Skip to main content
SpringerLink
Log in

Genome size and chromatin condensation in vertebrates

  • Research Article
  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

Cell membrane-dependent chromatin condensation was studied by flow cytometry in erythrocytes of 36 species from six classes of vertebrates. A positive relationship was found between the degree of condensation and genome size. The distribution of variances among taxonomic levels is similar for both parameters. However, chromatin condensation varied relatively more at the lower taxonomic levels, which suggests that the degree of DNA packaging might serve for fine-tuning the ‘skeletal’ and/or ‘buffering’ function of noncoding DNA (although the range of this fine-tuning is smaller than the range of genome size changes). For two closely related amphibian species differing in genome size, change in chromatin condensation under the action of elevated extracellular salinity was investigated. Condensation was steadier and its reaction to changes in solvent composition was more inertial in the species with a larger genome, which is in agreement with the buffering function postulated for redundant DNA. The uppermost genome size in vertebrates (and in living beings in general) was updated using flow cytometry and was found to be about 80 pg (78,400 Mb). The widespread opinion that the largest genome occurs in unicellular organisms is rejected as being based on artifacts.

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

Fig. 1a,b
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Allison DC, Ridolpho PF, Rasch EM, Rasch RW, Johnson TS (1981) Increased accuracy of absorption cytophotometric DNA values by control of stain intensity. J Histochem Cytochem 29:1219–1228

    CAS  PubMed  Google Scholar 

  • Anatskaya OV, Vinogradov AE (2004) Heart and liver as developmental bottlenecks of mammal design: evidence from cell polyploidization. Biol J Linn Soc 83:175–186

    Article  Google Scholar 

  • Bachmann K (1970) Feulgen slope determinations of urodele nuclear DNA amounts. Histochemistry 22:289–293

    CAS  PubMed  Google Scholar 

  • Beaton MJ, Cavalier-Smith T (1999) Eukaryotic non-coding DNA is functional: evidence from the differential scaling of cryptomonad genomes. Proc R Soc Lond B 266:2053–2059

    Article  CAS  PubMed  Google Scholar 

  • Bennett MD (1971) The duration of meiosis. Proc R Soc Lond B 178:277–299

    CAS  Google Scholar 

  • Bennett MD (1987) Variation in genomic form in plants and its ecological implications. New Phytol 106(Suppl):177–200

    Google Scholar 

  • Bennett MD (1998) Plant genome values: how much do we know? Proc Natl Acad Sci U S A 95:2011–2016

    Google Scholar 

  • Bennett MD, Leitch IJ (2003) Plant DNA C-values database (release 2.0). Available at http://www.rbgkew.org.uk/cval/homepage.html

  • Bird AP (1995) Gene number, noise reduction and biological complexity. Trends Genet 11:94–100

    Article  CAS  PubMed  Google Scholar 

  • Brodsky VY, Uryvaeva IV (1985) Genome multiplication in growth and development. Cambridge University Press, Cambridge

    Google Scholar 

  • Byers TJ (1986) Molecular biology of DNA in Acanthamoeba, Amoeba, Entamoeba, and Naegleria. Int Rev Cytol 99:311–341

    CAS  PubMed  Google Scholar 

  • Castillo-Davis CI, Mekhedov SL, Hartl DL, Koonin EV, Kondrashov FA (2002) Selection for short introns in highly expressed genes. Nat Genet 31:415–418

    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

    CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1985) Cell volume and the evolution of eukaryote genome size. In: Cavalier-Smith T (ed) The evolution of genome size. Wiley, Chichester, pp 105–184

    Google Scholar 

  • Cavalier-Smith T, Beaton MJ (1999) The skeletal function of non-genic nuclear DNA: new evidence from ancient cell chimaeras. Genetica 106:3–13

    Article  CAS  PubMed  Google Scholar 

  • Comeron JM (2001) What controls the length of noncoding DNA? Curr Opin Genet Dev 11:652–659

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg E, Levanon EY (2003) Human housekeeping genes are compact. Trends Genet 19:362–365

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Gregory TR (2001) Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol Rev Camb Philos Soc 76:65–101

    Article  CAS  PubMed  Google Scholar 

  • Gregory TR (2002a) A bird’s-eye view of the C-value enigma: genome size, cell size, and metabolic rate in the class Aves. Evolution 56:121–130

    CAS  PubMed  Google Scholar 

  • Gregory TR (2002b) Genome size and developmental complexity. Genetica 115:131–146

    Article  PubMed  Google Scholar 

  • Grime JP, Mowforth MA (1982) Variation in genome size—an ecological interpretation. Nature 299:151–153

    Article  Google Scholar 

  • Grime JP, Shacklock JML, Band SR (1985) Nuclear DNA contents, shoot phenology and species co-existence in a limestone grassland community. New Phytol 100:435–445

    CAS  Google Scholar 

  • Hartl DL (2000) Molecular melodies in high and low C. Nat Rev Genet 1:145–149

    Google Scholar 

  • Hoffman J, Katz U (1997) Salt and water balance in the toad Bufo viridis during recovery from two different osmotically stressful conditions. Comp Biochem Physiol A 117:147–154

    Article  Google Scholar 

  • Hurst LD (1995) Evolutionary genetics. The silence of the genes. Curr Biol 5:459–461

    Article  CAS  PubMed  Google Scholar 

  • James J (1972) DNA constancy and chromatin structure in some cell nuclei of Amphiuma. Histochem J 4:181–192

    CAS  PubMed  Google Scholar 

  • Kalney VS, Kudryavtsev BN, Kudryavtseva MV (1974) Relation between radiosensitivity and DNA content in nuclei of various Amoeba proteus strains. Acta Protozool 12:111–116

    Google Scholar 

  • Kato H, Harada M, Tsuchiya K, Moriwaki K (1980) Absence of correlation between DNA repair in ultraviolet irradiated mammalian cells and life span of the donor species. Jpn J Genet 55:99–108

    Google Scholar 

  • Kim C, Rubin CM, Schmid CW (2001) Genome-wide chromatin remodeling modulates the Alu heat shock response. Gene 276:127–133

    Article  CAS  PubMed  Google Scholar 

  • Kinsman EA, Lewis C, Davies MS, Young JE, Francis D, Vilhar B, Ougham HJ (1997) Elevated CO2 stimulates cells to divide in grass meristems: a differential effect in two natural populations of Dactylis glomerata. Plant Cell Environ 20:1309–1316

    Article  Google Scholar 

  • Kozlowski J, Konarzewski M, Gawelczyk AT (2003) Cell size as a link between noncoding DNA and metabolic rate scaling. Proc Natl Acad Sci U S A 100:14080–14085

    Google Scholar 

  • Li TH, Kim C, Rubin CM, Schmid CW (2000) K562 cells implicate increased chromatin accessibility in Alu transcriptional activation. Nucleic Acids Res 28:3031–3039

    Article  CAS  PubMed  Google Scholar 

  • Licht LE, Lowcock LA (1991) Genome size and metabolic rate in salamanders. Comp Biochem Physiol B 100:83–92

    Article  Google Scholar 

  • Loborg H, Rundquist I (1997) DNA binding fluorochromes as probes for histone H1–chromatin interactions in situ. Cytometry 28:212–219

    Article  CAS  PubMed  Google Scholar 

  • Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404

    Article  CAS  PubMed  Google Scholar 

  • Macgillivray CW, Grime JP (1995) Genome size predicts frost resistance in British herbaceous plants: implications for rates of vegetation response to global warming. Funct Ecol 9:320–325

    Google Scholar 

  • Martins EP (2001) COMPARE, v. 4.4. Computer programs for the statistical analysis of comparative data. Available at: http://compare.bio.indiana.edu/. Department of Biology, Indiana University, Bloomington, Ind

  • McAdams HH, Arkin A (1999) It’s a noisy business! Genetic regulation at the nanomolar scale. Trends Genet 15:65–69

    Article  CAS  PubMed  Google Scholar 

  • Mommsen TP (2001) Paradigms of growth in fish. Comp Biochem Physiol B Biochem Mol Biol 129:207–219

    Article  CAS  PubMed  Google Scholar 

  • Moore PD (1985) Nuclear DNA content as a guide to plant growth rate. Nature 318:412–413

    Google Scholar 

  • Ohno S (1999) Gene duplication and the uniqueness of vertebrate genomes circa 1970–1999. Semin Cell Dev Biol 10:517–522

    CAS  PubMed  Google Scholar 

  • Olmo E (1983) Nucleotype and cell size in vertebrates: a review. Basic Appl Histochem 27:227–254

    CAS  PubMed  Google Scholar 

  • Olmo E (2003) Reptiles: a group of transition in the evolution of genome size and of the nucleotypic effect. Cytogenet Genome Res 101:166–171

    Article  CAS  PubMed  Google Scholar 

  • Pedersen RA (1971) DNA content, ribosomal gene multiplicity, and cell size in fish. J Exp Zool 177:65–79

    CAS  PubMed  Google Scholar 

  • Petrov DA (2001) Evolution of genome size: new approaches to an old problem. Trends Genet 17:23–28

    Article  CAS  PubMed  Google Scholar 

  • Petrov DA (2002) Mutational equilibrium model of genome size evolution. Theor Popul Biol 61:531–544

    Article  PubMed  Google Scholar 

  • Rock J, Eldridge M, Champion A, Johnston P, Joss J (1996) Karyotype and nuclear DNA content of the Australian lungfish, Neoceratodus forsteri (Ceratodidae: Dipnoi). Cytogenet Cell Genet 73:187–189

    CAS  PubMed  Google Scholar 

  • Shpun S, Hoffman J, Katz U (1992) Anuran amphibia which are not acclimable to high salt, tolerate high plasma urea. Comp Biochem Physiol A 103:473–477

    Article  CAS  Google Scholar 

  • Spear BB, Prescott DM (1980) Nuclear DNA in normal and refed Amoeba proteus. Exp Cell Res 130:387–392

    CAS  PubMed  Google Scholar 

  • Sternberg R (2002) On the roles of repetitive DNA elements in the context of a unified genomic–epigenetic system. Ann NY Acad Sci 981: 154–188

    PubMed  Google Scholar 

  • Szarski H (1983) Cell size and the concept of wasteful and frugal evolutionary strategies. J Theor Biol 105:201–209

    CAS  PubMed  Google Scholar 

  • Tautvydas KJ (1971) Mass isolated ameba nuclei. I. Isolation procedure and determination of macromolecular composition and RNA polymerase activity. Exp Cell Res 68:299–308

    CAS  PubMed  Google Scholar 

  • Thastrom A, Lowary PT, Widom J (2004) Measurement of histone–DNA interaction free energy in nucleosomes. Methods 33:33–44

    Article  CAS  PubMed  Google Scholar 

  • Trivers R, Burt A, Palestis BG (2004) B chromosomes and genome size in flowering plants. Genome 47:1–8

    Article  PubMed  Google Scholar 

  • Urrutia AO, Hurst LD (2003) The signature of selection mediated by expression on human genes. Genome Res 13:2260–2264

    Google Scholar 

  • Van’t Hof J, Sparrow AH (1963) A relationship between DNA content, nuclear volume and minimum mitotic cycle time. Proc Natl Acad Sci U S A 49:897–902

    CAS  PubMed  Google Scholar 

  • Vervoort A (1980) Tetraploidy in Protopterus (Dipnoi). Experientia 36:294–296

    Google Scholar 

  • Vinogradov AE (1995a) Nucleotypic effect in homeotherms: body mass-corrected basal metabolic rate of mammals is related to genome size. Evolution 49:1249–1259

    Google Scholar 

  • Vinogradov AE (1995b) Cell membrane-dependent chromatin condensation. Cytometry 19:183–188

    CAS  PubMed  Google Scholar 

  • Vinogradov AE (1996) Post-fixation method of cell viability assessment with flow cytometry. Acta Histochem Cytochem 29(Suppl):527–528

    Google Scholar 

  • Vinogradov AE (1997) Nucleotypic effect in homeotherms: body mass-independent resting metabolic rate of passerine birds is related to genome size. Evolution 51:220–225

    Google Scholar 

  • Vinogradov AE (1998a) Buffering: a possible passive-homeostasis role for redundant DNA. J Theor Biol 193:197–199

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov AE (1998b) Genome size and GC-percent in vertebrates as determined by flow cytometry: the triangular relationship. Cytometry 31:100–109

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov AE (2000) Larger genomes for molluskan land pioneers. Genome 43:211–212

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov AE (2003) Selfish DNA is maladaptive: evidence from the plant Red List. Trends Genet 19:609–614

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov AE (2004a) Evolution of genome size: multi-level selection, mutation bias or dynamical chaos? Curr Opin Genet Dev 14:620–626

    Google Scholar 

  • Vinogradov AE (2004b) Genome size and extinction risk in vertebrates. Proc R Soc Lond B 271:1701–1705

    Article  PubMed  Google Scholar 

  • Vinogradov AE (2004c) Compactness of human housekeeping genes: selection for economy or genomic design? Trends Genet 20:248–253

    Article  CAS  PubMed  Google Scholar 

  • Vinogradov AE, Anatskaya OV (2004) Phenological resonance and quantum life-history. J Theor Biol 228:417–420

    Article  PubMed  Google Scholar 

  • Wakamiya I, Newton RJ, Johnston JS, Price HJ (1993) Genome size and environmental factors in the genus Pinus. Am J Bot 80:1235–1241

    Google Scholar 

  • Wakamiya I, Price HJ, Messina MG, Newton RJ (1996) Pine genome size diversity and water relations. Physiol Plantarum 96:13–20

    Article  CAS  Google Scholar 

  • Waltari E, Edwards SV (2002) Evolutionary dynamics of intron size, genome size, and physiological correlates in archosaurs. Am Nat 160:539–552

    Article  Google Scholar 

  • Zuckerkandl E (2002) Why so many noncoding nucleotides? The eukaryote genome as an epigenetic machine. Genetica 115:105–129

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Russian Foundation for Basic Research (RFBR) and by the Programme of the Presidium of the Russian Academy of Sciences ‘Molecular and Cellular Biology’ (MCB RAS).

Author information

Authors and Affiliations

  1. Institute of Cytology, Russian Academy of Sciences, Tikhoretsky Ave. 4, St. Petersburg, 194064, Russia

    Alexander E. Vinogradov

Authors
  1. Alexander E. Vinogradov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander E. Vinogradov.

Additional information

Communicated by E.A. Nigg

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vinogradov, A.E. Genome size and chromatin condensation in vertebrates. Chromosoma 113, 362–369 (2005). https://doi.org/10.1007/s00412-004-0323-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00412-004-0323-3

Keywords

Search

Navigation