Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Chromatin Structural Rearrangement during Dedifferentiation of Protoplasts of Cucumis sativus L.

  • Ondrej, Vladan (Department of Botany, Faculty of Science, Palacky University) ;
  • Kitner, Miloslav (Department of Botany, Faculty of Science, Palacky University) ;
  • Dolezalova, Ivana (Department of Botany, Faculty of Science, Palacky University) ;
  • Nadvornik, Petr (Department of Cell Biology and Genetics, Faculty of Science, Palacky University) ;
  • Navratilova, Bozena (Department of Botany, Faculty of Science, Palacky University) ;
  • Lebeda, Ales (Department of Botany, Faculty of Science, Palacky University)
  • Received : 2008.12.30
  • Accepted : 2009.02.17
  • Published : 2009.04.30
⟨ Previous Next ⟩

Abstract

This paper reports on the structural rearrangement of satellite DNA type I repeats and heterochromatin during the dedifferentiation and cell cycling of mesophyll protoplasts of cucumber (Cucumis sativus). These repeats were localized in the telomeric heterochromatin of cucumber chromosomes and in the chromocenters of interphase nuclei. The dramatic reduction of heterochromatin involves decondensation of subtelomeric repeats in freshly isolated protoplasts; however, there are not a great many remarkable changes in the expression profile. In spite of that, reformation of the chromocenters, occurring 48 h after protoplast isolation, is accompanied by recondensation of satellite DNA type I; however, only partial reassembly of these repeats was revealed. In this study, FISH and a flow cytometry assay show a correlation between the partial chromocenter and the repeats reassembly, and with the reentry of cultivated protoplasts into the cell cycle and first cell division. After that, divided cells displayed a higher variability in the expression profile than did leaves' mesophyll cells and protoplasts.

Keywords

Acknowledgement

Supported by : Ministry of Education of the Czech Republic

References

  1. Annis, S.L., and Goodwin, P.H. (1997). Recent advances in the molecular genetics of plant cell wall-degrading enzymes produced by plant pathogenic fungi. Eur. J. Plant. Pathol. 103, 1-14 https://doi.org/10.1023/A:1008656013255
  2. Bartova, E., Krejci, J., Harnicarova, A., Galiova, G., and Kozubek, S. (2008). Histone modifications and nuclear architecture: A review. J. Histochem. Cytochem. 56, 711-721 https://doi.org/10.1369/jhc.2008.951251
  3. Berta, G.L., Fusconi, A., Sampo, S., Lingua, G., Perticone, S., and Repetto, O. (2000). Polyploidy in tomato roots as affected by arbuscular mycorrhizal colonization. Plant Soil 226, 37-44 https://doi.org/10.1023/A:1026468810886
  4. Chen, J.Z., and Tian, L. (2007). Roles of dynamic and reversible histone acetylation in plant development and polyploidy. Biochim. Biophys. Acta 1769, 295-307 https://doi.org/10.1016/j.bbaexp.2007.04.007
  5. Cocking, E.C. (1960). A method for the isolation of plant protoplasts and vacuoles. Nature 187, 927-929
  6. Cremer, T., and Cremer, C. (2001). Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat. Rev. Genet. 2, 292-301 https://doi.org/10.1038/35066075
  7. Debeaujon, I., and Branchard, M. (1992). Induction of somatic embryogenesis and caulogenesis from cotyledon and leaf protoplast-derived colonies of melon (Cucumis melo L.). Plant Cell Rep. 12, 37-40
  8. Exner, V., and Hennig, L. (2008). Chromatin rearrangements in development. Curr. Opin. Plant Biol. 11, 64-69 https://doi.org/10.1016/j.pbi.2007.10.004
  9. Gajdova, J., Navratilova, B., Smolna, J., and Lebeda, A. (2007). Factor affecting protoplast isolation and cultivation of Cucumis spp. J. Appl. Bot. Food Quality 81, 1-6
  10. Ganal, M., Riede, I., and Hemleben, V. (1986). Organization and sequence analysis of two related satellite DNAs in cucumber (Cucumis satiuvus L.). J. Mol. Evol. 23, 23-30 https://doi.org/10.1093/jxb/23.1.23
  11. Goren, A., and Cedar, H. (2003). Replicating by the clock. Nat. Rev. Mol. Cell. Biol. 4, 25-32 https://doi.org/10.1038/nrm1008
  12. Jenuwein, T., and Allis, C.D. (2001). Translating the histone code. Science 293, 1074-1080 https://doi.org/10.1126/science.1063127
  13. Kitner, M., Lebeda, A., Dolezalova, I., Maras, M., Kristkova E., Nevo, E., Pavlicek, T., Meglic, V., and Beharav, A. (2008). AFLP analysis of Lactuca saligna germplasm collections from four European and three Middle Eastern countries. Israel J. Plant Sci. (in press)
  14. Koo, D.H., Hur, Y., Jin, D.C., and Bang, J.W. (2002). Karyotype analysis of a Korean cucumber cultivar (Cucumis sativus L. cv. Winter Long) using C-banding and bicolor fluorescence in sktu hybridization. Mol. Cells 13, 413-418
  15. Koo, D.H., Choi, H.W., Cho, J., Hur, Y., and Bang, J.W. (2005). A high-resolution karyotype of cucumber (Cucumis sativus L. Winter Long) revealed by C-banding, pachytene analysis, and RAPD-aided fluorescence in situ hybridization. Genome 48, 534-540 https://doi.org/10.1139/g04-128
  16. Kozubek, S., Lukasova E., Jirsova, P., Koutna, I., Kozubek, M., Ganova A., Bartova, E., Falk, M., and Pasekova, R. (2002). 3D structure of the human genome: order in randomness. Chromosoma 111, 321-331 https://doi.org/10.1007/s00412-002-0210-8
  17. Lebeda, A., Widrlechner, M.P., Staub, J., Ezura, H., Zalapa, J., and Kristkova E. (2007). Cucurbits (Cucurbitaceae; Cucumis spp., Cucurbita spp., Citrullus spp.). In Genetic Resources, Chromosome Engineering and Crop Improvement Series, Vol. 3 - Vegetable Crops, R.J. Singh, ed. (USA: CRC Press), pp. 271-376
  18. Mathieu, O., Jasencakova, Z., Vaillant, I., Gendrel, A.V., Colot, V., Schubert, I., and Tourmente, S. (2003). Changes in 5S rDNA chromatin organization and transcription during heterochromatin establishment in Aranidopsis. Plant Cell 15, 2929-2939 https://doi.org/10.1105/tpc.017467
  19. Milla, M.A.R., Maurer, A., Huete, A.R., and Gustafson, J.P. (2003). Glutathione peroxidise genes in Arabidopsis are ubiquitous and regulated by abiotic stresses through diverse signalling pathways. Plant J. 36, 602-615 https://doi.org/10.1046/j.1365-313X.2003.01901.x
  20. Ond$\check{r}$ej, V., Luk$\acute{a}$$\check{s}$ov$\acute{a}$, E., Krej$\check{c}$$\acute{i}$, J., Matula, P., and Kozubek, S.(2008). Lamin A/C and polymeric actin in genome organization. Mol. Cells OS, 356-361
  21. Papadakis, A.K., and Roubelakis-Angelakis, K.A. (2002). Oxidative stress could be responsible for the recalcitrance of plant protoplasts. Plant Physiol. Biochem. 40, 549-559
  22. Pecinka, A., Schubert, V., Maister, A., Kreth, G., Klatte, M., Lysak, M.A., Fuchs, J., and Schubert, I. (2004). Chromosome territory arrangement and homologous pairing in nuclei of Arabidopsis thaliana are predominantly random excerpt for NOR-bearing chromosomes. Chromosoma 113, 258-269 https://doi.org/10.1007/s00412-004-0316-2
  23. Sablowski, R. (2007). Flowering and determinancy in Arabidopsis. J. Exp. Bot. 58, 899-907 https://doi.org/10.1093/jxb/erm002
  24. Takebe, I., and Otsuki, Y. (1969). Infection of tobacco mesophyll protoplasts by tobacco mosaic virus. Proc. Natl. Acad. Sci. USA 64, 843-848 https://doi.org/10.1073/pnas.64.3.843
  25. Tessadori, F., van Driel, R., and Fransz, P. (2004). Cytogenetics as a tool to study gene regulation. Trends Plant Sci. 9 147-153 https://doi.org/10.1016/j.tplants.2004.01.008
  26. Tessadori, F., Chupeau, M.C., Chupeau, Y., Knip, M., Germann, S., van Driel, R., Fransz, P., and Gaudin, V. (2007). Large-scale dissociation and sequential reassembly of pericentric heterochromatin in dedifferentiated Arabidopsis cells. J. Cell Sci. 120, 1200-1208 https://doi.org/10.1242/jcs.000026
  27. van Driel, R., and Fransz, P. (2004). Nuclear architecture and genome functioning in plants and animals: what can we learn from both? Exp. Cell Res. 296, 86-90 https://doi.org/10.1016/j.yexcr.2004.03.009
  28. Vera-Estrella, R., Higgins, V.J., and Blumwald, E. (1994). Plant defense response to fungal pathogens. Plant Physiol. 106, 97-102 https://doi.org/10.1104/pp.106.1.97
  29. Verbsky, M.L., and Richards, E.J. (2001). Chromatin remodeling in plants. Curr. Opin. Plant Biol. 4, 494-500 https://doi.org/10.1016/S1369-5266(00)00206-5
  30. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Pelema, P., and Kuiper, M. (1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23, 4407-4414 https://doi.org/10.1093/nar/23.21.4407
  31. Yang, X., Tu, L., Zhu, L., Fu, L., Min, L., and Zhang, X. (2008). Expression profile analysis of genes involved in cell wall regeneration during protoplast culture in cotton by suppression subtractive hybridization and macroarray. J. Exp. Bot. 59, 3661-3674 https://doi.org/10.1093/jxb/ern214
  32. Zhao, J., Morozova, N., Williams, L., Libs, L., Avivi, Y., and Grafi, G. (2001). Two phases of chromatin decondensation of plant cells. J. Biol. Chem. 276, 22772-22778 https://doi.org/10.1074/jbc.M101756200

Cited by

  1. Recondensation level of repetitive sequences in the plant protoplast nucleus is limited by oxidative stress vol.61, pp.9, 2009, https://doi.org/10.1093/jxb/erq067
  2. Differential Histone Modification and Protein Expression Associated with Cell Wall Removal and Regeneration in Rice (Oryza sativa) vol.10, pp.2, 2011, https://doi.org/10.1021/pr100748e
  3. Quantification of DNA content in freshwater microalgae using flow cytometry: a modified protocol for selected green microalgae. vol.11, pp.2, 2009, https://doi.org/10.5507/fot.2011.030
  4. Transcriptome of Protoplasts Reprogrammed into Stem Cells in Physcomitrella patens vol.7, pp.4, 2012, https://doi.org/10.1371/journal.pone.0035961
  5. Unleashing the potential of the root hair cell as a single plant cell type model in root systems biology vol.4, pp.None, 2013, https://doi.org/10.3389/fpls.2013.00484
  6. Differences in oxidative stress, antioxidant systems, and microscopic analysis between regenerating callus-derived protoplasts and recalcitrant leaf mesophyll-derived protoplasts of Citrus reticulata vol.114, pp.2, 2009, https://doi.org/10.1007/s11240-013-0312-4
  7. Protoplasts: a useful research system for plant cell biology, especially dedifferentiation vol.250, pp.6, 2009, https://doi.org/10.1007/s00709-013-0513-z
  8. Identification of protoplast-isolation responsive microRNAs in Citrus reticulata Blanco by high-throughput sequencing vol.12, pp.8, 2009, https://doi.org/10.1371/journal.pone.0183524
  9. Evaluation of Methods to Assess in vivo Activity of Engineered Genome-Editing Nucleases in Protoplasts vol.10, pp.None, 2019, https://doi.org/10.3389/fpls.2019.00110
  10. A Streamlined Protocol for Wheat ( Triticum aestivum ) Protoplast Isolation and Transformation With CRISPR-Cas Ribonucleoprotein Complexes vol.11, pp.None, 2009, https://doi.org/10.3389/fpls.2020.00769
  11. From Single Cell to Plants: Mesophyll Protoplasts as a Versatile System for Investigating Plant Cell Reprogramming vol.21, pp.12, 2009, https://doi.org/10.3390/ijms21124195
  12. Characterization of a Non-flowering Cabbage Mutant Discovered 42 Years Ago vol.90, pp.4, 2021, https://doi.org/10.2503/hortj.utd-277