Skip to main content
Log in

Physiological aspects of genome variability in tissue culture. II. Growth phase-dependent quantitative variability of repetitive BstNI fragments of primary cultures of Daucus carota L.

  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Systematic investigations on the occurrence of differential DNA replication in carrot cultures, expressed at the total genome level, were performed. The genome of Daucus carota L. could be characterized by a pattern of repetitive BstNI fragments that was independent of tissue specificity or cultivar differences. Characterization of the genomic DNA of the secondary phloem of carrot roots, in comparison to the DNA of the induced primary cultures at different growth phases, revealed dramatic differences in the copy number of the repetitive fragments. Highly proliferative tissue showed extensive reduction in the proportion of repetitive sequences in the genome in all of the 37 investigated variants. In contrast, during subsequent transition to stationary growth the repetitive fragments re-amplified. The results suggest that the quantitative genome organisation was involved in the regulation of the growth potential of cells. A hypothesis is discussed suggesting a determining influence of the observed differential DNA replication on cell-cycle rates and the cell program of proliferative tissue by structural and positioning effects on DNA loops. To study the causality of somaclonal variation, research on the relationship between physiological genome variability and the induction of heritable changes is recommended.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams RLP (1990) DNA methylation. Biochem J 265:309–320

    Google Scholar 

  • Allen GC, Hall GE Jr., Childs LC, Weissinger AK, Spiker S, Thompson WF (1993) Scaffold attachment regions increase reporter gene expression in stably transformed plant cells. Plant Cell 5:603–613

    Google Scholar 

  • Altamura MM, Bassi P, Cavallini A, Cionini G, Cremonini R, Monacelli B, Pasqua G, Sassoli O, Tran Than Van K, Cionini PG (1987) Nuclear DNA changes during plant development and the morphogenetic response in vitro of Nicotiana tabacum tissues. Plant Sci 53:73–79

    Article  Google Scholar 

  • Arnholdt-Schmitt B (1993a) Rapid changes in amplification and methylation pattern of genomic DNA in cultured carrot root explants (Daucus carota L.). Theor Appl Genet 85:793–800

    Google Scholar 

  • Arnholdt-Schmitt B (1993b) Hormonsensitivität und genomische DNS-Variabilität in ihrem Bezug zur Ertragsbildung bei Daucus carota L. ssp. sativus. Ein Beitrag zur Zellbiologie pflanzlichen Wachstums. Habilitationsschrift, Giessen

  • Arnholdt-Schmitt B, Holzapfel B, Schillinger A, Neumann KH (1991) Variable methylation and differential replication of genomic DNA in cultured carrot root explants during growth induction as influenced by hormonal treatments. Theor Appl Genet 82:283–288

    Google Scholar 

  • Arnholdt-Schmitt B, Herterich S, Neumann K-H (1995) Physiological aspects of genome variability in tissue culture. I: Growth phase-dependent differential DNA methylation of the carrot genome (Daucus carota L.) during primary culture. Theor Appl Genet 91:809–815

    Google Scholar 

  • Bassi P, Cionini PG, Cremonini R, Seghizzi P (1984) Underrepresentation of nuclear DNA sequences in differentiating root cells of Vicia faba. Protoplasma 123:70–77

    Google Scholar 

  • Blumenthal AB, Kriegstein HJ, Hogness DS (1974) The units of DNA replication in Drosophila melanogaster chromosomes. Cold Spring Harbor Symp Quant Biol 38:205–223

    Google Scholar 

  • Bonifer C, Vidai M, Grosveld F, Sippel AE (1990) Tissue-specific and position-independent expression of the complete gene domain for chicken lysozyme in transgenic mice. EMBO J 9: 2843–2848

    Google Scholar 

  • Bonifer C, Hecht A, Saueressig H, Winter DM, Sippel AE (1991) Dynamic chromatin: the regulatory domain organization of eukaryotic gene loci. J Cell Biochem 47:99–108

    Google Scholar 

  • Bouchard RA (1982) Moderately repetitive DNA in evolution. Int Rev Cytol 76:113–193

    Google Scholar 

  • Cavalier-Smith T (1978) Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox. J Cell Sci 34:247–278

    Google Scholar 

  • Cullis CA (1987) The generation of somatic and heritable variation in response to stress. Am Nat 130:S62-S73

    Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603

    CAS  PubMed  Google Scholar 

  • Dührssen E (1983) Untersuchungen zur Charakterisierung der DNS einiger höherer Pflanzen (Reassoziationskinetiken, Interspezieshybridisierungen, Dichtegradienten-zentrifugationen). Dissertation, Giessen

  • Dührssen E, Neumann KH (1980) Characterization of satellite-DNA of Daucus carota L.. Z Pflanzenphysiol 100:447–454

    Google Scholar 

  • Dührssen E, Saavedra E, Neumann KH (1980) DNA reassociation kinetics and hybridization in different angiosperms. Plant Syst Evol 136:267–273

    Google Scholar 

  • Elder JK, Southern EM (1983) Measurement of DNA length by ge electrophoresis II: comparison of methods for relating mobility to fragment length. Anal Biochem 128:227–231

    Google Scholar 

  • Flavell R (1980) The molecular characterization and organisation of plant chromosomal DNA sequences. Annu Rev Plant Physiol 31:569–96

    Article  CAS  Google Scholar 

  • Flavell RB, Bennett MD, Smith IB, Smith DB (1974) Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem Genet 12:257–269

    Google Scholar 

  • Francis D, Kidd AD, Bennett MD (1985) DNA replication in relation to DNA C values. In: Bryant JA, Francis D (eds) The cell division cycle in plants. Cambridge University Press, pp 61–82

  • Fujimura T, Komamine A (1982) Molecular aspects of somatic embryogenesis in a synchronous system. In: Fujiwara (ed) Proc 5th Int Cong Plant Tissue and Cell Cult, Tokyo, pp 105–106

  • Gartenbach-Scharrer U, Habib S, Neumann KH (1990) Sequential synthesis of some proteins in cultured carrot explant (Daucus carota) cells during callus induction. Plant Cell, Tissue and Organ Cult. 22:27–35

    Google Scholar 

  • Hall G, Allen GC, Loer DS, Thompson WF (1991) Nuclear scaffolds and scaffold-attachment regions in higher plants. Proc Natl Acad Sci USA 88:9320–9324

    Google Scholar 

  • Harley CB, Reis RJS, Goldstein S (1982) Loss of repetitious DNA in proliferating somatic cells may be due to unequal recombination. J Theor Biol 94:1–12

    Google Scholar 

  • Havelange A, Jeanny JC (1984) Changes in density of chromatin in the meristematic cells of Sinapis alba during transition to flowering. Protoplasma 122:222–232

    Google Scholar 

  • Houssa C, Jacqmard A, Bernier G (1990) Activation of replicon origins as a possible target for cytokinins in shoot meristems of Sinapis. Planta 181:324–326

    Google Scholar 

  • Jacqmard A, Houssa C (1988) DNA fiber replication during a morphogenetic switch in the shoot meristematic cells of a higher plant. Exp Cell Res 179:454–461

    Google Scholar 

  • Jenns SM, Bryant JA (1978) Correlation between deoxyribonuclease activity and DNA replication in the embryonic axes of germinating peas (Pisum sativum L.). Planta 138:99–103

    Google Scholar 

  • Kuhrová V, Bezdek M, Vyskot B, Koukalová B, Fajkus J (1991) Isolation and characterization of two middle repetitive DNA sequences of nuclear tobacco genome. Theor Appl Genet 81: 740–744

    Google Scholar 

  • Larkin PJ, Scowcroft WR (1981) Somaclonal variation — a novel source of variability from cell culture for plant improvement. Theor Appl Genet 60:197–214

    Google Scholar 

  • Leeton PRJ, Smyth DR (1993) An abundant LINE-like element amplified in the genome of Lilium speciosum. Mol Gen Genet 237:97–104

    Google Scholar 

  • Liu YG, Ikeda TM, Tsunewaki K (1992) Moderately repeated, dispersed, and highly variable (MRDHV) genomic sequences of common wheat usable for cultivar identification. Theor Appl Genet 84:535–543

    Google Scholar 

  • Ludérus MEE, Graaf A, Mattia E, Blaauwen JL, Grande MA, Jong L, Driel R (1992) Binding of matrix attachment regions to lamin B1. Cell 70:949–959

    Google Scholar 

  • Matousek J, Rakousky S, Nemcova B (1987) Occurrence of sugar non-specific nuclease in tobacco callus: changes of nuclease activity during callus growth and plant regeneration. Plant Cell, Tissue Organ Cult 8:61–71

    Google Scholar 

  • Mellerowicz EJ, Riding RT, Little CHA (1992) Periodicity of cambial activity in Abies balsamea. II. Effects of temperature and photoperiod on the size of the nuclear genome in fusiform cambial cells. Physiol Plant 85:526–530

    Google Scholar 

  • Mitra J, Mapes MO, Steward FC (1960) Growth and organized development of cultured cells. IV. The behavior of the nucleus. Am J Bot 47:357–368

    Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high-molecular-weight plant DNA. Nucleic Acids Res 8:4321–4325

    CAS  PubMed  Google Scholar 

  • Nagl W (1976) Zellkern und Zellzyklen. Ulmer, Stuttgart

  • Nagl W (1979) Differential DNA replication in plants: a critical re-view. Z Pflanzenphysiol 95:283–314

    Google Scholar 

  • Nagl W (1987) Replication. Progr Bot 49:181–191

    Google Scholar 

  • Nagl W (1989) Replication. Prog Bot 51:173–180

    Google Scholar 

  • Nagl W (1990) Gene amplification and related events. Biotechnol agric for 11:15.3–201

    Google Scholar 

  • Nagl W (1992) Replication. Prog Bot 53:166–180

    Google Scholar 

  • Nagl W, Jeanjour M, Kling H, Kühner S, Michels I, Müller T, Stein B (1983) Genome and chromatin organisation in higher plants. Biol. Zentralbl 102:129–148

    Google Scholar 

  • Natali L, Cavallini A, Cremonini R, Bassi P, Cionini PG (1986) Amplification of nuclear DNA sequences during induced plant cell de-differentiation. Cell Differ 18:157–161

    Google Scholar 

  • Neumann KH (1962) Untersuchungen über den Einfluß essentieller Schwermetalle auf das Wachstum und den Proteinstoffwechsel von Karottengewebekulturen. Dissertation, Giessen

  • Neumann KH (1966) Wurzelbildung und Nucleinsäuregehalt bei Phloem-Gewebekulturen der Karottenwurzel auf synthetischem Nährmedium verschiedener Hormonkombinationen. Phytohormones et l'Organogenèse 38:95–102

    Google Scholar 

  • Neumann KH (1968) Über Beziehungen zwischen hormonal gesteuerter Zellteilungsgeschwindigkeit und Differenzierung. Ein Beitrag zur Physiologie der pflanzlichen Ertragsbildung. Habilitationsschrift, Giessen

  • Neumann KH (1972) Untersuchungen über den Einfluß des Kinetins und des Eisens auf den Nukleinsäure- und Protein-Stoffwechsel von Karottengewebekulturen. Z Pflanzenernaehr Bodenkd 131: 211–220

    Google Scholar 

  • Neumann KH, Pertzsch C, Moos M, Krömmelbein G (1978) Untersuchungen zur Charakterisierung des Ernährungssystems von Karottengewebekulturen: Photosynthese, Kohlenstoff- und Stickstoff-ernährung, Mineralstoffverbrauch. Z Pflanzenernaehr Bodenkd 141:299–311

    Google Scholar 

  • Nuti Ronchi V, Bennici A, Martini G (1973) Nuclear fragmentation in de-differentiating cells of Nicotiana glauca pith tissue grown in vitro. Cell Differ 2:77–85

    Google Scholar 

  • Olszewska MJ, Maszewski J, Bilecka A (1990) DNA replication in relation to S phase duration in six angiosperm annual species. Cytologia 55:31–35

    Google Scholar 

  • Opstelten RJ, Clement JME, Wanka F (1989) Direct repeats at nuclear matrix-associated DNA regions and their putative control function in the replicating eukaryotic genome. Chromosoma 98:422–427

    Google Scholar 

  • Orgel LE, Crick HC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607

    CAS  PubMed  Google Scholar 

  • Peschke VM, Phillips RL (1992) Genetic implications of somaclonal variation in plants. Adv Genet 30:41–75

    Google Scholar 

  • Power JB, Davey MR, Freeman JP, Mulligan BJ, Cocking EC (1986) Fusion and transformation of plant protoplasts. Methods Enzymol 118:578–595

    Google Scholar 

  • Richards GM (1974) Modification of the diphenylamine reaction giving increased sensitivity and simplicity in the estimation of DNA.Anal Biochem 57:369–376

    Google Scholar 

  • Rogowsky PM, Manning S., Liu JY, Langridge P (1991) The R173 family of rye-specific repetitive DNA sequences: a structural analysis. Genome 34:88–95

    Google Scholar 

  • Rudnicki K, Rzepecki R, Szopa J (1988) Rearrangement of the nuclease-inhibitor complex components within cells of white bush treated with phytohormones. J Plant Physiol 132:658–663

    Google Scholar 

  • Schäfer A (1976) Untersuchungen zur Charakterisierung der DNS von Daucus carota L. Dissertation, Giessen

  • Solano R, Hueros G, Fominaya A, Ferrer E (1992) Organization of repeated sequences in species of the genus Avena. Theor Appl Genet 83:602–607

    Google Scholar 

  • Southern EM (1979) Measurement of DNA length by gel electrophoresis. Anal Biochem 100:319–323

    Google Scholar 

  • Steward FC, Caplin SM, Millar FK (1952) Investigations on growth and metabolism of plant cells. I. New techniques for the investigation of metabolism, nutrition and growth in undifferentiated cells. Ann Bot 16(1):57–77

    Google Scholar 

  • Steward FC, Mapes MO, Kent AE, Hosten RD (1964) Growth and development of cultured plant cells. Science 143:20–27

    Google Scholar 

  • Stief AD, Winter M, Strätling WH, Sippel AE (1989) A nuclear element mediates elevated and position-independent gene activity. Nature 341:343–345

    Google Scholar 

  • Szopa J, Wagner KG (1980) Purification and properties of a DNase inhibitor from Nicotiana tabacum cell cultures. Eur J Biochem 111:211–215

    Google Scholar 

  • Van Driel R, Humbel B, de Jong L (1991) The nucleus: a black box being opened. J Cell Biochem 47:311–316

    Google Scholar 

  • Van't Hof J (1985) Control points within the cell cycle. In: Bryant JA, Francis D (eds): The cell-division cycle in plants. Cambridge University Press, pp 1–13

  • Waterborg JH, Shall S (1985) The organisation of replicons. In: Bryant JA, Francis D (eds): The cell-division cycle in plants. Cambridge University Press, pp 15–35

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by H. R Linskens

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arnholdt-Schmitt, B. Physiological aspects of genome variability in tissue culture. II. Growth phase-dependent quantitative variability of repetitive BstNI fragments of primary cultures of Daucus carota L.. Theoret. Appl. Genetics 91, 816–823 (1995). https://doi.org/10.1007/BF00220965

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00220965

Key words

Navigation