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Study on the relationship between genetic variation of DNA methylation and heterosis in soybean leaves

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Abstract

In order to well understand the molecular basis of heterosis in soybean, the methylation-sensitive amplification polymorphism (MSAP) method based on capillary electrophoresis was used to estimate levels and patterns of cytosine methylation in 15-day post-emergence leaves of four parental lines [Jilin 47 (no. 19), EXP (no. 12), Jilin 38 (no. 3) and Yi 3 (no. 6)] and 12 hybrids [Jilin 38 × Yi 3(3 ×  6), Jilin 38 ×  EXP(3 ×  12), Jilin 38 ×  Jilin 47(3 ×  19), Yi 3 ×  Jilin 38(6 ×  3), Yi 3 ×  EXP(6 ×  12), Yi 3 ×  Jilin 47(6 ×  19), EXP × Jilin 38(12 × 3), EXP × Yi 3(12 ×  6), EXP ×  Jilin 47(12 ×  19), Jilin 47 ×  Jilin 38(19 ×  3), Jilin 47 × Yi 3(19 × 6), Jilin 47 × EXP(19 × 12)]. In addition, 12 traits of the hybrids and their parents were also analyzed to understand the relationship between DNA methylation variation and heterosis. MSAP results showed that the total relative methylation level of all hybrids was lower than the corresponding middle parent value, indicating that the methylation degree was decreasing. And may express a variety of genes related to the phenotypic variation of hybridization. Moreover, the hemi-methylation levels of Jilin 38 × Jilin 47 and Yi 3 × Jilin 47 hybrids and full-methylation levels of EXP × Yi 3 and EXP × Jilin 47 hybrids was significant higher than the corresponding mid-parent values. In addition, the heredity of methylation from parents in hybrids is more than the variations, in which there were four types appeared great higher: A1, B4, B8, and D2. Furthermore, the results of relationship between genetic variation in DNA methylation and heterosis showed that the hypo-methylation had a promoting effect to increase node number, and the hype-methylation of hybrids was helpful to add to stem thick. Our results may provide new insights into well understanding the molecular mechanisms of heterosis at the epigenetic level in soybean.

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References

  • Baránek M, Čechová J, Kovacs T, Eichmeier A, Wan S, Raddová J, Nečas T, Ye X (2016) Use of combined MSAP and NGS techniques to identify differentially methylated regions in somaclones: a case study of two stable somatic wheat mutants. PLoS ONE 11(10):e0165749

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA (2010) Heterosis. Plant Cell 22:2105–2112

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cappetta M, Berdasco M, Hochmann J, Bonilla C, Sans M, Hidalgo PC, Artagaveytia N, Kittles R, Martinez M, Esteller M, Bertoni B (2015) Effect of genetic ancestry on leukocyte global DNA methylation in cancer patients. BMC Cancer 15(1):434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dyachenko OV, Tarlachkov SV, Marinitch DV, Shevchuk TV, Buryanov YI (2014) Expression of exogenous DNA methyltransferases: application in molecular and cell biology. Biochemistry 79(2):77–87

    PubMed  CAS  Google Scholar 

  • Garg R, Chevala VN, Shankar R, Jain M (2015) Divergent DNA methylation patterns associated with gene expression in rice cultivars with contrasting drought and salinity stress response. Sci Rep 5:144922. https://doi.org/10.1038/srep14922

    Article  CAS  Google Scholar 

  • Hassan-Zadeh V, Rugg-Gunn P, Bazett-Jones DP (2017) DNA methylation is dispensable for changes in global chromatin architecture but required for chromocentre formation in early stem cell differentiation. Chromosoma 126(5):605–614. https://doi.org/10.1007/s00412-017-0625-x

    Article  PubMed  CAS  Google Scholar 

  • He GM, Zhu XP, Elling AA, Chen LB, Wang XF, Guo L, Liang MZ, He H, Zhang HY, Chen FF, Qi YJ, Chen RS, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • He GM, He H, Deng XW (2013) Epigenetic variations in plant hybrids and their potential roles in heterosis. J Genet Genomics 40:205–210

    Article  PubMed  CAS  Google Scholar 

  • Hernandez HG, Tse MY, Pang SC, Arboleda H, Forero DA (2013) Optimizing methodologies for PCR-based DNA methylation analysis. Biotechniques 55(4):181–197

    Article  PubMed  CAS  Google Scholar 

  • Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432

    Article  PubMed  CAS  Google Scholar 

  • Hsieh TF, Ibarra CA, Silva P, Zemach A, Eshed-Williams L, Fischer RL, Zilberman D (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324(5933):1451–1454

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Joel, Zhang (2001) Immune related genetic polymorphisms and schizophrenia among the Chinese. Hum Immunol 62(7):714–724

    Article  Google Scholar 

  • Kawanabe T, Ishikura S, Miyaji N, Sasaki T, Wu LM, Itabashi E, Takada S, Shimizu M, Takasa-Yasuda T, Osabe K, Peacock WJ (2016) Role of DNA methylation in hybrid vigor in Arabidopsis thaliana. Proc Natl Acad Sci USA 113(43):E6704–E6711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Keown CL, Berletch JB, Castanon R, Nery JR, Disteche CM, Ecker JR, Mukamel EA (2017) Allele-specific non-CG DNA methylation marks domains of active chromatin in female mouse brain. Proc Natl Acad Sci USA 114(14):E2882–E2890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kidwell KK, Osborn TC (1992) Simple plant DNA isolation procedures. In: Beckman JS, Osborn TC (eds) Plant genomes: methods for genetic and physical mapping. Kluwer, Dordrecht, pp 1–13

    Google Scholar 

  • Kumari R, Yadav G, Sharma V, Sharma V, Kumar S (2013) Cytosine hypomethylation at CHG and CHH sites in the pleiotropic mutants of Mendelian inheritance in Catharanthus roseus. J. Genet. 92(3):499–511

    Article  PubMed  CAS  Google Scholar 

  • Li A, Song WQ, Chen CB, Zhou YN, Qi LW, Wang CG (2013) DNA methylation status is associated with the formation of heterosis in Larix kaempferi intraspecific hybrids. Mol Breed 31(2):463–475

    Article  CAS  Google Scholar 

  • 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(9):2095–2103

    Article  PubMed  CAS  Google Scholar 

  • Liu B, Wendel JF (2003) Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol 29(3):365–379

    Article  PubMed  CAS  Google Scholar 

  • Luo JY, Pan XL, Peng TC, Chen YY, Zhao H, Mu L, Peng Y, He R, Tang H (2016) DNA methylation patterns of banana leaves in response to Fusarium oxysporum f. sp. cubense tropical race 4. J Integr Agric 15(12):2736–2744

    Article  CAS  Google Scholar 

  • Sakthivel K, Girishkumar K, Ramkumar G, Shenoy VV, Kajjidoni ST, Salimath PM (2010) Alterations in inheritance pattern and level of cytosine DNA methylation, and their relationship with heterosis in rice. Euphytica 175:303–314

    Article  CAS  Google Scholar 

  • Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14(4):1163–1175

    Article  PubMed  CAS  Google Scholar 

  • Sanetomo R, Hosaka K (2011) Reciprocal differences in DNA sequence and methylation status of the pollen DNA between F1 hybrids of Solanum tuberosum × S. demissum. Euphytica 182:219–229

    Article  CAS  Google Scholar 

  • Shull GH (1908) The composition of a field of maize. Am Breed Assoc. Rep. 4:296–301

    Google Scholar 

  • Shull GH (1952) Beginnings of the heterosis concept. In: Gowen JW (ed) Heterosis. A record of researches directed toward explaining and utilizing the vigor of hybrids. Iowa State College Press, Ames, pp 14–48

    Google Scholar 

  • Sun LF, Liu TJ, Liu HK, Shan XH, Su SZ, Li SP, Yuan YP, Zhang J (2015) Analysis of DNA cytosine methylation patterns in maize hybrids and their parents. Biol Plantarum 59(2):266–272

    Article  CAS  Google Scholar 

  • Venetsky A, Levy-Zamir A, Khasdan V, Domb K, Kashkush K (2015) Structure and extent of DNA methylation-based epigenetic variation in wild emmer wheat (T. turgidum ssp. dicoccoides) populations. BMC Plant Biol 15(1):200

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang B, Zhang M, Fu R, Qian X, Rong P, Zhang Y, Jiang P, Wang JJ, Lu XK, Wang D, Ye W, Zhu XY (2016a) Epigenetic mechanisms of salt tolerance and heterosis in Upland cotton (Gossypium hirsutum L.) revealed by methylation-sensitive amplified polymorphism analysis. Euphytica 208(3):477–491

    Article  CAS  Google Scholar 

  • Wang Y, Rong H, Xie T, Jiang J, Wu J (2016b) Comparison of DNA methylation in the developing seeds of yellow-and black-seeded Brassica napus through MSAP analysis. Euphytica 209(1):157–169

    Article  CAS  Google Scholar 

  • Xia H, Huang W, Xiong J, Tao T, Zheng X, Wei H, Yue Y, Chen L, Luo L (2016) Adaptive epigenetic differentiation between upland and lowland rice ecotypes revealed by methylation-sensitive amplified polymorphism. PLoS ONE 11(7):e0157810

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang H, Chang F, You C, Cui J, Zhu G, Wang L, Zheng Y, Qi J, Ma H (2015) Whole-genome DNA methylation patterns and complex associations with gene structure and expression during flower development in Arabidopsis. Plant J 81(2):268–281

    Article  PubMed  CAS  Google Scholar 

  • Zhang MS, Yan HY, Zhao N et al (2007) Endosperm-specific hypomethylation, and meiotic inheritance and variation of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) inter-strain hybrids. Theor Appl Genet 115:195–207

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Xu C, von Wettstein D, Liu B (2011) Tissue-specific differences in cytosine methylation and their association with differential gene expression in sorghum. Plant Physiol 156(4):1955–1966

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang T, Termanis A, Özkan B, Bao XX, Culley J, de Lima Alves F, Rappsilber J, Ramsahoye B, Stancheva I (2016) G9a/GLP complex maintains imprinted DNA methylation in embryonic stem cells. Cell Rep 15(1):77–85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao XX, Chai Y, Liu B (2007) Epigenetic inheritance and variation of DNA methylation level and pattern in maize intra-specific hybrids. Plant Sci 172:930–938

    Article  CAS  Google Scholar 

  • Zhao X, Ruan Y, Wei C-L (2008) Tackling the epigenome in the pluripotent stem cells. J Genetics Genom 35(7):403-412

    Article  PubMed  CAS  Google Scholar 

  • Zhu N, Cheng S, Liu X, Du H, Dai M, Zhou D-X, Yang W, Zhao Y (2015) The R2R3-type MYB gene OsMYB91 has a function in coordinating plant growth and salt stress tolerance in rice. Plant Sci 236:146–156

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This study was supported by the Jilin Provincial Science Foundation of China (20140101015JC) and Jilin Provincial Key Scientific and Technological Project of China (20150204004NY).

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Authors and Affiliations

  1. College of Agronomy, Jilin Agricultural University, Changchun, 130118, China

    Yuanqian Wang, Xiao Han, Sujie Fan, Xueying Li, Yiwei Qu, Dan Yao, Piwu Wang & Jun Zhang

  2. College of Agronomy, Northeast Agricultural University, Harbin, 150030, China

    Kaixin Zhang & Piwu Wang

  3. Key Laboratory of Modern Agricultural Cultivation and Crop Germplasm Improvement of Heilongjiang Province, Agronomy College of Heilongjiang Bayi Agricultural University, Daqing, 163319, China

    Lifang Sun & Piwu Wang

Authors
  1. Yuanqian Wang
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  2. Kaixin Zhang
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  3. Lifang Sun
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  4. Xiao Han
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  5. Sujie Fan
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  6. Xueying Li
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  7. Yiwei Qu
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  8. Dan Yao
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  9. Piwu Wang
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  10. Jun Zhang
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Contributions

Conceived and designed the experiments: Jun Zhang and Piwu Wang. Performed the experiments: Yuanqian, Kaixin Zhang, Xiao Han and Shujie Fan. Analyzed the data: Lifang Sun, Xueying Li and Yiwei Qu. Contributed reagents/materials/analysis tools: Dan Yao. Wrote the paper: Kaixin Zhang, Yuanqiang Wang and Lifang Sun. All authors read and approved the final version of the manuscript.

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Correspondence to Jun Zhang.

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Wang, Y., Zhang, K., Sun, L. et al. Study on the relationship between genetic variation of DNA methylation and heterosis in soybean leaves. Euphytica 214, 85 (2018). https://doi.org/10.1007/s10681-018-2161-z

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