Xudong Wang

  3. Key Laboratory of State Administration of Traditional Chinese Medicine for Production & Development of Cantonese Medicinal Materials, Guangzhou, 510006, China

    Quan Yang & Hongyang Gao

  4. Guangdong Provincial Research Center On Good Agricultural Practice & Comprehensive Agricultural Development Engineering Technology of Cantonese Medicinal Materials, Guangzhou, 510006, China

    Quan Yang & Hongyang Gao

  5. Comprehensive Experimental Station of Guangzhou, Chinese Material Medica, China Agriculture Research System (CARS-21-16), Guangzhou, 510006, China

    Quan Yang & Hongyang Gao

Authors
  1. Huiju Zhang
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  2. Min Shi
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  3. Shuting Su
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  4. Sikai Zheng
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  5. Miao Wang
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  6. Jun Lv
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  7. Xudong Wang
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  8. Quan Yang
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  9. Hongyang Gao
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Contributions

Huiju Zhang, Min Shi: conceptualization, methodology, formal analysis, investigation, data curation, methodology, writing—original draft, visualization. Shuting Su, Sikai Zheng, Miao Wang, Jun Lv: investigation, data curation, writing—original draft. Xudong Wang: resources, writing—review and editing. Quan Yang: resources, funding acquisition, writing—review and editing. Hongyang Gao: supervision, project administration, funding acquisition.

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Correspondence to Hongyang Gao.

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The authors declare no competing interests.

Additional information

Huiju Zhang and Min Shi contributed equally to this work and should be considered co-first authors.

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Zhang, H., Shi, M., Su, S. et al. Whole-genome methylation analysis reveals epigenetic differences in the occurrence and recovery of hyperhydricity in Dendrobium officinale plantlets. In Vitro Cell.Dev.Biol.-Plant 58, 290–301 (2022). https://doi.org/10.1007/s11627-022-10250-3

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  • DOI: https://doi.org/10.1007/s11627-022-10250-3

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