Abstract
The Paternal-Sex-Ratio (PSR) chromosome of Nasonia vitripennis contains several families of repetitive DNAs that show significant sequence divergence but share two palindromic regions. This study reports on the analysis of junctions between two of these repetitive DNA families (psr2 and psr18). Three lambda clones that hybridized to both repeat families were isolated from PSR-genomic DNA libraries through multiple screenings and analyzed by Southern blots. Analysis of clones showed a region in which the two repeat types are interspersed, flanked by uniform blocks of each repeat type. PCR amplification of genomic DNA confirmed the contiguous arrangement of psr2 and psr18 on PSR and identified an additional junction region between these repeats that was not present in the lambda inserts. We isolated and sequenced 41 clones from the lambda inserts and genomic PCR products containing junction sequences. Sequence analysis showed that all transitions between psr2 and psr18 repeats occurred near one of the two palindromes. Based on the inheritance pattern of PSR, recombination between repeats on this chromosome must be mitotic (rather than meiotic) in origin. The occurrence of exchanges near the palindromes suggests that these sequences enhance recombination between repeat units. Rapid amplification of repetitive DNA may have been an important factor in the evolution of the PSR chromosome.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Abastado J-P, Darche F, Godeau B, Cami B, Kourilsky P (1987) Intramolecular recombination between partially homologous sequences in Eschericia coli and Xenopus laevis oocytes. Proc Natl Acad Sci USA 84:6496–6500
Anderson RP, Roth J (1978) Tandem chromosomal duplications in Salmonella typhimurium: fusion of histidine genes to novel promoters. J Mol Biol 119:147–166
Arnheim N, Kuehn M (1979) The genetic behavior of a cloned mouse ribosomal DNA segment mimics ribosomal gene evolution. J Mol Biol 134:743–763
Beukeboom LW (1992) Genetics and population biology of the paternal sex ratio (PSR) chromosome. PhD thesis, University of Rochester, Rochester, NY
Beukeboom LW, Reed KM, Werren JH (1992) Effects of deletions on mitotic stability of the Paternal-Sex-Ratio (PSR) chromosome from Nasonia. Chromosoma 102:20–26
Beukeboom LW, Werren JH (1993) Deletion analysis of the parasitic paternal-sex-ratio (PSR) chromosome from Nasonia vitripennis. Genetics 133:637–648
Bigot Y, Hamelin M-H, Periquet G (1990) Heterochromatin condensation and evolution of unique satellite-DNA families in two parasitic was species: Diadromus pulchellus and Eupelmus vuilleti (Hymenoptera). Mol Biol Evol 7:351–364
Breeuwer JAJ (1992) Postzygotic reproductive isolation in the genus Nasonia (Hymenoptera, Pteromalidae): the role of cytoplasmic microorganisms and other heritable cytoplasmic factors. PhD thesis, University of Rochester, Rochester, NY
Breeuwer JAJ, Werren JH (1990) Microorganisms associated with chromosome destruction and reproductive isolation between two insect species. Nature 346:558–560
Britten RJ, Kohne DE (1986) Repeated sequences in DNA. Science 161:529–540
Brown FL, Musich PR, Maio JJ (1979) The repetitive sequence structure of component alpha DNA and its relationship to the nucleosomes of African green monkey. J Mol Biol 131:777–799
Cabot EL, Beckenbach AT (1989) Simultaneous editing of multiple nucleic acid and protein sequences using ESEE. Comp Appl Biosci 5:233–234
Cabot EL, Doshi P, Wu M-L, Wu C-I (1993) Population genetics of tandem repeats in centromeric heterochromatin: evidence for unequal crossovers at the Responder locus of Drosophila melanogaster. Genetics 135:477–487
Chalker AF, Okeley EA, Davison A, Leach DRF (1993) The effects of central asymmetry on the propagation of palindromic DNA in bacteriophage λ are consistent with cruciform extrusion in vivo. Genetics 133:143–148
Cohen SN, Kopecko DJ (1976) Structural evolution of bacterial plasmids: role of translocating genetic elements and DNA sequence insertions. Fed Proc 35:2031–2036
Collins M, Rubin GM (1983) High frequency precise excision of the Drosophila foldback transposable element. Nature 303:259–260
Dod B, Mottez E, Desmarais E, Bonhomme F, Roizés G (1989) Concerted evolution of light satellite DNA in genus Mus implies amplification and homogenization of large blocks of repeats. Mol Biol Evol 6:478–491
Doyle GG (1978) A general theory of chromosome pairing based on the palindromic DNA model of Sobell with modifications and amplifications. J Theor Biol 70:171–184
Eickbush DG, Eickbush TH, Werren JH (1992) Molecular characterization of repetitive DNA sequences from a B chromosome. Chromosoma 101:575–583
Ekker M, Andreas F, Westerfield M (1992) Identification of two families of satellite-like repetitive DNA sequences from zebra fish (Brachydanio rerio). Genomics 13:1169–1173
Gilson E, Perrin D, Clement J-M, Szmelcman S, Dassa E, Hofnung M (1986) Palindromic units from E. coli as binding sites for a chromoid-associated protein. FEBS 206:323–328
Gretarsdottir S, Amason U (1992) Evolution of the common cetacean highly repetitive DNA component and the systematic position of Orcaella brevirostris. J Mol Evol 34:201–208
Henthorn PS, Mager DL, Huisman THJ, Smithies O (1986) A gene deletion ending within a complex array of repeated sequences 3′ to the human β-globin gene cluster. Proc Natl Acad Sci USA 83: 5194–5198
Higgins CF, McLaren RS, Newbury SF (1988) Repetitive extragenic palindromic sequences, mRNA stability and gene expression: evolution by gene conversion? Gene 72:3–14
Hyrien O, Debatisse M, Buttin G, de Saint Vincent BR (1987) A hotspot for normal amplification joints in a mosaic of Alu-like repeats and palindromic A+T-rich DNA. EMBO J 6:2401–2408
Innis MA, Gelfand DH, Sninsky JJ, White TJ (1990) PCR protocols: a guide to methods and applications. Academic Press, San Diego, CA
Israelewski N (1983) Structure and function of an AT-rich, interspersed repetitive sequence from Chironomus thummi solenoid DNA, 142bp palindrome-frame and homologies with the sequence for site-specific recombination of bacterial transposons. Nucleic Acids Res 11:6985–6996
Kiyama R, Okumura K, Matsui H, Bruns GAP, Kanda N, Oishi M (1987) Nature of recombination involved in excision and rearrangements of human repetitive DNA. J Mol Biol 198:589–598
Kubota S, Kuro-o M, Mizuno S, Kohno S (1993) Germ line-restricted, highly repeated DNA sequences and their chromosomal localization in a Japanese hagfish (Eptatretus okinoseanus). Chromosoma 102:163–173
Krawinkel V, Zoebelein G, Bothwell ALM (1986) Palindromic sequences are associated with sites of DNA breakage during gene conversion. Nucleic Acids Res 14:3871–3882
Levis R, Rubin GM (1982) The unstable WDZL mutation of Drosophila is caused by a 13 kilobase insertion that is precisely excised in phenotypic revertants. Cell 30:543–550
Lobe AR, Brutlag M (1987) Adjacent satellite DNA segments in Drosophila: structure of junctions. J Mol Biol 194:171–179
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
Metzenberg AB, Wurzer G, Huisman THJ, Smithies O (1991) Homology requirements for unequal crossing over in humans. Genetics 128:143–161
Musich PR, Brown FL, Maio JJ (1977) Mammalian repetitive DNA and the subunit structure of chromatin. Cold Spring Harbor Symp Quant Biol 42:1147–1160
Nur U, Werren JH, Eickbush D, Burke W, Eickbush T (1988) A “selfish” B chromosome that enhances its transmission by eliminating the paternal chromosomes. Science 240:512–514
Ohno S (1990) Grammatical analysis of DNA sequences provides a rationale for the regulatory control of an entire chromosome. Genet Res, Cambridge 56:115–120
Rasch EM, Cassidy JD, King RC (dy1975) Estimates of genome size in haploid-diploid species of parasitoid wasps. Abstr Histochem Soc, p 317
Richmond TJ, Finch JT, Rushton B, Rhodes D, Klug A (1984) Structure of the nucleosome core particle at 7Å resolution. Nature 311: 532–537
Rojas-Rousse D, Bigot Y, Periquet G (1993) DNA insertions as a component of the evolution of unique satellite DNA families in two genera of parasitoid wasps; Diadromus and Eupelmus (Hymenoptera). Mol Biol Evol 10:383–396
Ryan SL, Saul GB (1968) Post-fertilization effect of incompatibility factors in Mormoniella. Mol Gen Genet 103:29–36
Sawadogo M, Van Dyke MW (1991) A rapid method for the purification of deprotected oligodeoxynucleotides. Nucleic Acids Res 19:674
Shmookler Reis RJ, Srivastava A, Beranek DT, Goldstein S (1985) Human alphoid family of tandemly repeated DNA. Sequence of cloned tetrameric fragments and analysis of familial divergence. J Mol Biol 186:31–41
Smith GP (1976) Evolution of repeated DNA sequences by unequal crossover. Science 191:528–535
Sobell HM (1972) Molecular mechanism for genetic recombination. Proc Natl Acad Sci USA 69:2483–2487
Southern EM (1975) Long range periodicities in mouse satellite DNA. J Mol Biol 94:51–69
Stephan W (1989) Tandem-repetitive noncoding DNA: forms and forces. Mol Biol Evol 6:198–212
Sutton WD, McCallum M (1972) Related satellite DNAs in the genus Mus. J Mol Biol 71:633–656
Trinh TQ, Sinden RR (1993) The influence of primary and secondary DNA structure in deletion and duplication between direct repeats in Escherichia coli. Genetics 134:409–422
Vogel JM, Nieto MC, Fischer A, Goodenow RS (1990) Overlapping palindromic sequences associated with somatic deletion and meiotic recombination of MHC class I genes. Mol Immunol 27:875–886
Waldman AS, Liskay RM (1987) Differential effects of base-pair mismatch on intrachromosomal versus extrachromosomal recombination in mouse cells. Proc Natl Acad Sci USA 84:5340–5344
Walker PBM (1971) Origin of satellite DNA. Nature 229:306–308
Walsch JB (1987) Persistence of tandem arrays: implications for satellite and simple-sequence DNAs. Genetics 115:553–567
Warren GJ, Green RL (1985) Comparison of physical and genetic properties of palindromic DNA sequences. J Bacteriol 161:1103–1111
Werren JH (1990) The paternal-sex-ratio chromosome of Nasonia. Am Nat 137:392–402
Werren JH, Nur U, Eickbush D (1987) An extrachromosomal factor causing loss of paternal chromosomes. Nature 327:75–76
Werren JH, Nur U, Wu C-I (1988) Selfish genetic elements. Trends Ecol Evol 3:297–302
Wevrick R, Willard VP, Willard HF (1992) Structure of DNA near long tandem arrays of alpha satellite DNA at the centromere of human chromosome 7. Genomics 14:912–923
Willard HF, Waye JS (1987) Hierarchical order in chromosome-specific human alpha satellite DNA. Trends Genet 3:192–198
Author information
Authors and Affiliations
Additional information
Correspondence to: John H. Werren
Rights and permissions
About this article
Cite this article
Reed, K.M., Beukeboom, L.W., Eickbush, D.G. et al. Junctions between repetitive DNAs on the PSR chromosome of Nasonia vitripennis: Association of palindromes with recombination. J Mol Evol 38, 352–362 (1994). https://doi.org/10.1007/BF00163152
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00163152