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. 1987 Dec 23;15(24):10569–10582. doi: 10.1093/nar/15.24.10569

Evolution of late H2A, H2B, and H4 histone genes of the sea urchin, Strongylocentrotus purpuratus.

R Maxson 1, T Mohun 1, G Gormezano 1, L Kedes 1
PMCID: PMC339963  PMID: 3697096

Abstract

Sea urchins possess several distinct sets of histone genes, including "early" genes, maximally active in cleavage and blastula stages, and "late" genes, active from the late blastula stage onwards. We determined the nucleotide sequences of six sea urchin (Strongylocentrotus purpuratus) late histone genes located on four genomic segments. Comparative analysis of these sequences identified several conserved elements in 5' flanking regions, including the sequences ATGPyATANTATA shared by all late genes and GGCGGGAAATTGAAAA shared by two late H4s. Comparisons of protein-coding sequences of late H4 and H2B genes with their early counterparts showed that silent sites have diverged to the theoretical maximum, indicating that early and late histone gene classes diverged at least 200 million years ago. Since extant echinoderms evolved from a common ancestor at about that time, it is likely that early and late histone gene sets are characteristic of all echinoderm groups. Amino acid sequences derived from nucleotide sequences of late H2A and H2B gistone genes differ substantially from amino acid sequences of their late counterparts. Most such differences are in highly mutable positions. A few, however, occur in positions that do not mutate frequently and thus may reflect functional differences between the early and late forms of the H2A and H2B proteins.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ares M., Jr, Mangin M., Weiner A. M. Orientation-dependent transcriptional activator upstream of a human U2 snRNA gene. Mol Cell Biol. 1985 Jul;5(7):1560–1570. doi: 10.1128/mcb.5.7.1560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bergman Y., Rice D., Grosschedl R., Baltimore D. Two regulatory elements for immunoglobulin kappa light chain gene expression. Proc Natl Acad Sci U S A. 1984 Nov;81(22):7041–7045. doi: 10.1073/pnas.81.22.7041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Biggin M. D., Gibson T. J., Hong G. F. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963–3965. doi: 10.1073/pnas.80.13.3963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Birnstiel M. L., Busslinger M., Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985 Jun;41(2):349–359. doi: 10.1016/s0092-8674(85)80007-6. [DOI] [PubMed] [Google Scholar]
  5. Busslinger M., Barberis A. Synthesis of sperm and late histone cDNAs of the sea urchin with a primer complementary to the conserved 3' terminal palindrome: evidence for tissue-specific and more general histone gene variants. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5676–5680. doi: 10.1073/pnas.82.17.5676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Busslinger M., Rusconi S., Birnstiel M. L. An unusual evolutionary behaviour of a sea urchin histone gene cluster. EMBO J. 1982;1(1):27–33. doi: 10.1002/j.1460-2075.1982.tb01119.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Childs G., Maxson R., Kedes L. H. Histone gene expression during sea urchin embryogenesis: isolation and characterization of early and late messenger RNAs of Strongylocentrotus purpuratus by gene-specific hybridization and template activity. Dev Biol. 1979 Nov;73(1):153–173. doi: 10.1016/0012-1606(79)90144-1. [DOI] [PubMed] [Google Scholar]
  8. Childs G., Nocente-McGrath C., Lieber T., Holt C., Knowles J. A. Sea urchin (lytechinus pictus) late-stage histone H3 and H4 genes: characterization and mapping of a clustered but nontandemly linked multigene family. Cell. 1982 Dec;31(2 Pt 1):383–393. doi: 10.1016/0092-8674(82)90132-5. [DOI] [PubMed] [Google Scholar]
  9. Ephrussi A., Church G. M., Tonegawa S., Gilbert W. B lineage--specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science. 1985 Jan 11;227(4683):134–140. doi: 10.1126/science.3917574. [DOI] [PubMed] [Google Scholar]
  10. Falkner F. G., Zachau H. G. Correct transcription of an immunoglobulin kappa gene requires an upstream fragment containing conserved sequence elements. Nature. 1984 Jul 5;310(5972):71–74. doi: 10.1038/310071a0. [DOI] [PubMed] [Google Scholar]
  11. Harvey R. P., Robins A. J., Wells J. R. Independently evolving chicken histone H2B genes: identification of a ubiquitous H2B-specific 5' element. Nucleic Acids Res. 1982 Dec 11;10(23):7851–7863. doi: 10.1093/nar/10.23.7851. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Isenberg I. Histones. Annu Rev Biochem. 1979;48:159–191. doi: 10.1146/annurev.bi.48.070179.001111. [DOI] [PubMed] [Google Scholar]
  13. Kaumeyer J. F., Weinberg E. S. Sequence, organization and expression of late embryonic H3 and H4 histone genes from the sea urchin, Strongylocentrotus purpuratus. Nucleic Acids Res. 1986 Jun 11;14(11):4557–4576. doi: 10.1093/nar/14.11.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kedes L. H. Histone genes and histone messengers. Annu Rev Biochem. 1979;48:837–870. doi: 10.1146/annurev.bi.48.070179.004201. [DOI] [PubMed] [Google Scholar]
  15. Knowles J. A., Childs G. J. Temporal expression of late histone messenger RNA in the sea urchin Lytechinus pictus. Proc Natl Acad Sci U S A. 1984 Apr;81(8):2411–2415. doi: 10.1073/pnas.81.8.2411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Krol A., Lund E., Dahlberg J. E. The two embryonic U1 RNA genes of Xenopus laevis have both common and gene-specific transcription signals. EMBO J. 1985 Jun;4(6):1529–1535. doi: 10.1002/j.1460-2075.1985.tb03813.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lieber T., Weisser K., Childs G. Analysis of histone gene expression in adult tissues of the sea urchins Strongylocentrotus purpuratus and Lytechinus pictus: tissue-specific expression of sperm histone genes. Mol Cell Biol. 1986 Jul;6(7):2602–2612. doi: 10.1128/mcb.6.7.2602. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Mattaj I. W., Lienhard S., Jiricny J., De Robertis E. M. An enhancer-like sequence within the Xenopus U2 gene promoter facilitates the formation of stable transcription complexes. Nature. 1985 Jul 11;316(6024):163–167. doi: 10.1038/316163a0. [DOI] [PubMed] [Google Scholar]
  19. Maxam A. M., Gilbert W. A new method for sequencing DNA. Proc Natl Acad Sci U S A. 1977 Feb;74(2):560–564. doi: 10.1073/pnas.74.2.560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maxson R., Cohn R., Kedes L., Mohun T. Expression and organization of histone genes. Annu Rev Genet. 1983;17:239–277. doi: 10.1146/annurev.ge.17.120183.001323. [DOI] [PubMed] [Google Scholar]
  21. Maxson R., Mohun T., Gormezano G., Childs G., Kedes L. Distinct organizations and patterns of expression of early and late histone gene sets in the sea urchin. Nature. 1983 Jan 13;301(5896):120–125. doi: 10.1038/301120a0. [DOI] [PubMed] [Google Scholar]
  22. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  23. Mous J., Stunnenberg H., Georgiev O., Birnstiel M. L. Stimulation of sea urchin H2B histone gene transcription by a chromatin-associated protein fraction depends on gene sequences downstream of the transcription start site. Mol Cell Biol. 1985 Oct;5(10):2764–2769. doi: 10.1128/mcb.5.10.2764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Osley M. A., Gould J., Kim S., Kane M. Y., Hereford L. Identification of sequences in a yeast histone promoter involved in periodic transcription. Cell. 1986 May 23;45(4):537–544. doi: 10.1016/0092-8674(86)90285-0. [DOI] [PubMed] [Google Scholar]
  25. Overton G. C., Weinberg E. S. Length and sequence heterogeneity of the histone gene repeat unit of the sea urchin, S. purpuratus. Cell. 1978 Jun;14(2):247–257. doi: 10.1016/0092-8674(78)90111-3. [DOI] [PubMed] [Google Scholar]
  26. Parslow T. G., Blair D. L., Murphy W. J., Granner D. K. Structure of the 5' ends of immunoglobulin genes: a novel conserved sequence. Proc Natl Acad Sci U S A. 1984 May;81(9):2650–2654. doi: 10.1073/pnas.81.9.2650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Perler F., Efstratiadis A., Lomedico P., Gilbert W., Kolodner R., Dodgson J. The evolution of genes: the chicken preproinsulin gene. Cell. 1980 Jun;20(2):555–566. doi: 10.1016/0092-8674(80)90641-8. [DOI] [PubMed] [Google Scholar]
  28. Roberts S. B., Weisser K. E., Childs G. Sequence comparisons of non-allelic late histone genes and their early stage counterparts. Evidence for gene conversion within the sea urchin late stage gene family. J Mol Biol. 1984 Apr 25;174(4):647–662. doi: 10.1016/0022-2836(84)90088-3. [DOI] [PubMed] [Google Scholar]
  29. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Smith H. O., Birnstiel M. L. A simple method for DNA restriction site mapping. Nucleic Acids Res. 1976 Sep;3(9):2387–2398. doi: 10.1093/nar/3.9.2387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smith M. M., Andrésson O. S. DNA sequences of yeast H3 and H4 histone genes from two non-allelic gene sets encode identical H3 and H4 proteins. J Mol Biol. 1983 Sep 25;169(3):663–690. doi: 10.1016/s0022-2836(83)80164-8. [DOI] [PubMed] [Google Scholar]
  32. Sures I., Lowry J., Kedes L. H. The DNA sequence of sea urchin (S. purpuratus) H2A, H2B and H3 histone coding and spacer regions. Cell. 1978 Nov;15(3):1033–1044. doi: 10.1016/0092-8674(78)90287-8. [DOI] [PubMed] [Google Scholar]

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