Sex chromosome evolution involves the accumulation of repeat sequences such as multigenic families, noncoding repetitive DNA (satellite, minisatellite, and microsatellite), and mobile elements such as transposons and retrotransposons. Most species of Characidium exhibit heteromorphic ZZ/ZW sex chromosomes; the W is characterized by an intense accumulation of repetitive DNA including dispersed satellite DNA sequences and transposable elements. The aim of this study was to analyze the distribution pattern of 18 different tandem repeats, including (GATA)n and (TTAGGG)n, in the genomes of C. zebra and C. gomesi, especially in the C. gomesi W chromosome. In the C. gomesi W chromosome, weak signals were seen for (CAA)10, (CAC)10, (CAT)10, (CGG)10, (GAC)10, and (CA)15 probes. (GA)15 and (TA)15 hybridized to the autosomes but not to the W chromosome. The (GATA)n probe hybridized to the short arms of the W chromosome as well as the (CG)15 probe. The (GATA)n repeat is known to be a protein-binding motif. GATA-binding proteins are necessary for the decondensation of heterochromatic regions that hold coding genes, especially in some heteromorphic sex chromosomes that may keep genes related to oocyte development. The (TAA)10 repeat is accumulated in the entire W chromosome, and this microsatellite accumulation is probably involved in the sex chromosome differentiation process and crossover suppression in C. gomesi. These additional data on the W chromosome DNA composition help to explain the evolution of sex chromosomes in Characidium.

1.
Abuín M, Martínez P, Sánchez L: Localization of the repetitive telomeric sequence (TTAGGG)n in four salmonid species. Genome 39:1035-1038 (1996).
2.
Akagi H, Yokozeki Y, Inagaki A, Mori K, Fujimura T: Micron, a microsatellite-targeting transposable element in the rice genome. Mol Genet Genomics 266:471-480 (2001).
3.
Bertollo LAC, Takahashi CS, Moreira-Filho O: Cytotaxonomic considerations on Hoplias lacerdae (Pisces, Erythrinidae). Brazil J Genet 1:103-120 (1978).
4.
Centofante L, Bertollo LAC, Moreira-Filho O: Comparative cytogenetics among sympatric species of Characidium (Pisces, Characiformes). Diversity analysis with the description of a ZW sex chromosome system and natural triploidy. Caryologia 54:253-260 (2001).
5.
Coates BS, Sumerford DV, Hellmich RL, Lewis LC: A Helitron-like transposon superfamily from Lepidoptera disrupts (GAAA)n microsatellites and is responsible for flanking sequence similarity within a microsatellite family. J Mol Evol 70:275-288 (2010).
6.
Cross I, Merlo A, Manchado M, Infante C, Cañavate JP, Rebordinos L: Cytogenetic characterization of the sole Solea senegalensis (Teleostei: Pleuronectiformes: Soleidae): Ag-NOR, (GATA)n, (TTAGGG)n and ribosomal genes by one-color and two-color FISH. Genetica 128:253-259 (2006).
7.
de Lange T: Protection of mammalian telomeres. Oncogene 21:532-540 (2002).
8.
Eschmeyer WN, Fricke R, van der Laan R (eds): Catalog of Fishes: Genera, Species, References. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. Electronic version accessed October 8, 2015.
9.
Grandi FC, An W: Non-LTR retrotransposons and microsatellites: partners in genomic variation. Mob Genet Elements 3:e25674 (2013).
10.
Hardman N: Structure and function of repetitive DNA in eukaryotes. Biochem J 234:1-11 (1986).
11.
Hatanaka T, Galetti PM Jr: Mapping of the 18S and 5S ribosomal RNA genes in the fish Prochilodus argenteus Agassiz, 1829 (Characiformes, Prochilodontidae). Genetica 122:239-244 (2004).
12.
Ijdo JW, Wells RA, Baldini A, Reeders ST: Improved telomere detection using a telomere repeat probe (TTAGGG)n generated by PCR. Nucleic Acids Res 19:4780 (1991).
13.
Kelkar YD, Eckert KA, Chiaromonte F, Makova KD: A matter of life or death: How microsatellites emerge in and vanish from the human genome. Genome Res 21:2038-2048 (2011).
14.
Kiel-Metzger K, Erickson RP: Regional localization of sex-specific Bkm-related sequences on proximal chromosome 17 of mice. Nature 310:579-581 (1984).
15.
Lui RL, Blanco DR, Martinez JF, Margarido VP, Venere PC, Moreira Filho O: The role of chromosomal fusion in the karyotypic evolution of the genus Ageneiosus (Siluriformes: Auchenipteridae). Neotrop Ichthyol 11:327-334 (2013).
16.
Machado TC, Pansonato-Alves JC, Pucci MB, Nogaroto V, Almeida MC, et al: Chromosomal painting and ZW sex chromosomes differentiation in Characidium (Characiformes, Crenuchidae). BMC Genet 12:65 (2011).
17.
Meyne J, Baker RJ, Hobart HH, Hsu TC, Ryder OA, et al: Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma 99:3-10 (1990).
18.
Milani D, Cabral-de-Mello DC: Microsatellite organization in the grasshopper Abracris flavolineata (Orthoptera: Acrididae) revealed by FISH mapping: remarkable spreading in the A and B chromosomes. PLoS One 9:e97956 (2014).
19.
Ocalewicz K: Telomeres in fishes. Cytogenet Genome Res 141:114-125 (2013).
20.
Palacios-Gimenez OM, Castillo ER, Martí DA, Cabral-de-Mello DC: Tracking the evolution of sex chromosome systems in Melanoplinae grasshoppers through chromosomal mapping of repetitive DNA sequences. BMC Evol Biol 13:167 (2013).
21.
Pansonato-Alves JC, Paiva LRS, Oliveira C, Foresti F: Interspecific chromosomal divergences in the genus Characidium (Teleostei: Characiformes: Crenuchidae). Neotrop Ichthyol 8:77-86 (2010).
22.
Pansonato-Alves JC, Vicari MR, Oliveira C, Foresti F: Chromosomal diversification in populations of Characidium cf. gomesi (Teleostei, Crenuchidae). J Fish Biol 78:183-194 (2011).
23.
Pansonato-Alves JC, Serrano É, Utsunomia R, Camacho JP, da Costa Silva GJ, et al: Single origin of sex chromosomes and multiple origins of B chromosomes in fish genus Characidium. PLoS One 9:e107169 (2014).
24.
Pazian MF, Shimabukuro-Dias CK, Pansonato-Alves JC, Oliveira C, Foresti F: Chromosome painting of Z and W sex chromosomes in Characidium (Characiformes, Crenuchidae). Genetica 141:1-9 (2013).
25.
Pinkel D, Straume T, Gray JW: Cytogenetic analysis using quantitative, high sensitivity, fluorescence hybridization. Proc Natl Acad Sci USA 83:2934-2938 (1986).
26.
Poltronieri J, Marquioni V, Bertollo LAC, Kejnovský E, Molina WF, et al: Comparative chromosomal mapping of microsatellites in Leporinus species (Characiformes, Anostomidae): unequal accumulation on the W chromosomes. Cytogenet Genome Res 142:40-45 (2013).
27.
Priyadarshini P, Murthy BS, Nagaraju J, Singh L: A GATA-binding protein expressed predominantly in the pupal ovary of the silkworm, Bombyx mori. Insect Biochem Mol Biol 33:185-195 (2003).
28.
Pucci MB, Barbosa P, Nogaroto V, Almeida MC, Artoni RF, et al: Population differentiation and speciation in the genus Characidium (Characiformes: Crenuchidae): effects of reproductive and chromosomal barriers. Biol J Linn Soc 111:541-553 (2014).
29.
Rosa KO, Ziemniczak K, Barros AV, Nogaroto V, Almeida MC, et al: Numeric and structural chromosome polymorphism in Rineloricaria lima (Siluriformes: Loricariidae): fusion points carrying 5S rDNA or telomere sequence vestiges. Rev Fish Biol Fisher 22:739-749 (2012).
30.
Ross JA, Peichel CL: Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish. Genetics 179:2173-2182 (2008).
31.
Scacchetti PC, Utsunomia R, Pansonato-Alves JC, Costa-Silva GJ, Oliveira C, Foresti F: Extensive spreading of interstitial telomeric sites on the chromosomes of Characidium (Teleostei, Characiformes). Genetica 143:263-270 (2015a).
32.
Scacchetti PC, Utsunomia R, Pansonato-Alves JC, Vicari MR, Artoni RF, et al: Chromosomal mapping of repetitive DNAs in Characidium (Teleostei, Characiformes): genomic organization and diversification of ZW sex chromosomes. Cytogenet Genome Res 146:136-143 (2015b).
33.
Scacchetti PC, Utsunomia R, Pansonato-Alves JC, da Costa Silva GJ, Vicari MR, et al: Repetitive DNA sequences and evolution of ZZ/ZW sex chromosomes in Characidium (Teleostei: Characiformes). PLoS One 10:e0137231 (2015c).
34.
Singh L, Purdom IF, Jones KW: Conserved sex-chromosome-associated nucleotide sequences in eukaryotes. Cold Spring Harb Symp Quant Biol 45:805-814 (1981).
35.
Singh L, Wadhwan R, Naidu S, Nagaraj R, Ganesan M: Sex- and tissue-specific Bkm (GATA)-binding protein in the germ cells of heterogametic sex. J Biol Chem 269:25321-25327 (1994).
36.
Steinemann S, Steinemann M: Retroelements: tools for sex chromosome evolution. Cytogenet Genome Res 110:134-143 (2005).
37.
Sumner AT: A simple technique for demonstrating centromeric heterochromatin. Exp Cell Res 75:304-306 (1972).
38.
Sumner AT: Chromosomes - Organization and Function (Blackwell Publishing, Malden 2003).
39.
Terencio ML, Schneider CH, Gross MC, Vicari MR, Farias IP, et al: Evolutionary dynamics of repetitive DNA in Semaprochilodus (Characiformes, Prochilodontidae): a fish model for sex chromosome differentiation. Sex Dev 7:325-333 (2013).
40.
Tóth G, Gáspári Z, Jurka J: Microsatellites in different eukaryotic genomes: survey and analysis. Genome Res 10:967-981 (2000).
41.
Trainor CD, Omichinski JG, Vandergon TL, Gronenborn AM, Clore GM, Felsenfeld G: A palindromic regulatory site within vertebrate GATA-1 promoters requires both zinc fingers of the GATA-1 DNA-binding domain for high-affinity interaction. Mol Cell Biol 16:2238-2247 (1996).
42.
Traldi JB, Blanco DR, Vicari MR, Martinez JF, Lui RL, et al: Physical mapping of (GATA)n and (TTAGGG)n sequences in species of Hypostomus (Siluriformes, Loricariidae). J Genet 1:127-30 (2013).
43.
Vicari MR, Artoni RF, Moreira-Filho O, Bertollo LAC: Diversification of a ZZ/ZW sex chromosome system in Characidium fish (Crenuchidae, Characiformes). Genetica 134:311-317 (2008).
44.
Ziemniczak K, Traldi JB, Nogaroto V, Almeida MC, Artoni RF, et al: In situ localization of (GATA)n and (TTAGGG)n repeated DNAs and W sex chromosome differentiation in Parodontidae (Actinopterygii: Characiformes). Cytogenet Genome Res 144:325-332 (2014).
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.