Summary
A common polymorphism of the early embryonic histone-gene repeat ofStrongylocentrotus purpuratus is a 195-bp insertion within the H4-H2B spacer. The sequence, found as an insert in histone-gene repeats of 6 of 22 individuals screened, is also found at approximately 50 sites elsewhere in the genome of every individual. We compare the sequences of the histone-gene spacers that do and do not contain the insert. The insert is found not to have transposon-like features, and no sequence in the original spacer has been duplicated to flank the insert. There is, however, a hexanucleotide sequence that is repeated three times at one end of the insert, and the element has inserted between direct repeats of 5 bp that were present in the original spacer. One of the copies found outside the histone gene cluster was cloned and sequenced and is compared with the insert. Again, no transposon-like features are evident. Regions flanking the homologous sequence in this clone were used as hybridization probes in whole-genome blots. Results indicate that the 195-bp sequence insert is itself embedded within a larger element that is repeated within the genome. Therefore, only a portion of a larger repetitive sequence has integrated into the histone-gene spacer. The sequence features of the insert, although not typical of mobile elements, may be representative of other illegitimate recombination events.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Anderson DM, Scheller RH, Posakony JW, McAllister L, Trabert SG, Beall C, Britten RJ, Davidson EH (1981) Repetitive sequences of the sea urchin genome. J Mol Biol 145:5–28
Birnboim D (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 1:1513–1523
Britten RJ, Cetta A, Davidson EH (1978) The single copy DNA sequence polymorphism of the sea urchinStrongylocentrotus purpuratus. Cell 15:1175–1186
Busslinger M, Rusconi S, Birnstiel ML (1982) An unusual evolutionary behavior of a sea urchin histone gene cluster. EMBO J 1:27–33
Cappello J, Cohen SM, Lodish HF (1984)Dictyostelium transposable element DIRS-1 preferentially inserts into DIRS-1 sequences. Mol Cell Biol 4:2207–2213
Childs G, Maxson R, Cohn RH, Kedes L (1981) Orphons: dispersed genetic elements derived from tandem repetitive genes of eucaryotes. Cell 23:651–663
Childs G, Nocente-McGrath C, Lieber T, Holt C, Knowles J (1982) Sea urchin (Lytechinus pictus) late stage histone H3 and H4 genes: characterization and mapping of a clustered but nontandemly linked multigene family. Cell 31:383–393
Cohen JB, Hoffman-Liebermann B, Kedes L (1985a) Structure and unusual characteristics of a new family of transposable elements in the sea urchinStrongylocentrotus purpuratus. Mol Cell Biol 5:2804–2813
Cohen JB, Hoffman D, Kedes L (1985b) Tsp transposons: a heterogeneous family of mobile sequences in the genome of the sea urchinStrongylocentrotus purpuratus. Mol Cell Biol 5:2814–2825
Fedoroff NV (1983) Controlling elements in maize. In: Shapiro JA (ed) Mobile genetic elements. Academic Press, New York, pp 1–63
Grula JW, Hall TJ, Hunt JA, Giugni TD, Graham GJ, Davidson EH, Britten RJ (1982) Sea urchin DNA sequence variation and reduced interspecies differences of the less variable DNA sequences. Evolution 36:665–676
Hess JF, Fox M, Schmid C, Shen C-KJ (1983) Molecular evolution of the human adult α-globin-like gene region: insertion and deletion of Alu family repeats and non-Alu DNA sequences. Proc Natl Acad Sci USA 80:5970–5974
Hoffman-Liebermann B, Liebermann D, Kedes LH, Cohen SN (1985) TU elements: a heterogeneous family of modularly structured eucaryotic transposons. Mol Cell Biol 5:991–1001
Houck CM, Rinehart FP, Schmid CW (1978) Fractionation of renatured repetitive human DNA according to thermal stability, sequence length and renaturation rate. Biochim Biophys Acta 518:37–52
Houck CM, Rinehart FP, Schmid CW (1979) A ubiquitous family of repeated DNA sequences in the human genome. J Mol Biol 132:289–306
Jelinek WR, Schmid CW (1982) Repetitive sequences in eukarytoic DNA and their expression. Annu Rev Biochem 51:813–844
Johnson SA, Davidson EH, Britten RJ (1984) Insertion of a short repetitive sequence (D881) in a sea urchin gene: a typical interspersed repeat? J Mol Evol 20:195–201
Joseph DR, Stafford DW (1976) Purification of sea urchin ribosomal RNA genes with a single-strand specific nuclease. Biochim Biophys Acta 418:167–174
Kafatos FC, Jones CW, Efstratiadis A (1979) Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res 7:1541–1552
Kaumeyer JF, Weinberg ES (1986) Sequence and organization of late embryonic H3 and H4 histone genes from the sea urchin,Strongylocentrotus purpuratus. Nucleic Acids Res 14:4557–4576
Liebermann D, Hoffman-Liebermann B, Weinthal J, Childs G, Maxson R, Mauron A, Cohen SN, Kedes L (1983) An unusual transposon with long terminal inverted repeats in the sea urchinStrongylocentrotus purpuratus. Nature 306:342–347
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York
Maxam AH, Gilbert W (1980) Sequencing end labeled DNA with base-specific chemical cleavages. Methods Enzymol 65:499–560
Maxson R, Mohun T, Gormezano G, Childs G, Kedes L (1983) Distinct organizations and patterns of expression of early and late histone gene sets in the sea urchin. Nature 301:120–125
Messing J (1983) New M13 vectors for cloning. Methods Enzymol 101:20–78
Moore GF, Scheller RH, Davidson EH, Britten RJ (1978) Evolutionary change in the repetition frequency of sea urchin sequences. Cell 15:649–660
Moore GF, Pearson WR, Davidson EH, Britten RJ (1981) Long and short repeats of the sea urchin DNA and their evolution. Chromosoma 84:19–32
Murphy E, Loefdahl S (1984) Transposition of Tn 554 does not generate a target duplication. Nature 307:292–294
Overton C, Weinberg ES (1978) Length and sequence heterogeneity of the histone gene repeat unit of the sea urchin,S. purpuratus. Cell 14:247–257
Paro R, Goldberg ML, Gehring WJ (1983) Molecular analysis of large transposable elements carrying the white locus ofDrosophila melanogaster. EMBO J 2:853–860
Poole SJ, Firtel RA (1984) Genomic instability and mobile genetic elements in regions surrounding two discoidin genes ofDictyostelium discoideum. Mol Cell Biol 4:671–680
Posakony JW, Flytzanis CN, Britten RJ, Davidson EH (1983) Interspersed sequence organization and developmental representation of cloned poly(A) RNAs from sea urchin eggs. J Mol Biol 167:361–389
Potter S, Truett M, Phillips M, Maher A (1980) Eukaryotic transposable genetic elements with inverted terminal repeats. Cell 20:639–647
Pustell J, Kafatos FC (1982a) A convenient and adaptable package of DNA sequence analysis programs for microcomputers. Nucleic Acids Res 10:51–59
Pustell J, Kafatos FC (1982b) A high speed, high capacity homology matrix: zooming through SV40 and polyoma. Nucleic Acids Res 10:4765–4782
Rigby PWJ, Dieckmann M, Rhodes C, Berg P (1977) Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol 113:237–251
Rinehart FP, Ritch TG, Deininger PL, Schmid CW (1981) Renaturation rate studies of a single family of interspersed repeated sequences in human deoxyribonucleic acid. Biochemistry 20:3003–3010
Roberts SB, Weisser KE, Childs G (1984) 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 174:647–662
Roeder GS, Fink GR (1983) Transposable elements in yeast. In: Shapiro JA (ed) Mobile genetic elements. Academic Press, New York, pp 299–328
Rubin GM (1983) Dispersed repetitive DNAs inDrosophila. In: Shapiro JA (ed) Mobile genetic elements. Academic Pres, New York, pp 329–361
Schnabel H, Palm A, Dick K, Gramps B (1984) Sequence analysis of the insertion element ISH 1.8 and of associated structural changes in the genome of phage ϕH of the archaebacteriumHalobacterium halobium. EMBO J 3:1717–1722
Sharp PA (1983) Conversion of RNA to DNA in mammals: Alu-like elements and pseudogenes. Nature 301:471–472
Shott-Akhurst RJ, Calzone FJ, Britten RJ, Davidson EH (1984) Isolation and characterization of a cell lineage-specific cytoskeletal actin gene family ofStrongylocentrotus purpuratus. In: Davidson EH, Firtel RA (eds). Molecular biology of development. Alan R Liss, New York, pp 119–128
Southern EM (1975) Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98:503–517
Stafford DW, Bieber D (1975) Concentration of DNA solutions by extraction with 2-butanol. Biochim Biophys Acta 378:18–21
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 15:1033–1044
Truett MA, Jones RS, Potter SS (1981) Unusual structure of the FB family of transposable elements inDrosophila. Cell 24:753–762
Yager LN, Kaumeyer JF, Weinberg ES (1984) Evolving sea urchin histone genes-nucleotide polymorphisms in the H4 gene spacers ofStrongylocentrotus purpuratus. J Mol Evol 20:215–226
Zucker C, Cappello J, Lodish HF, George P, Chung S (1984)Dictyostelium transposable element DIRS-I has 350-basepair inverted terminal repeats that contain a heat shock promoter. Proc Natl Acad Sci USA 81:2660–2664
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Yager, L.N., Kaumeyer, J.F., Lee, I. et al. Insertion of an intermediate repetitive sequence into a sea urchin histone-gene spacer. J Mol Evol 24, 346–356 (1987). https://doi.org/10.1007/BF02134133
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF02134133