Repeated DNA elements have been extensively applied as physical chromosome markers in comparative studies for the identification of chromosomal rearrangements, the identification of sex chromosomes, chromosome evolution analysis and applied genetics. Here, we report the characterization of the transposable elements (TE) Tc1, Rex1, Rex3 and Rex6 and a new element called RCk in the genome of the South American cichlid fish Cichla kelberi using nucleotide sequence analysis and hybridization to metaphase chromosomes. The analysis of the repeated elements demonstrated that they are, in most cases, compartmentalized in heterochromatic regions, as has been observed in several other vertebrates. On the other hand, the elements Rex1 and Rex3 were also observed spanning extensive euchromatic regions on 2 chromosome pairs. The RCk element exhibits a wide distribution among fishes and also in amphibians, and it was spread throughout the chromosomes of C. kelberi. Our results have demonstrated that the compartmentalization of repeated elements is not restricted to heterochromatic segments, which has provided new concepts with regard to the genomic organization of transposons.

Keywords:
Chromosome evolution, Cichlidae, Cytogenetics, Evolution, Genome, Heterochromatin, Transposons
1.
Accioly IV, Molina WF: Cytogenetic studies in Brazilian marine Sciaenidae and Sparidae fishes (Perciformes). Genet Mol Res 7:358–370 (2008).
2.
Alkan C, Ventura M, Archidiacono N, Rocchi M, Sahinalp SC, et al: Organization and evolution of primate centromeric DNA from whole-genome shotgun sequence data. PLoS Comput Biol 3:181 (2007).
3.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 215:403–410 (1990).
4.
Anderson P, Emmons SW, Moerman DG: Discovery of Tc1 in the nematode Caenorhabditis elegans, in Fedoroff N, Botstein D (eds): The Dynamic Genome, pp 319–333 (Cold Spring Harbor Laboratory Press, Cold Spring Harbor 1992).
5.
Avancini RMP, Walden KKO, Robertson HM: The genomes of most animals have multiple members of the Tc1 family of transposable elements. Genetica 98:131–140 (1996).
6.
Bertollo LAC, Takahashi CS, Moreira-Filho O: Cytotaxonomic consideration on Hoplias lacerdae (Pisces, Erythrinidae). Braz J Genet 1:103–120 (1978).
7.
Brenner S, Elgar G, Sandford R, Macrae A, Venkatesh B, Aparício S: Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome. Nature 366:265–268 (1993).
8.
Brezinsky L, Wang GVL, Humphreys T, Hunt J: The transposable element Uhu from Hawaiian Drosophila – member of the widely dispersed class of Tc1-like transposons. Nucleic Acids Res 18:2053–2059 (1990).
9.
Brinn MNA, Porto JIR, Feldeberg E: Karyological evidence for interspecific hybridization between Cichla monoculus and C. temensis (Perciformes, Cichlidae) in the Amazon. Hereditas 141:252–257 (2004).
10.
Busseau I, Chaboissier MC, Pélisson A, Bucheton A: I factors in Drosophila melanogaster: transposition under control. Genetica 93:101–116 (1994).
11.
Capriglione T, Odierna G, Caputo V, Canapa A, Olmo E: Characterization of a Tc1-like transposon in the Antarctic ice-fish, Chionodraco hamatus. Gene 295:193–198 (2002).
12.
Cavalier-Smith T: The Evolution of Genome Size (Wiley, New York 1985).
13.
Charlesworth B, Langley CH: The population genetics of Drosophila transposable elements. Annu Rev Genet 23:251–287 (1989).
14.
DaSilva C, Hadji H, Ozouf-Costaz C, Nicaud S, Jaillon O, et al: Remarkable compartmentalization of transposable elements and pseudogenes in the heterochromatin of the Tetraodon nigroviridis genome. Proc Natl Acad Sci USA 99:13636–13641 (2002).
15.
Dawe RK: RNA interference, transposons, and the centromere. Plant Cell 15:297–301 (2003).
16.
Eickbush TH, Furano AV: Fruit flies and humans respond differently to retrotransposons. Curr Opin Genet Dev 12:669–674 (2002).
17.
Feldberg E, Porto JIR, Santos EBP, Valentim FCS: Cytogenetics studies of two freshwater sciaenids of the genus Plagioscion (Perciformes, Scianidae) from the Central Amazon. Genet Mol Biol 22:351–356 (1999).
18.
Feldberg E, Porto JIR, Bertollo LAC: Chromosomal changes and adaptation of cichlid fishes during evolution, in Val AL, Kappor BG (eds): Fish Adaptations, pp 285–308 (Science Publishers, New Dehli 2003).
19.
Ferreira IA, Martins C: Physical chromosome mapping of repetitive DNA sequences in Nile tilapia Oreochromis niloticus: Evidences for a differential distribution of repetitive elements in the sex chromosomes. Micron 39:411–418 (2008).
20.
Feschotte C, Pritham EJ: DNA transposons and the evolution of eukaryotic genomes. Ann Rev Genet 41:331–368 (2007).
21.
Feschotte C, Jiang N, Wessler SR: Plant transposable elements: Where genetics meets genomics. Nat Rev Genet 3:329–341 (2002).
22.
Grady DL, Ratliff RL, Robinson DL, McCanlies EC, Meyne J, Moyzis RK: Highly conserved repetitive DNA sequences are present at human centromeres. Proc Natl Acad Sci USA 89:1695–1699 (1992).
23.
Hall TA: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98 (1999).
24.
Hasegawa M, Kishino K, Yano T: Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174 (1985).
25.
Herrán De la R, Robles F, Navas JI, López-Flores I, Herrera M, et al: The centromeric satellite of the wedge sole (Dicologoglossa cuneata, Pleuronectiformes) is composed mainly of a sequence motif conserved in other vertebrate centromeric DNAs. Cytogenet Genome Res 121:271–276 (2008).
26.
Horvath JE, Bailey JA, Locke DP, Eichler EE: Lessons from the human genome: transitions between euchromatin and heterochromatin. Hum Mol Genet 10:2215–2223 (2001).
27.
Howell WM, Black DA: Controlled silver staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36:1014–1015 (1980).
28.
Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP: Bayesian inference of phylogeny and its impact on evolutionary biology. Science 294:2310–2314 (2001).
29.
Ivics Z, Izsvak Z, Minter A, Hackett PB: Identification of functional domains and evolution of Tc1-like transposable elements. Proc Natl Acad Sci USA 93:5008–5013 (1996).
30.
Kimura M: A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 (1980).
31.
Komiya H, Takemura S: Nucleotide sequence of 5S ribosomal RNA from rainbow trout (Salmo gairdnerii) liver. J Biochem 86:1067–1080 (1979).
32.
Kullander SO, Ferreira EJG: A review of the South American cichlid genus Cichla, with descriptions of nine new species (Teleostei: Cichlidae). Ichth Expl Fresh 17:289–398 (2006).
33.
Leaver MJ: A family of Tc1-like transposons from the genomes of fishes and frogs: evidence for horizontal transmission. Gene 271:203–214 (2001).
34.
Martins C, Galetti PM Jr: Chromosome localization of 5S rRNA genes in Leporinus (Anostomidae, Characiformes). Chromosome Res 7:363–367 (1999).
35.
Martins C, Wasko AP, Oliveira C, Wright J: Nucleotide sequence of 5S rDNA and localization of the ribosomal RNA genes to metaphase chromosomes of the Tilapiini cichlid fish, Oreochromis niloticus. Hereditas 133:39–46 (2000).
36.
Martins C, Wasko AP, Oliveira C, Porto-Foresti F, Parise-Maltempi PP, et al: Dynamics of 5S rDNA in the tilapia (Oreochromis niloticus) genome: repeat units, inverted sequences, pseudogenes and chromosome loci. Cytogenet Genome Res 98:78–85 (2002).
37.
Mazzuchelli J, Martins C: Genomic organization of repetitive DNAs in the cichlid fish Astronotus ocellatus. Genetica 136:461–469 (2009).
38.
Molina WF, Galetti PM Jr: Robertsonian rearrangements in the reef fish Chromis (Perciformes, Pomacentridae) involving chromosomes bearing 5S rRNA genes. Genet Mol Biol 25:373–377 (2002).
39.
Mravinac B, Plohl M, Ugarkovic D: Conserved patterns in the evolution of Tribolium satellite DNAs. Gene 332:169–177 (2004).
40.
Nirchio M, Gaviria JI, Oliveira C, Ferreira IA, Martins C: Cytogenetic analysis of three species of the genus Haemulon (Teleostei: Haemulinae) from Margarita Island, Venezuela. Genetica 131:135–140 (2007).
41.
Ozouf-Costaz C, Brandt J, Körting C, Pisano E, Bonillo C, et al: Genome dynamics and chromosomal localization of the non-LTR retrotransposons Rex1 and Rex3 in Antarctic fish. Antarct Sci 16:51–57 (2004).
42.
Pinkel D, Straume T, Gray JW: Cytogenetic analysis using quantitative, high-sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938 (1986).
43.
Pontecorvo G, Felice BD, Carfagna M: A novel repeated sequence DNA originated from a Tc1-like transposon in water green frog Rana esculenta. Gene 261:205–210 (2000).
44.
Posada D, Crandall KA: Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818 (1998).
45.
Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574 (2003).
46.
Sambrook J, Russel DW: Molecular Cloning. A Laboratory Manual, 3rd ed (Cold Spring Harbor Laboratory Press, Cold Spring Harbor 2001).
47.
Schueler MG, Higgins AW, Rudd MK, Gustashaw K, Willard H: Genomic and genetic definition of a functional human centromere. Science 294:109–115 (2001).
48.
Smith WL, Chakrabarty P, Sparks JS: Phylogeny, taxonomy, and evolution of Neotropical cichlids (Teleostei: Cichlidae: Cichlinae). Cladistics 24:625–641 (2008).
49.
Sumner AT: A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304–306 (1972).
50.
Swofford DL: PAUP* – Phylogenetic analysis using parsimony (* and other methods). Version 4b10 (Sinauer, Sunderland 2002).
51.
Swofford DL, Olsen GJ, Waddell PJ, Hillis DM: Phylogenetic inference, in Hillis DM, Mable BK, Moritz C (eds): Molecular Systematics, pp 407–514 (Sinauer, Sunderland 1996).
52.
Szauter P: An analysis of regional constraints on exchange in Drosophila melanogaster using recombination-defective meiotic mutants. Genetics 106:45–71 (1984).
53.
Tamura K, Dudley J, Nei M, Kumar S: MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599 (2007).
54.
Tavaré S: Some probabilistic and statisical problems on the analysis of DNA sequences. Lect Math Life Sci 17:57–86 (1986).
55.
The International Cichlid Genome Consortium: Genetic basis of vertebrate diversity: the cichlid fish model. Available at http://hcgs.unh.edu/cichlid/ (2006).
56.
Thompson KW: Cytotaxonomy of 41 species of Neotropical Cichlidae. Copeia 1979:679–691 (1979).
57.
Vicari MR, Artoni RF, Moreira-Filho O, Bertollo LAC: Basic and molecular cytogenetics in freshwater Cichlidae (Osteichthyes, Perciformes). Karyotypic conservationism and divergence. Caryologia 59:260–266 (2006).
58.
Volff JN, Körting C, Sweeney K, Schartl M: The non-LTR retrotransposon Rex3 from the fish Xiphophorus is widespread among teleosts. Mol Biol Evol 16:1427–1438 (1999).
59.
Volff JN, Körting C, Schartl M: Multiple lineages of the non-LTR retrotransposon Rex1 with varying success in invading fish genomes. Mol Biol Evol 17:1673–1684 (2000).
60.
Volff JN, Körting C, Froschauer A, Sweeney K, Schartl M: Non-LTR retrotransposons encoding a restriction enzyme-like endonuclease in vertebrates. J Mol Evol 52:351–360 (2001).
61.
Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C: Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 19:674–678 (2003).
62.
Wong LH, Choo KH: Evolutionary dynamics of transposable elements at the centromere. Trends Genet 20:611–616 (2004).
63.
Xia X, Xie Z: DAMBE: Data analysis in molecular biology and evolution. J Hered 92:371–373 (2001).
© 2009 S. Karger AG, Basel
2009
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.