Journal of Molecular Evolution

, Volume 25, Issue 1, pp 29–36 | Cite as

Organization and unusual expression of histone genes in the sea starPisaster ochraceus

  • A. M. Howell
  • D. Cool
  • J. Hewitt
  • B. Ydenberg
  • M. J. Smith
  • B. M. Honda


The organization and maternal expression of histone genes differ greatly between the two echinoderm classes represented by the sea stars and sea urchins. We have isolated and characterized a 5.3-kb genomic DNA fragment encoding core histone genes in the sea starPisaster ochraceus. The majority of histone genes are organized as tandem repeats of the 5.3-kb fragment, which is present in as many as 700 copies per haploid genome. The identity, precise location, and transcriptional polarity of individual core histone genes within the repeat were determined by DNA sequence analyses. The gene order in the sea star (H2B, H2A, H4, H3) is different from that in sea urchins (H2B, H3, H2A, H4). What is remarkable is the low level of maternal histone mRNA inP. ochraceus eggs relative to that in sea urchins. This observation supports a recent suggestion that major changes in mode of gene expression, rather than in gene organization or copy number, can be correlated with major events in echinoderm evolution.

Key words

Histone genes Echinoderms Maternal mRNA Development Evolution 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Benton WD, Davis RW (1977) Screening λgt recombinant clones by hybridization to single plaques in situ. Science 196:180–182PubMedGoogle Scholar
  2. Blin N, Stafford DW (1976) A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 3:2303–2308PubMedGoogle Scholar
  3. Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL, Boyer HW (1977) Construction and characterization of new cloning vehicles. Gene 2:95–113CrossRefPubMedGoogle Scholar
  4. Britten RJ, Graham DE, Neufeld BR (1974) Analysis of repeating DNA sequences by reassociation. Methods Enzymol 29E:363–418Google Scholar
  5. Childs G, Maxson R, Kedes L (1977) Histone gene expression during sea urchin embryogenesis: isolation and characterization of early and late messenger RNAs ofStrongylocentrotus purpuratus by gene specific hybridization and template activity. Dev Biol 73:153–178Google Scholar
  6. Clerc RG, Bucher P, Strub K, Birnstiel ML (1983) Transcription of a clonedXenopus laevis H4 histone gene in the homologous frog oocyte system depends on an evolutionary conserved sequence motif in the-50 region. Nucleic Acids Res 11:8641–8657PubMedGoogle Scholar
  7. Cohn RH, Kedes L (1979) Nonallelic histone gene clusters of individual sea urchin (Lytechinus pictus): polarity and gene organization. Cell 18:843–853CrossRefPubMedGoogle Scholar
  8. Cool D (1983) Evolution of a specific cloned repeat DNA sequence in sea stars. MSc thesis, Simon Fraser University, Burnaby, British Columbia, CanadaGoogle Scholar
  9. Crain WR Jr, Durica DS, Van Doren K (1981) Actin gene expression in developing sea urchin embryos. Mol Cell Biol 1:711–720PubMedGoogle Scholar
  10. Davis RW, Botstein D, Roth JR (1980) A manual for genetic engineering: advanced bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  11. Deeley RG, Gordon JI, Burns ATH, Mullinix KP, Binastein M, Goldberger RF (1977) Primary activation of the vitellogenin gene in the rooster. J Biol Chem 252:8310–8319PubMedGoogle Scholar
  12. Fraser A, Gomez J, Hartwick EB, Smith MJ (1981) Observations on the reproduction and development ofPisaster ochraceus (Brandt). Can J Zool 59:1700–1707Google Scholar
  13. Glisin V, Crkvenjakov R, Byus C (1974) Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry 13:2633–2637CrossRefPubMedGoogle Scholar
  14. Grunstein M, Diamond KE, Knoppel E, Grunstein JE (1981) Comparison of the early histone H4 gene sequence ofS. purpuratus with maternal, early and late H4 mRNA sequences. Biochemistry 20:1216–1223CrossRefPubMedGoogle Scholar
  15. Hanly SM, Bleecker GC, Heintz N (1985) Identification of promoter elements necessary for transcriptional regulation of a human histone H4 gene in vitro. Mol Cell Biol 5:380–389PubMedGoogle Scholar
  16. Harvey RP, Robins AJ, Wells JRE (1982) Independently evolving chicken H2B genes: identification of a ubiquitous H2B specific 5′ element. Nucleic Acids Res 10:7851–7863PubMedGoogle Scholar
  17. Hentschel CC, Birnstiel ML (1981) The organization and expression of histone gene families. Cell 25:301–313CrossRefPubMedGoogle Scholar
  18. Isenberg I (1979) Histones. Annu Rev Biochem 48:159–191CrossRefPubMedGoogle Scholar
  19. Kedes L (1979) Histone genes and histone messages. Annu Rev Biochem 48:837–870CrossRefPubMedGoogle Scholar
  20. Kovesdi I (1985) Molecular studies of gene expression in development of the sea starPisaster ochraceus (Brandt). PhD thesis, Simon Fraser University, Burnaby, British Columbia, CanadaGoogle Scholar
  21. Kovesdi I, Smith MJ (1982) Sequence complexity in the maternal RNA of the starfishPisaster ochraceus (Brandt). Dev Biol 89:56–63CrossRefPubMedGoogle Scholar
  22. Kovesdi I, Smith MJ (1985) Quantitative assessment of action transcripts in eggs, embryos and tube feet of the sea star,P. ochraceus. Mol Cell Biol 5:3001–3008PubMedGoogle Scholar
  23. Kovesdi I, Preugschat F, Stuerzl M, Smith MJ (1984) Genomic and cDNA clones of actin genes from the sea starPisaster ochraceus. Biochim Biophys Acta 782:76–86PubMedGoogle Scholar
  24. Laskey RA, Mills AD (1977) Enhanced radiographic detection of32P and125I using intensifying screens and hypersensitized films. FEBS Lett 82:314–316CrossRefPubMedGoogle Scholar
  25. Lehrach H, Diamond D, Wozney JM, Boedtker H (1977) RNA molecular weight determinations by gel electrophoresis under denaturing conditions: a critical examination. Biochemistry 16:4743–4751CrossRefPubMedGoogle Scholar
  26. Maniatis T, Hardison RC, Lacy E, Lauer J, O'Connell C, Quon D, Kim GK, Efstratiadis A (1978) The isolation of structural genes from libraries of eukaryotic DNA. Cell 15:687–701CrossRefPubMedGoogle Scholar
  27. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New YorkGoogle Scholar
  28. Mauron A, Kedes L, Hough-Evans BR, Davidson EH (1982) Accumulation of individual histone mRNAs during embryogenesis of the sea urchinStrongylocentrotus purpuratus. Dev Biol 94:425–434CrossRefPubMedGoogle Scholar
  29. Maxam AM, Gilbert W (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol 65:499–560PubMedGoogle Scholar
  30. Maxson RE, Wilt T (1982) Accumulation of the early histone messenger RNA during the development ofStrongylocentrotus purpuratus. Dev Biol 94:435–450CrossRefPubMedGoogle Scholar
  31. McDonnell MW, Simon MN, Studier FW (1977) Analysis of restriction fragments of T7 DNA and determination of molecular weight by electrophoresis in neutral and alkaline gels. J Mol Biol 110:119–146PubMedGoogle Scholar
  32. McMaster GK, Carmichael GG (1977) Analysis of single and double-stranded nucleic acids on polyacrylamide and agarose gels by using glyoxal and acridine orange. Proc Natl Acad Sci USA 74:4835–4838PubMedGoogle Scholar
  33. Messing J, Vieira J (1982) A new pair of M13 vectors for selecting either strand of double-digest restriction fragments. Gene 19:269–276CrossRefPubMedGoogle Scholar
  34. Newrock KM, Cohen LH, Hendricks MB, Donnelly RJ, Weinberg ES (1978) Stage-specific mRNAs coding for subtypes of H2A and H2B histones in the sea urchin embryo. Cell 14:327–336CrossRefPubMedGoogle Scholar
  35. Old RW, Woodland HR (1984) Histone genes: not so simple after all. Cell 38:624–626CrossRefPubMedGoogle Scholar
  36. Paul CRC (1977) Evolution of primitive echinoderms. In: Hallam A (ed) Patterns of evolution illustrated by the fossil record. Elsevier, Amsterdam, pp 123–158Google Scholar
  37. Pearson W, Davidson EH, Britten RJ (1977) Program for least squares analyses of reassociation and hybridization data. Nucleic Acids Res 4:1727–1737PubMedGoogle Scholar
  38. Perry M, Thomsen GH, Roeder RG (1985) Genomic organization and sequence of two distinct histone gene clusters fromX. laevis. J Mol Biol 185:479–499CrossRefPubMedGoogle Scholar
  39. Raff R, Kaufman TC (1983) Embryos, genes, and evolution: the developmental-genetic basis of evolutionary change. Macmillan, New YorkGoogle Scholar
  40. Raff RA, Anstrom JA, Huffman CJ, Leaf DS, Loo J-H., Showman RM, Wells DE (1984) Origin of a gene regulatory mechanism in the evolution of echinoderms. Nature 310:312–314PubMedGoogle Scholar
  41. Rigby PW, Dieckman M, Rhodes C, Berg P (1977) Labelling DNA to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol 113:237–251CrossRefPubMedGoogle Scholar
  42. Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467PubMedGoogle Scholar
  43. Schaffner W, Kunz G, Daetwyler H, Telford J, Smith HO, Birnstiel ML (1978) Genes and spacers of cloned sea urchin histone DNA analyzed by sequencing. Cell 14:655–671CrossRefPubMedGoogle Scholar
  44. Shott RJ, Lee JJ, Britten RJ, Davidson EH (1984) Differential expression of the actin gene family ofStrongylocentrotus purpuratus. Dev Biol 101:295–306CrossRefPubMedGoogle Scholar
  45. Smith MJ, Nicholson R, Stuerzl M, Lui A (1982) Single copy DNA homology in sea stars. J Mol Evol 18:92–101CrossRefPubMedGoogle Scholar
  46. Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517PubMedGoogle Scholar
  47. Sugarman BJ, Dodgson J, Engel JD (1983) Genomic organization, DNA sequence and expression of chicken embryonic histone genes. J Biol Chem 258:9005–9016PubMedGoogle Scholar
  48. Sures I, Lowry J, Kedes LH (1978) The DNA sequence of sea urchin (S. purpuratus) H2A, H2B and H3 histone coding and spacer regions. Cell 15:1033–1044CrossRefPubMedGoogle Scholar
  49. Thayer RE (1979) An improved method for detecting foreig DNA in plasmids ofE. coli. Anal Biochem 98:60–63CrossRefPubMedGoogle Scholar
  50. Thomas PS (1980) Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci USA 77:5201–5205PubMedGoogle Scholar
  51. Zernik M, Heintz N, Boime I, Roeder RG (1980)Xenopus laevis histone genes: Variant H1 genes are present in different clusters. Cell 22:807–815CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1987

Authors and Affiliations

  • A. M. Howell
    • 1
  • D. Cool
    • 1
  • J. Hewitt
    • 1
  • B. Ydenberg
    • 1
  • M. J. Smith
    • 1
  • B. M. Honda
    • 1
  1. 1.Department of Biological SciencesSimon Fraser UniversityBurnabyCanada

Personalised recommendations