Skip to main content
SpringerLink
Log in

Analysis of DNA methylation during spontaneous rooting from the stem apex in Rubus idaeus

  • Research Papers
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Rubus idaeus L. is of great economic value. Some varieties of Rubus idaeus have a unique feature of spontaneous rooting from the stem apex. To determine whether DNA methylation is associated with the spontaneous rooting process, variations in the methylation at stem apex during four root developmental stages were investigated, using the methylation-sensitive amplification polymorphism (MSAP) technique and the bisulfite sequencing analysis (BSA). The results showed that the DNA methylation levels and patterns were significantly different between the four developmental stages. A total of 824 CCGG amplified sites were detected by MSAP. MSAP screening revealed that the level of DNA methylation at stages I to IV was 34.95, 36.04, 36.29, and 37.50%, respectively. The number of methylated sites and their methylation levels tended to decrease at stages III and IV (root differentiation and elongation) compared with those at stage I (stem elongation). After cloning and sequencing of the 16 polymorphic differentially methylated DNA fragments, BLAST search results indicated that they might be involved in differentiation of the lateral root primordium, plant defense, signal transduction, and energy metabolism. Results of the qRT-PCR and BSA analyses confirmed that methylation of some key genes was closely associated with their expression at the different developmental stages. These findings could be useful for future studies on the potential role of DNA methylation in spontaneous rooting from the stem apex, implying its importance in rooting regulation and rapid expansion of raspberry populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

AR:

adventitious rooting

BSA:

bisulfite sequencing analysis

MSAP:

methylation-sensitive amplification polymorphism

NR:

non-redundant database

RLKs:

receptor-like protein kinases

References

  1. Brennan, R. and Graham, J., Improving fruit quality in Rubus and Ribes through breeding, Funct. Plant Sci. Biotechnol., 2009, vol. 3, pp. 22–29.

    Google Scholar 

  2. Heslop-Harrison, Y., Natural and induced rooting of the stem apex in Rubus, Ann. Bot., 1959, vol. 23, pp. 307–318.

    Article  Google Scholar 

  3. Cao, D., Gao, X., Liu, J., Wang, X.P., Geng, S.J., Yang, C.W., Liu, B., and Shi, D.C., Root-specific DNA methylation in Chloris virgata, a natural alkalineresistant halophyte, in response to salt and alkaline stresses, Plant Mol. Biol. Rep., 2012, vol. 30, pp. 1102–1109.

    Article  CAS  Google Scholar 

  4. Osabe, K., Clement, J.D., Bedon, F., Pettolino, F.A., Ziolkowski, L., Llewellyn, D.J., Walford, S.A., Dennis, E.S., Llewellyn, D.J., and Wilson, I.W., Genetic and DNA methylation changes in cotton (Gossypium) genotypes and tissues, PLoS One, 2014, vol. 9, no. 1. p. e86049. doi 10.1371/journal.pone.0086049

    Article  PubMed  PubMed Central  Google Scholar 

  5. Pikaard, C.S. and Scheid, O.M., Epigenetic regulation in plants, Cold Spring Harb. Perspect. Biol., 2014, vol. 6. p. a019315. doi 10.1101/cshperspect.a019315

    Article  PubMed  PubMed Central  Google Scholar 

  6. Kawakatsu., T., Stuart, T., Valdes, M., Breakfield, N., Schmitz, R.J., Nery, J.R., Urich, M.A., Han, X., Lister, R., Benfey, P.N., and Ecker, J.R., Unique celltype-specific patterns of DNA methylation in the root meristem, Nat. Plants, 2016, vol. 2. doi 10.1038/nplants.2016.58

  7. Shemer, O., Landau, U., Candela, H., Zemach, A., and Williams, L.E., Competency for shoot regeneration from Arabidopsis root explants is regulated by DNA methylation, Plant Sci., 2015, vol. 238, pp. 251–261.

    Article  CAS  PubMed  Google Scholar 

  8. Cheng, Y.Q., Liu, J.F., Yang, X., Ma, R., Liu, C., and Liu, Q., RNA-seq analysis reveals ethylene-mediated reproductive organ development and abscission in soybean (Glycine max L. Merr.), Plant Mol. Biol. Rep., 2013, vol. 31, pp. 607–619.

    Article  CAS  Google Scholar 

  9. Cheng, Y., Wang, J., Liu, J., Zhao, Y., Geng, W., and Zhang, H., Analysis of ovary DNA methylation during delayed fertilization in hazel using the methylationsensitive amplification polymorphism technique, Acta Physiol. Plant., 2015, vol. 37, p. 231. doi 10.1007/s11738-015-1984-7

    Article  Google Scholar 

  10. Bassam, B.J., Caetano-Anollés, G., and Gresshoff, P.M., Fast and sensitive silver staining of DNA in polyacrylamide gels, Anal. Biochem., 1991, vol. 196, pp. 80–83.

    Article  CAS  PubMed  Google Scholar 

  11. Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., and Madden, T.L., NCBI BLAST: a better web interface, Nucleic Acids Res., 2008, vol. 36: W5–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Schmittgen, T.D. and Livak, K.J., Analyzing real-time PCR data by the comparative CTmethod, Nat. Protoc., 2008, vol. 3, pp. 1101–1108.

    Article  CAS  PubMed  Google Scholar 

  13. Yendrek, C.R., Lee, Y.C., Morris, V., Liang, Y., Pislariu, C.I., Burkart, G., Meckfessel, M.H., Salehin, M., Kessler, H., Wessler, H., Lloyd, M., Lutton, H., Teillet, A., Sherrier, D.J., Journet, E.P., et al., Putative transporter is essential for integrating nutrient and hormone signaling with lateral root growth and nodule development in Medicago truncatula, Plant J., 2010, vol. 62, pp. 100–112.

    Article  CAS  PubMed  Google Scholar 

  14. Jenuwein, T. and Allis, C.D., Translating the histone code, Science, 2001, vol. 293, pp. 1074–1080.

    Article  CAS  PubMed  Google Scholar 

  15. Widman, N., Feng, S., Jacobsen, S.E., and Pellegrini, M., Epigenetic differences between shoots and roots in Arabi dopsis reveals tissue-specific regulation, Epigenetics, 2014, vol. 9, pp. 236–242.

    Article  CAS  PubMed  Google Scholar 

  16. Jones, P.A., Functions of DNA methylation: islands, start sites, gene bodies and beyond, Nat. Rev. Genet., 2012, vol. 13, no. 7, pp. 484–492.

    Article  CAS  PubMed  Google Scholar 

  17. Gojon, A., Krouk, G., Perrine-Walker, F., and Laugier, E., Nitrate transceptor(s) in plants, J. Exp. Bot., 2011, vol. 62, pp. 2299–2308.

    Article  CAS  PubMed  Google Scholar 

  18. Léran, S., Muños, S., Brachet, C., Tillard, P., Gojon, A., and Lacombe, B., Arabidopsis NRT1.1 is a bidirectional transporter involved in root-to-shoot nitrate translocation, Mol. Plant., 2013, vol. 6, pp. 1984–1987.

    Article  PubMed  Google Scholar 

  19. Shimizu, N., Ishida, T., Yamada, M., Shigenobu, S., Tabata, R., Kinoshita, A., Yamaguchi, K., Hasebe, M., Mitsumasu, K., and Sawa, S., BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root, New Phytol., 2015, vol. 208, pp. 1104–1113.

    Article  CAS  PubMed  Google Scholar 

  20. Lavenus, J., Goh, T., Guyomarc’h, S., Hill, K., Lucas, M., Voß, U., Kenobi, K., Wilson, M.H., Farcot, E., Hagen, G., Guilfoyle, T.J., and Fukaki, H., Inference of the Arabidopsis lateral root gene regulatory network suggests a bifurcation mechanism that defines primordia flanking and central zones, Plant Cell, 2015, vol. 114, no. 5, pp. 1368–1388.

    Article  Google Scholar 

  21. Saze, H., Tsugane, K., Kanno, T., and Nishimura, T., DNA methylation in plants: relationship to small RNAs and histone modifications, and functions in transposon inactivation, Plant Cell Physiol., 2012, vol. 53, pp. 766–784.

    Article  CAS  PubMed  Google Scholar 

  22. Us-Camas, R., Rivera-Solís, G., Duarte-Aké, F., and De-la-Peña C., In vitro culture: an epigenetic challenge for plants, Plant Cell Tissue Organ Cult., 2014, vol. 118, pp. 187–201.

    Article  CAS  Google Scholar 

  23. Bird, A.P. and Wolffe, A.P., Methylation-induced repression—belts, braces, and chromatin, Cell, 1999, vol. 99, pp. 451–454.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Jilin Provincial Key Laboratory of Plant Resource Science and Green Production, Jilin Normal University, Siping City of Jilin Province, 136000, China

    Y. Cheng, W. Geng, B. Yang & J. Liu

Authors
  1. Y. Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. W. Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Liu.

Additional information

The article is published in the original.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cheng, Y., Geng, W., Yang, B. et al. Analysis of DNA methylation during spontaneous rooting from the stem apex in Rubus idaeus . Russ J Plant Physiol 64, 566–575 (2017). https://doi.org/10.1134/S1021443717040033

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443717040033

Keywords

Search

Navigation