To enhance our understanding of the organization of the genome and chromosome evolution of cichlid fish species, we have isolated and physically mapped onto the chromosomes the transposable elements (TEs) Rex1, Rex3 and Rex6, which are conserved in teleost fish, in the chromosomes of African and South American cichlid species. The physical mapping of different Rex elements showed that they are primarily compartmentalized in the pericentromeric heterochromatic regions, although dispersed or clustered signals in euchromatic regions were also observed. The presence of TEs in heterochromatin can be correlated with their role in the structure and organization of heterochromatic areas (such as centromeres) or with the lower selective pressure that act on these gene-poor regions. The Rex elements were also concentrated in the largest chromosome pair of the Nile tilapia, Oreochromis niloticus. This chromosome pair is supposed to have originated by fusions, demonstrating the possible involvement of TEs with chromosome rearrangements. Besides general patterns of chromosomal distribution, comparative analysis suggests that Rex elements could differ in their chromosomal distribution among different fish groups or species and that intrinsic aspects of the genomes could influence the spread, accumulation or elimination of TEs.

1.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 215:403–410 (1990).
2.
Aparicio S, Chapman J, Stupka E, Putnam N, Chia JM, et al: Whole-genome shotgun assembly and analysis of the genome of Fugu rubripes. Science 297:1301–1310 (2002).
3.
Bachtrog D: Sex chromosome evolution: Molecular aspects of Y-chromosome degeneration in Drosophila. Genome Res 15:1393–1401 (2005).
4.
Bertollo LAC, Takahashi CS, Moreira-Filho O: Cytotaxonomic consideration on Hoplias lacerdae (Pisces, Erythrinidae). Braz J Genet 1:103–120 (1978).
5.
Biémont C, Vieira C: Junk DNA as an evolutionary force. Nature 443:521–524 (2006).
6.
Böhne A, Brunet F, Galiana-Arnoux D, Schultheis C, Volff JN: Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res 16:203–215 (2008).
7.
Bouneau L, Fischer C, Ozouf-Costaz C, Froschauer A, Jaillon O, et al: An active non-LTR retrotransposon with tandem structure in the compact genome of the pufferfish Tetraodon nigroviridis. Genome Res 13:1686–1695 (2003).
8.
Cáceres M, Ranz JM, Barbadilla A, Long M, Ruiz A: Generation of a widespread Drosophila inversion by a transposable element. Science 285:415–418 (1999).
9.
Cáceres M, Puig M, Ruiz A: Molecular characterization of two natural hotspots in the Drosophila buzzatii genome induced by transposon insertions. Genome Res 11:1353–1364 (2001).
10.
Capriglione T, Odierna G, Caputo V, Canapa A, Olmo E: Caracterization of Tc1-like transposon in Antarctic ice-fish Chionodraco hamatus. Gene 295:193–198 (2002).
11.
Carrasco LAP, Penman DJ, Bromage N: Evidence for the presence of sex chromosomes in the Nile tilapia (Oreochromis niloticus) from synaptonemal complex analysis of XX, XY and YY genotypes. Aquaculture 173:207–218 (1999).
12.
Charlesworth B, Sniegowski P, Stephan W: The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371:215–220 (1994).
13.
Charlesworth D, Charlesworth B, Marais G: Steps in the evolution of heteromorphic sex chromosomes. Heredity 95:118–128 (2005).
14.
Chew JSK, Oliveira C, Wright JM, Dobson MJ: Molecular and cytogenetic analysis of the telomeric (TTAGGG)n repetitive sequences in the Nile tilapia, Oreochromis niloticus (Teleostei: Cichlidae). Chromosoma 111:45–52 (2002).
15.
Cioffi MB, Martins C, Vicari MR, Rebordinos L, Bertollo LAC: Differentiation of the XY sex chromosomes in Hoplias malabaricus (Characiformes, Erythrinidae). Unusual accumulation of repetitive sequences on the X chromosome. Sex Dev 4:176–185 (2010).
16.
Cnaani A, Lee B-Y, Zilberman N, Ozouf-Costaz C, Hulata G, et al: Genetics of sex determination in tilapiine species. Sex Dev 2:43–54 (2008).
17.
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).
18.
Dawe RK: RNA interference, transposons, and the centromere. Plant Cell 15:297–301 (2003).
19.
Devlin RH, Stone GW, Smailus DE: Extensive direct-tandem organization of a long repeat DNA sequence on the Y chromosome of Chinook salmon (Oncorhynchus tshawytscha). J Mol Evol 46:277–287 (1998).
20.
Dimitri P, Junakovic N: Revising the selfish DNA hypothesis new evidence on accumulation of transposable elements in heterochromatin. Trends Genet 15:123–124 (1999).
21.
Dimitri P, Arca B, Berghella L, Mei E: High genetic instability of heterochromatin after transposition of the LINE-like I factor in Drosophila melanogaster. Proc Natl Acad Sci USA 94:8052–8057 (1997).
22.
Doolittle WF, Sapienza C: Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603 (1980).
23.
Evgen’ev MB, Zelentsova H, Poluectova H, Lyozin GT, Veleikodvorskaja V, et al: Mobile elements and chromosomal evolution in the virilis group of Drosophila. Proc Natl Acad Sci USA 97:11337–11342 (2000).
24.
FAO: World aquaculture production of fish, crustaceans, mollusks, etc., by principal species in 2008. Food and Agriculture Organization of the United Nations (2008) at ftp://ftp.fao.org/fi/stat/summary/a-6.pdf.
25.
Ferreira IA, Martins C: Physical chromosome mapping of the Nile tilapia Oreochromis niloticus using repetitive DNA sequences. Micron 39:411–418 (2008).
26.
Ferreira IA, Poletto A, Kocher TD, Mota-Velasco JC, Penman D, Martins C: Chromosome evolution in African cichlid fish: contributions from the physical mapping of repeated DNAs. Cytogenet Genome Res 129:314–322 (2010).
27.
Feschotte C, Pritham EJ: DNA transposons and the evolution of eukaryotic genomes. Annu Rev Genet 41:331–368 (2007).
28.
Fisher C, Bouneau L, Coutanceau JP, Weissenbach J, Volff JN, Ozouf-Costaz C: Global heterochromatic colocalization of transposable elements with minisatellites in the compact genome of the pufferfish Tetraodon nigroviridis. Gene 336:175–184 (2004).
29.
Flavell RB, Bennett MD, Smith JB, Smith DB: Genome size and the proportion of repeated nucleotide sequence DNA in plants. Biochem Genet 12:257–269 (1974).
30.
Fraser JA, Heitman J: Chromosomal sex-determining regions in animals, plants and fungi. Curr Opin Genet Dev 15:645–651 (2005).
31.
Griffin DK, Harvey SC, Campos-Ramos R, Ayling L-J, Bromage NR, et al: Early origins of the X and Y chromosomes: lessons from tilapia. Cytogenet Genome Res 99:157–163 (2002).
32.
Gross MC, Schneider CH, Valente GT, Porto JIR, Martins C, Feldberg E: Comparative cytogenetic analysis of the genus Symphysodon (Discus fishes, Cichlidae): chromosomal characteristics of retrotransposons and minor ribosomal DNA. Cytogenet Genome Res 127:43–53 (2009).
33.
Gross MC, Schneider CH, Valente GT, Martins C, Feldberg E: Variability of 18S rDNA locus among Symphysodon fishes: chromosomal rearrangements. J Fish Biol 76:1117–1127 (2010).
34.
Harvey SC, Boonphakdee C, Campos-Ramos R, Ezaz MT, Griffin DK, et al: Analysis of repetitive DNA sequences in the sex chromosomes of Oreochromis niloticus. Cytogenet Genome Res 101:314–319 (2003).
35.
Hua-Van A, Le Rouzic A, Maisonhaute C, Capy P: Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences. Cytogenet Genome Res 110:426–440 (2005).
36.
International Human Genome Sequencing Consortium: Initial sequencing and analysis of the human genome. Nature 409:860–921 (2001).
37.
Jiang J, Gill BS, Wang GL, Ronald PC, Ward DC: Metaphase and interphase fluorescence in situ hybridization mapping of the rice genome with bacterial artificial chromosomes. Proc Natl Acad Sci USA 92:4487–4491 (1995).
38.
Kidwell MG: Transposable elements, in Gregory T (ed): The Evolution of the Genome, pp 165–223 (Elsevier Academic Press, Burlington 2005).
39.
Kidwell MG, Lisch DR: Transposable elements and host genome evolution. Trends Ecol Evol 15:95–99 (2000).
40.
Kocher TD: Adaptive evolution and explosive speciation: the cichlid fish model. Nature 5:288–298 (2004).
41.
Kocher TD: Genetic basis of vertebrate diversity: the cichlid fish model. The International Cichlid Genome Consortium (2006) at http://cichlid.umd.edu/CGCindex.html.
42.
Kornfield IL, Ritte U, Richler C, Wahrman J: Biochemical and cytological differentiation among cichlid fishes of the Sea of Galilee. Evolution 33:1–14 (1979).
43.
Lanfredi M, Congiu L, Garrido-Ramos MA, Herrán RD, Leis M, et al: Chromosomal location and evolution of a satellite DNA family in seven sturgeon species. Chromosome Res 9:47–52 (2001).
44.
Liem KF: Functional morphology, in Keenleyside MHA (ed): Cichlid Fishes: Behavior, Ecology and Evolution, pp 129–150 (Chapman and Hall, London 1991).
45.
Lim JK, Simmons MJ: Gross chromosome rearrangements mediated by transposable elements in Drosophila melanogaster. BioEssays 16:269–275 (1994).
46.
Lowe-McConnell RH: Estudos ecológicos de comunidades de peixes tropicais. (EDUSP, São Paulo 1999).
47.
Lyttle TW, Haymer DS: The role of the transposable element hobo in the origin of endemic inversions in wild populations of Drosophila melanogaster. Genetica 86:113–126 (1992).
48.
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).
49.
Mazzuchelli J, Martins C: Genomic organization of repetitive DNAs in the cichlid fish Astronotus ocellatus. Genetica 136:461–469 (2009).
50.
Mestriner CA, Galetti PM Jr, Valentini SR, Ruiz IR, Abel LD, et al: Structural and functional evidence that a B chromosome in the characid fish Astyanax scabripinnis is an isochromosome. Heredity 85:1–9 (2000).
51.
Ming R, Moore PH: Genomics of sex chromosomes. Curr Opin Plant Biol 10:123–130 (2007).
52.
Mota-Velasco JC, Ferreira IA, Cioffi MB, Ocalewicz K, Campos-Ramos R, et al: Characterization of the chromosome fusions in Oreochromis karongae. Chromosome Res 18:575–586 (2010).
53.
Oliveira C, Wright JM: Molecular cytogenetic analysis of heterochromatin in the chromosomes of tilapia, Oreochromis niloticus (Teleostei: Cichlidae). Chromosome Res 6:205–211 (1998).
54.
Oliveira C, Chew JSK, Porto-Foresti F, Dobson MJ, Wright JM: A LINE-like repetitive DNA sequence from the cichlid fish, Oreochromis niloticus: sequence analysis and chromosomal distribution. Chromosoma 108:457–468 (1999).
55.
Oliveira C, Wang Y, Bryden LJ, Wright J: Short interspersed repetitive elements (SINEs) from the cichlid fish, Oreochromis niloticus, and their chromosomal localization by fluorescent in situ hybridization. Caryologia 56:181–189 (2003).
56.
Ozouf-Costaz C, Brandt J, Körting C, Pisano E, Bonillo C: Genome dynamics and chromosomal localization of the non-LTR retrotransposons Rex1 and Rex3 in Antarctic fish. Antarctic Sci 16:51–57 (2004).
57.
Pinkel D, Straume T, Gray JW: Cytogenetic analysis using quantitative, high-sensitivity fluorescence hybridization. Proc Natl Acad Sci USA 83:2934–2938 (1986).
58.
Poletto AB, Ferreira IA, Martins C: The B chromosomes of the African cichlid fish Haplochromis obliquidens harbour 18S rRNA gene copies. BMC Genet 11:1 (2010a).
59.
Poletto AB, Ferreira IA, Cabral-de-Mello DC, Nakajima RT, Mazzuchelli J, et al: Chromosome differentiation patterns during cichlid fish evolution. BMC Genet 11:50 (2010b).
60.
Raskina O, Barber JC, Nevo E, Belyayev A: Repetitive DNA and chromosomal rearrangements: speciation-related events in plant genomes. Cytogenet Genome Res 120:351–357 (2008).
61.
Sambrook J, Russel DW: Molecular Cloning. A Laboratory Manual, 3rd ed. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor 2001).
62.
Smith WL, Chakrabarty P, Sparks J: Phylogeny, taxonomy, and evolution of neotropical Cichlids (Teleostei: Cichlidae: Cichlinae). Cladistics 24:625–641 (2008).
63.
Stein J, Phillips RB, Devlin RH: Identification of the Y chromosome in chinook salmon (Oncorhynchus tshawytscha). Cytogenet Cell Genet 92:108–110 (2001).
64.
Syvanen M: Horizontal gene transfer: evidence and possible consequences. Annu Rev Genet 28:237–261 (1994).
65.
Teixeira WG, Ferreira IA, Cabral-de-Mello DC, Mazzuchelli J, Valente GT, et al: Organization of repeated DNA elements in the genome of the cichlid fish Cichla kelberi and its contributions to the knowledge of fish genomes. Cytogenet Genome Res 125:224–234 (2009).
66.
The Arabidopsis Genome Initiative: Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815 (2000).
67.
Turner GF: Adaptive radiation of cichlid fish. Curr Biol 17:R827-R831 (2007).
68.
Valente GT, Schneider CH, Gross MC, Feldberg E, Martins C: Comparative cytogenetics of cichlid fishes through genomic in-situ hybridization (GISH) with emphasis on Oreochromis niloticus. Chromosome Res 17:791–799 (2009).
69.
Vicari MR, Moreira-Filho O, Artoni RF, Bertollo LAC: Basic and molecular cytogenetics in freshwater Cichlidae (Osteichthyes, Perciformes). Karyotypic conservationism and divergence. Caryologia 59:260–266 (2006).
70.
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).
71.
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).
72.
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).
73.
Volff JN, Bouneau L, Ozouf-Costaz C, Fischer C: Diversity of retrotransposable elements in compact pufferfish genomes. Trends Genet 19:674–678 (2003).
74.
Zhang J, Peterson T: Genome rearrangements by non-linear transposons in maize. Genetics 153:1403–1410 (1999).
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.