Skip to main content
Download PDF

DNA methylation polymorphism and stability in Chinese indica hybrid rice

Science China Life Sciences volume 56, pages 1097–1106 (2013)Cite this article

Abstract

Conventional rice breeding has long focused on exploiting the DNA sequence diversity. However, epigenetic diversity, reflected particularly in DNA methylation, can also contribute to phenotypic variation and should not be overlooked in rice breeding. In this study, 20 parental lines of indica rice, which are widely used in hybrid rice breeding in China, were analyzed to investigate variations of DNA methylation and its inheritance. The results revealed a wide diversity in DNA methylation among these breeding lines. A positive correlation was seen between DNA methylation and genetic diversity. Furthermore, some of the methylated DNA was inherited in the subsequent generation, regardless of whether they were produced by selfing or hybrid-crossing. This study provides insight into the methylation patterns in rice, and suggests the importance of epigenetic diversity in rice breeding.

References

  1. Becker C, Hagmann J, Muller J, et al. Spontaneous epigenetic variation in the Arabidopsis thaliana methylome. Nature, 2011, 480: 245–249

    PubMed  CAS  Article  Google Scholar 

  2. Sha A H, Lin X H, Huang J B, et al. Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP (MSAP) analysis. Mol Genet Genomics, 2005, 273: 484–490

    PubMed  CAS  Article  Google Scholar 

  3. Akimoto K, Katakami H, Kim H J, et al. Epigenetic inheritance in rice plants. Ann Bot (Lond), 2007, 100: 205–217

    CAS  Article  Google Scholar 

  4. Fieldes M A. Heritable effects of 5-azacytidine treatments on the growth and development of flax (Linum usitatissimum) genotrophs and genotypes. Genome, 1994, 37: 1–11

    PubMed  CAS  Article  Google Scholar 

  5. Qi X, Li Z H, Jiang L L, et al. Grain-yield heterosis in Zea mays L. shows positive correlation with parental difference in CHG methylation. Crop Sci, 2010, 50: 2338–2346

    CAS  Google Scholar 

  6. Habu Y, Kakutani T, Paszkowski J. Epigenetic developmental mechanisms in plants: Molecules and targets of plant epigenetic regulation. Curr Opin Genet Dev, 2001, 11: 215–220

    PubMed  CAS  Article  Google Scholar 

  7. Kakutani T. Epi-alleles in plants: Inheritance of epigenetic information over generations. Plant Cell Physiol, 2002, 43: 1106–1111

    PubMed  CAS  Article  Google Scholar 

  8. Guo Z, Zeng L, Li M, et al. Inheritance of DNA methylation in DH and its backcrossed lines of Brassica napus. Afr J Biotechnol, 2011, 10: 7736–7745

    CAS  Google Scholar 

  9. Teixeira F K, Heredia F, Sarazin A, et al. A role for RNAi in the selective correction of DNA methylation defects. Science, 2009, 323: 1600–1604

    PubMed  CAS  Article  Google Scholar 

  10. Peng H, Zhang J. Plant genomic DNA methylation in response to stresses: Potential applications and challenges in plant breeding. Prog Nat Sci, 2009, 14: 265–271

    Google Scholar 

  11. Xie Q, Peng H. Breeding and utilization of good quality Indica CMS line Jinke 1A in rice (in Chinese). Hybrid Rice, 2007, 22: 11–13

    Google Scholar 

  12. Hoagland D R, Arnon D I. The water-culture method for growing plants without soil. Berkeley: College of Agriculture, University of California, 1950

    Google Scholar 

  13. Keyte A L, Percifield R, Liu B, et al. Infraspecific DNA methylation polymorphism in cotton (Gossypium hirsutum L.). J Hered, 2006, 97: 444–450

    PubMed  CAS  Article  Google Scholar 

  14. Ajibade S R, Weeden N F, Chite S M. Inter simple sequence repeat analysis of genetic relationships in the genus Vigna. Euphytica, 2000, 111: 47–55

    CAS  Article  Google Scholar 

  15. Yeh F, Yang R, Boyle T, et al. POPGEN Ver. 1.32. The user-friendly software for population genetic analysis. Molecular Biology and Bio-technology Center, University of Alberta, Alberta, Canada, 1997

    Google Scholar 

  16. Mantel N. The detection of disease clustering and a generalized regression approach. Cancer Res, 1967, 27: 209–220

    PubMed  CAS  Google Scholar 

  17. Tamura K, Peterson D, Peterson N, et al. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evoluti-onary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28: 2731–2739

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  18. McClelland M, Nelson M, Raschke E. Effect of site-specific modification on restriction endonucleases and DNA modification methyltransferases. Nucleic Acids Res, 1994, 22: 3640–3659

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  19. Xiong L Z, Xu C G, Saghai Maroof M A, et al. Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet, 1999, 261: 439–446

    PubMed  CAS  Article  Google Scholar 

  20. Ashikawa I. Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars. Plant Mol Biol, 2001, 45: 31–39

    PubMed  CAS  Article  Google Scholar 

  21. Nei M. Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA, 1973, 70: 3321–3323

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  22. Nimmakayala P, Vajja G, Gist R A, et al. Effect of DNA methylation on molecular diversity of watermelon heirlooms and stability of methylation specific polymorphisms across the genealogies. Euphytica, 2011, 177: 79–89

    CAS  Article  Google Scholar 

  23. He G, Zhu X, Elling A A, et al. Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell, 2010, 22: 17–33

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  24. Cokus S J, Feng S, Zhang X, et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature, 2008, 452: 215–219

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  25. Li X, Zhu J, Hu F, et al. Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics, 2012, 13: 300

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  26. Zhang X Y, Yazaki J, Sundaresan A, et al. Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell, 2006, 126: 1189–1201

    PubMed  CAS  Article  Google Scholar 

  27. Schmitz R J, Schultz M D, Urich M A, et al. Patterns of population epigenomic diversity. Nature, 2013, 495: 193–198

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  28. Liu C G, Zhang G Q. SSR analysis of genetic diversity and the temporal trends of major commercial inbred indica rice cultivars in south China in 1949–2005 (in Chinese). Acta Agron Sin, 2010, 36: 1843–1852

    CAS  Article  Google Scholar 

  29. Takata M, Kishima Y, Sano Y. DNA methylation polymorphisms in rice and wild rice strains: Detection of epigenetic markers. Breeding Sci, 2005, 55: 57–63

    CAS  Article  Google Scholar 

  30. Yang W, Yu X, Liu B. Parental epigenetic difference in DNA methylation-level may play contrasting roles for different agronomic traits related to yield heterosis in maize. Afr J Biotechnol, 2011, 10: 9253–9263

    CAS  Google Scholar 

  31. Levi A, Thomas C E, Newman M, et al. ISSR and AFLP markers differ among American watermelon cultivars with limited genetic diversity. J Am Soc Hortic Sci, 2004, 129: 553–558

    CAS  Google Scholar 

  32. Peng H, Xi T, Zhang J, et al. Stability of stress-Induced DNA methylation in plant (in Chinese). Acta Agron Sin, 2011, 44: 2431–2438

    CAS  Google Scholar 

  33. Schmitz R J, Schultz M D, Lewsey M G, et al. Transgenerational epigenetic instability is a source of novel methylation variants. Science, 2011, 334: 369–373

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  34. Messeguer R, Ganal M W, Steffens J C, et al. Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol Biol, 1991, 16: 753–770

    PubMed  CAS  Article  Google Scholar 

  35. Greaves I K, Groszmann M, Ying H, et al. Trans chromosomal methylation in Arabidopsis hybrids. Proc Natl Acad Sci USA, 2012, 109: 3570–3575

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  36. Birchler J A, Auger D L, Riddle N C. In search of the molecular basis of heterosis. Plant Cell, 2003, 15: 2236–2239

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  37. Swanson-Wagner R A, Jia Y, DeCook R, et al. All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA, 2006, 103: 6805–6810

    PubMed  CAS  PubMed Central  Article  Google Scholar 

  38. Springer N M, Stupar R M. Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res, 2007, 17: 264–275

    PubMed  CAS  Article  Google Scholar 

  39. Tarutani Y, Shiba H, Iwano M, et al. Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature, 2010, 466: 983–986

    PubMed  CAS  Article  Google Scholar 

  40. Zhang M S, Yan H Y, Zhao N, et al. 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, 2007, 115: 195–207

    PubMed  CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

  1. Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, 100101, China

    Hai Peng, GuangHuai Jiang & WenXue Zhai

  2. Institute for Systems Biology and College of Life Science, Jianghan University, Wuhan, 430056, China

    Hai Peng, Jing Zhang & Weixiong Zhang

  3. Department of Computer Science and Department of Genetics, Washington University, St. Louis, MO, 63130, USA

    Weixiong Zhang

Authors
  1. Hai Peng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. GuangHuai Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Weixiong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. WenXue Zhai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to WenXue Zhai.

Additional information

Contributed equally to this work

This article is published with open access at Springerlink.com

Electronic supplementary material

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Reprints and Permissions

About this article

Cite this article

Peng, H., Jiang, G., Zhang, J. et al. DNA methylation polymorphism and stability in Chinese indica hybrid rice. Sci. China Life Sci. 56, 1097–1106 (2013). https://doi.org/10.1007/s11427-013-4576-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-013-4576-z

Keywords

  • epigenetic diversity
  • genetic diversity
  • rice breeding line