Journal of Molecular Evolution

, Volume 22, Issue 1, pp 1–19 | Cite as

Histone H4 and H2B genes in rainbow trout (Salmo gairdnerii)

  • Robert J. Winkfein
  • Wayne Connor
  • Jovita Mezquita
  • Gordon H. Dixon


The complete nucleotide sequence of the 3.0-kb BamH I-Sst I restriction fragment contained within the rainbow trout genomic clone λTH2 has been determined. This region contains the rainbow trout H4 and H2B histone genes and 5′ and 3′ flanking and spacer sequences, and represents the 5′ half of the histone-gene cluster; the remaining half has been characterized previously. The genes are uninterrupted, and are transcribed from the same strand. The protein sequence of H4, as determined from the nucleic acid sequence, is the same as that derived for other vertebrate H4 proteins, although comparison of nucleotide sequences shows a great deal of sequence divergence, especially in the third base position. The amino acid sequence of H2B, though largely homologous to those of other vertebrate H2B proteins, displays some characteristic differences in primary structure. Consensus sequences noted in many other eukaryotic genes, as well as histone-specific consensus sequences, have been identified. An unusual feature of the spacer region between the H4 and H2B genes is the presence of a duplicated sequence 87 bp in length. The 5′ and 3′ ends of each repeat are complementary, and each repeat contains smaller repeated sequences internally, as well as a possible cruciform structure.

Key words

Histone genes Histone H2B Histone H4 Gene organization Nucleotide sequence Rainbow trout 


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  1. Aiken JM, McKenzie DI, Zhao H-Z, States JC, Dixon GH (1983) Sequence homologies in the protamine gene family of rainbow trout. Nucleic Acids Res 11:4907–4922PubMedGoogle Scholar
  2. Bannon GA, Bowen JK, Yao M-C, Gorovsky MA (1984)Tetrahymena H4 genes: structure, evolution and organization in macro- and micronuclei. Nucleic Acids Res 12:1961–1975PubMedGoogle Scholar
  3. Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50:349–383PubMedGoogle Scholar
  4. Busslinger M, Portmann R, Irminger JC, Birnstiel ML (1980) Ubiquitous and gene-specific regulatory 5′ sequences in a sea urchin histone DNA clone coding for histone protein variants. Nucleic Acids Res 8:957–977PubMedGoogle Scholar
  5. Busslinger M, Rusconi S, Birnstiel ML (1982) An unusual evolutionary behavior of sea urchin histone gene cluster. EMBO 1:27–33Google Scholar
  6. Childs G, Maxson R, Cohn RH, Kedes L (1981) Orphons: dispersed genetic elements derived from tandem repetitive genes of eucaryotes. Cell 23:651–663PubMedGoogle Scholar
  7. Childs G, Nocente-McGrath C, Lieber T, Holt C, Knowles JA (1982) Sea urchin (Lytechinus pictus) late-stage histone H3 and H4 genes: characterization and mapping of a clustered but nontandemly linked multigene family. Cell 31:383–393PubMedGoogle Scholar
  8. Choe J, Kolodrubetz D, Grunstein M (1982) The two yeast histone H2A genes encode similar protein subtypes. Proc Natl Acad Sci USA 79:1484–1487PubMedGoogle Scholar
  9. 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
  10. Clewell DB, Helinski Dr (1972) Effect of growth conditions on the formation of the relaxation complex of supercoiled Col E1 deoxyribonucleic acid and protein inEscherichia coli. J Bacteriol 110:1135–1146PubMedGoogle Scholar
  11. Connor W, Mezquita J, Winkfein RJ, States JC, Dixon GH (1984a) Organization of the histone genes in the rainbow trout (Salmo gairdnerii). J Mol Evol 20:227–235PubMedGoogle Scholar
  12. Connor W, States JC, Mezquita J, Dixon GH (1984b) Organization and nucleotide sequence of rainbow trout histone H2A and H3 genes. J Mol Evol 20:236–250PubMedGoogle Scholar
  13. Dixon GH, Candido EPM, Honda BM, Louie AJ, Macleod AR, Sung MT (1975) The biological roles of post-synthetic modifications of nuclear proteins. Ciba Found Symp 28:229–258Google Scholar
  14. Engel JD, Sugarman BJ (1982) A chicken histone H3 gene contains intervening sequences. Nature 297:434–436PubMedGoogle Scholar
  15. Grandy DK, Engel JD, Dodgson JB (1982) Complete nucleotide sequence of a chicken H2B histone gene. J Biol Chem 257: 8577–8589PubMedGoogle Scholar
  16. Grosschedl R, Machler M, Rohrer U, Birnstiel ML (1983) A functional component of the sea urchin H2A gene modulator contains an extended sequence homology to a viral enhancer. Nucleic Acids Res 11:8123–8136PubMedGoogle Scholar
  17. Grunstein M, Hogness D (1975) Colony hybridization: a method for the isolation of cloned DNA's that contain a specific gene. Proc Natl Acad Sci USA 72:3961–3965PubMedGoogle Scholar
  18. Grunstein M, Diamond KE, Knoppel E, Grunstein JE (1981) Comparison of the early histone H4 gene sequence ofStrongylocentrotus purpuratus with maternal, early, and late histone H4 mRNA sequences. Biochemistry 20:1216–1223PubMedGoogle Scholar
  19. Harvey RP, Robins AJ, Wells JRE (1982) Independently evolving chicken histone H2B genes: identification of an ubiquitous H2B-specific 5′ element. Nucleic Acids Res 10:7851–7863PubMedGoogle Scholar
  20. Hentschel CC (1982) Homocopolymer sequences in the spacer of a sea urchin histone gene repeat are sensitive to S1 nuclease. Nature 295:714–716PubMedGoogle Scholar
  21. Hentschel CC, Birnstiel ML (1981) The organization and expression of histone gene families. Cell 25:301–313PubMedGoogle Scholar
  22. Holmes DS, Quigley M (1981) A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem 114:193–197PubMedGoogle Scholar
  23. Isenberg I (1979) Histones. Annu Rev Biochem 48:159–191PubMedGoogle Scholar
  24. Klug A, Rhodes D, Smith J, Finch JT, Thomas JO (1980) A low resolution structure for the histone core of the nucleosome. Nature 287:508–516Google Scholar
  25. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning—a laboratory manual. Cold Spring Harbor Laboratory, New YorkGoogle Scholar
  26. Maxam AM, Gilbert W (1980) Sequencing end-labelled DNA with base-specific chemical cleavages. Methods Enzymol 65:499–560PubMedGoogle Scholar
  27. Maxson R, Cohn R, Kedes L (1983) Expression and organization of histone genes. Annu Rev Genet 17:239–277PubMedGoogle Scholar
  28. McGhee JD, Felsenfeld G (1980) Nucleosome structure. Annu Rev Biochem 49:1115–1156PubMedGoogle Scholar
  29. Mezquita J, Connor W, Winkfein RJ, Dixon GH (1985) An H1 histone gene from rainbow trout (Salmo gairdnerii). J Mol Evol 21:209–219Google Scholar
  30. Moorman AFM, De Boer AJ, De Laaf RTM, Van Dongen WMAM, Destree OHJ (1981) Primary structure of the histone H3 and H4 genes and their flanking sequences in a minor histone gene cluster ofXenopus laevis. FEBS Lett 136:45–52PubMedGoogle Scholar
  31. Moorman AFM, De Boer PAJ, De Laaf RTM, Destree OHJ (1982) Primary structure of the histone H2A and H2B genes and their flanking sequences in a minor histone gene cluster ofXenopus laevis. FEBS Lett 144:235–241PubMedGoogle Scholar
  32. Pentecost BT, Wright JM, Dixon GH (1985) Isolation and sequence of cDNA clones coding for a member of the family of high mobility. Group proteins (HMG-T) in trout and analysis. Nucleic Acids Res (in press)Google Scholar
  33. Richmond TJ, Finch JT, Rushton B, Rhodes D, Klug A (1984) Structure of the nucleosome core particle at 7Å resolution. Nature 311:532–537PubMedGoogle Scholar
  34. 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 14:655–671PubMedGoogle Scholar
  35. Seiler-Tuyns A, Birnstiel ML (1981) Structure and expression in L-cells of a cloned H4 histone gene of the mouse. J Mol Biol 151:607–625PubMedGoogle Scholar
  36. Sittman DB, Graves RA, Marzluff WF (1983) Structure of a cluster of mouse histone genes. Nucleic Acids Res 11:6679–6697PubMedGoogle Scholar
  37. Smith MM, Andresson OS (1983) DNA sequences of yeast H3 and H4 histone genes from two non-allelic gene sets encode identical H3 and H4 proteins. J Mol Biol 169:663–690PubMedGoogle Scholar
  38. States JC, Connor W, Wosnick MA, Aiken JM, Gedamu L, Dixon GH (1982) Nucleotide sequence of a protamine component CII gene ofSalmo gairdnerii. Nucleic Acids Res 10:4551–4563PubMedGoogle Scholar
  39. Stephenson EC, Erba HP, Gall JG (1981) Characterization of a cloned histone gene cluster of the newtNotophthalmus viridescens. Nucleic Acids Res 9:2281–2295PubMedGoogle Scholar
  40. Sugarman BJ, Dodgson JB, Engel JD (1983) Genomic organization, DNA sequence, and expression of chicken embryonic histone genes. J Biol Chem 258:9005–9016PubMedGoogle Scholar
  41. 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 15:1033–1044PubMedGoogle Scholar
  42. Tabata T, Saski K, Iwabuchi M (1983) The structural organization and DNA sequence of a wheat histone H4 gene. Nucleic Acids Res 11:5865–5875PubMedGoogle Scholar
  43. von Holt C, Strickland WN, Brandt WF, Strickland MS (1979) More histone structures. FEBS Lett 100:201–218PubMedGoogle Scholar
  44. Wallis JW, Hereford L, Grunstein M (1980) Histone H2B genes of yeast encode two different proteins. Cell 22:799–805PubMedGoogle Scholar
  45. Wilhelm ML, Wilhelm F-X (1984) A transposon-like DNA fragment interrupts aPhysarum polycephalum histone H4 gene. FEBS Lett 168:249–254PubMedGoogle Scholar
  46. Woudt LP, Pastink A, Kempers-Veenstra AE, Jansen AEM, Mager WH, Planta RJ (1983) The genes coding for histone H3 and H4 inNeurospora crassa are unique and contain intervening sequences. Nucleic Acids Res 11:5347–5360PubMedGoogle Scholar
  47. Yamamoto KR, Alberts BM, Benzinger R, Lawhorne L, Treiber G (1970) Rapid bacteriophage sedimentation in the presence of polyethylene glycol and its application to large-scale virus purification. Virology 40:734–744PubMedGoogle Scholar
  48. Zhong R, Roeder RG, Heintz N (1983) The primary structure and expression of four cloned human histone genes. Nucleic Acids Res 11:7409–7425PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1985

Authors and Affiliations

  • Robert J. Winkfein
    • 1
  • Wayne Connor
    • 1
  • Jovita Mezquita
    • 1
  • Gordon H. Dixon
    • 1
  1. 1.Department of Medical Biochemistry, Health Sciences CentreUniversity of CalgaryCalgaryCanada

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