Repetitive Sequences: the Hidden Diversity of Heterochromatin in Prochilodontid Fish

Overview

Journal Comp Cytogenet

Date 2016 Jan 12

PMID 26752156

Citations 8

Authors

Maria L Terencio

Carlos H Schneider

Maria C Gross

Edson Junior do Carmo

Viviane Nogaroto

Mara Cristina de Almeida

Roberto Ferreira Artoni

Marcelo R Vicari

Eliana Feldberg

Affiliations

Soon will be listed here.

Abstract

The structure and organization of repetitive elements in fish genomes are still relatively poorly understood, although most of these elements are believed to be located in heterochromatic regions. Repetitive elements are considered essential in evolutionary processes as hotspots for mutations and chromosomal rearrangements, among other functions - thus providing new genomic alternatives and regulatory sites for gene expression. The present study sought to characterize repetitive DNA sequences in the genomes of Semaprochilodus insignis (Jardine & Schomburgk, 1841) and Semaprochilodus taeniurus (Valenciennes, 1817) and identify regions of conserved syntenic blocks in this genome fraction of three species of Prochilodontidae (Semaprochilodus insignis, Semaprochilodus taeniurus, and Prochilodus lineatus (Valenciennes, 1836) by cross-FISH using Cot-1 DNA (renaturation kinetics) probes. We found that the repetitive fractions of the genomes of Semaprochilodus insignis and Semaprochilodus taeniurus have significant amounts of conserved syntenic blocks in hybridization sites, but with low degrees of similarity between them and the genome of Prochilodus lineatus, especially in relation to B chromosomes. The cloning and sequencing of the repetitive genomic elements of Semaprochilodus insignis and Semaprochilodus taeniurus using Cot-1 DNA identified 48 fragments that displayed high similarity with repetitive sequences deposited in public DNA databases and classified as microsatellites, transposons, and retrotransposons. The repetitive fractions of the Semaprochilodus insignis and Semaprochilodus taeniurus genomes exhibited high degrees of conserved syntenic blocks in terms of both the structures and locations of hybridization sites, but a low degree of similarity with the syntenic blocks of the Prochilodus lineatus genome. Future comparative analyses of other prochilodontidae species will be needed to advance our understanding of the organization and evolution of the genomes in this group of fish.

Citing Articles

Chromosomal characterization of three species of Serrasalmini (Serrasalmidae: Characiformes).

Santos A, de Sousa E Souza J, Cardoso Soares S, Nakayama C, Feldberg E Genet Mol Biol. 2023; 46(4):e20230088.

PMID: 37992304 PMC: 10664975. DOI: 10.1590/1678-4685-GMB-2023-0088.

Telomeres and Their Neighbors.

Jenner L, Peska V, Fulneckova J, Sykorova E Genes (Basel). 2022; 13(9).

PMID: 36140830 PMC: 9498494. DOI: 10.3390/genes13091663.

A new view on the scenario of karyotypic stasis in Epinephelidae fish: Cytogenetic, historical, and biogeographic approaches.

Amorim K, Werneck Felix da Costa G, Cioffi M, Tanomtong A, Bertollo L, Molina W Genet Mol Biol. 2021; 44(4):e20210122.

PMID: 34807969 PMC: 8608104. DOI: 10.1590/1678-4685-GMB-2021-0122.

Organization and expression analysis of 5S and 45S ribosomal DNA clusters in autotetraploid Carassius auratus.

Zhao C, Zhang Y, Qin H, Wang C, Huang X, Yang L BMC Ecol Evol. 2021; 21(1):201.

PMID: 34740327 PMC: 8569995. DOI: 10.1186/s12862-021-01918-2.

Cytogenetic analysis of Bienertia sinuspersici Akhani as the first step in genome sequencing.

Sevilleno S, Ju Y, Kim J, Mancia F, Byeon E, Cabahug R Genes Genomics. 2020; 42(3):337-345.

PMID: 31902107 DOI: 10.1007/s13258-019-00908-5.

References

Wichman H, Van Den Bussche R, Hamilton M, Baker R . Transposable elements and the evolution of genome organization in mammals. Genetica. 1992; 86(1-3):287-93. DOI: 10.1007/BF00133727. View

Artoni R, Vicari M, Endler A, Cavallaro Z, de Jesus C, de Almeida M . Banding pattern of A and B chromosomes of Prochilodus lineatus (Characiformes, Prochilodontidae), with comments on B chromosomes evolution. Genetica. 2006; 127(1-3):277-84. DOI: 10.1007/s10709-005-4846-1. View

Teixeira W, Ferreira I, Cabral-de-Mello D, Mazzuchelli J, Valente G, Pinhal D . 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. 2009; 125(3):224-34. DOI: 10.1159/000230006. View

Shapiro J, von Sternberg R . Why repetitive DNA is essential to genome function. Biol Rev Camb Philos Soc. 2005; 80(2):227-50. DOI: 10.1017/s1464793104006657. View

Gross M, Schneider C, Valente G, Porto J, 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. 2010; 127(1):43-53. DOI: 10.1159/000279443. View

Zhou Q, Froschauer A, Schultheis C, Schmidt C, Bienert G, Wenning M . Helitron Transposons on the Sex Chromosomes of the Platyfish Xiphophorus maculatus and Their Evolution in Animal Genomes. Zebrafish. 2008; 3(1):39-52. DOI: 10.1089/zeb.2006.3.39. View

Valente G, Mazzuchelli J, Ferreira I, Poletto A, Fantinatti B, Martins C . Cytogenetic mapping of the retroelements Rex1, Rex3 and Rex6 among cichlid fish: new insights on the chromosomal distribution of transposable elements. Cytogenet Genome Res. 2011; 133(1):34-42. DOI: 10.1159/000322888. View

Li Y, Korol A, Fahima T, Beiles A, Nevo E . Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review. Mol Ecol. 2002; 11(12):2453-65. DOI: 10.1046/j.1365-294x.2002.01643.x. View

Mazzuchelli J, Martins C . Genomic organization of repetitive DNAs in the cichlid fish Astronotus ocellatus. Genetica. 2008; 136(3):461-9. DOI: 10.1007/s10709-008-9346-7. View

10.

Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A . Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet. 2005; 37(9):997-1002. DOI: 10.1038/ng1615. View

11.

Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M . B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet. 2011; 7(8):e1002203. PMC: 3158035. DOI: 10.1371/journal.pgen.1002203. View

12.

Ivics Z, Izsvak Z, Minter A, Hackett P . Identification of functional domains and evolution of Tc1-like transposable elements. Proc Natl Acad Sci U S A. 1996; 93(10):5008-13. PMC: 39397. DOI: 10.1073/pnas.93.10.5008. View

13.

Bohne A, Zhou Q, Darras A, Schmidt C, Schartl M, Galiana-Arnoux D . Zisupton--a novel superfamily of DNA transposable elements recently active in fish. Mol Biol Evol. 2011; 29(2):631-45. DOI: 10.1093/molbev/msr208. View

14.

Jurka J, Kapitonov V, Pavlicek A, Klonowski P, Kohany O, Walichiewicz J . Repbase Update, a database of eukaryotic repetitive elements. Cytogenet Genome Res. 2005; 110(1-4):462-7. DOI: 10.1159/000084979. View

15.

Doolittle W, Sapienza C . Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980; 284(5757):601-3. DOI: 10.1038/284601a0. View

16.

Zwick M, Hanson R, Islam-Faridi M, Stelly D, Wing R, Price H . A rapid procedure for the isolation of C0t-1 DNA from plants. Genome. 1997; 40(1):138-42. DOI: 10.1139/g97-020. View

17.

Fernandez-Medina R, Ribeiro J, Carareto C, Velasque L, Struchiner C . Losing identity: structural diversity of transposable elements belonging to different classes in the genome of Anopheles gambiae. BMC Genomics. 2012; 13:272. PMC: 3442997. DOI: 10.1186/1471-2164-13-272. View

18.

Kapitonov V, Jurka J . A novel class of SINE elements derived from 5S rRNA. Mol Biol Evol. 2003; 20(5):694-702. DOI: 10.1093/molbev/msg075. View

19.

Timberlake W . Low repetitive DNA content in Aspergillus nidulans. Science. 1978; 202(4371):973-5. DOI: 10.1126/science.362530. View

20.

Camacho J, Sharbel T, Beukeboom L . B-chromosome evolution. Philos Trans R Soc Lond B Biol Sci. 2000; 355(1394):163-78. PMC: 1692730. DOI: 10.1098/rstb.2000.0556. View