Hypermethylated Chromosome Regions in Nine Fish Species with Heteromorphic Sex Chromosomes

Schmid, Michael; Steinlein, Claus; Yano, Cássia Fernanda; Cioffi, Marcelo de Bello

doi:10.1159/000444067

Cited by 14 publications

(8 citation statements)

References 44 publications

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“…The Z is a metacentric chromosome, the largest one in the karyotype, whereas the W is always smaller than the Z, and varies in size and morphology among species (Bertollo and Cavallaro, 1992;Sánchez and Jorge, 1999;Artoni et al, 2001;Artoni and Bertollo, 2002;Nirchio et al, 2007;Diniz et al, 2008;Yano et al, 2014Yano et al, , 2016. Besides, the W chromosome is rich in heterochromatin and carries an 18S ribosomal DNA (rDNA) site on its long arms (Artoni and Bertollo, 2002;Nirchio et al, 2007;Diniz et al, 2009;Marquioni et al, 2013;Yano et al, 2014;Schmid et al, 2016). Recently, a molecular phylogeny of the Triportheidae family was introduced based on the 16S rRNA and cytochrome b (CytB) mitochondrial genes, and on the recombination activating gene 1 (Rag1), recombination activating gene 2 (Rag2) and myosin heavy chain 6 cardiac muscle-α (Myh6) nuclear genes (Mariguela et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

et al. 2016

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The main objectives of this study were to test: (1) whether the W-chromosome differentiation matches to species' evolutionary divergence (phylogenetic concordance) and (2) whether sex chromosomes share a common ancestor within a congeneric group. The monophyletic genus Triportheus (Characiformes, Triportheidae) was the model group for this study. All species in this genus so far analyzed have ZW sex chromosome system, where the Z is always the largest chromosome of the karyotype, whereas the W chromosome is highly variable ranging from almost homomorphic to highly heteromorphic. We applied conventional and molecular cytogenetic approaches including C-banding, ribosomal DNA mapping, comparative genomic hybridization (CGH) and cross-species whole chromosome painting (WCP) to test our questions. We developed Z-and W-chromosome paints from T. auritus for cross-species WCP and performed CGH in a representative species (T. signatus) to decipher level of homologies and rates of differentiation of W chromosomes. Our study revealed that the ZW sex chromosome system had a common origin, showing highly conserved Z chromosomes and remarkably divergent W chromosomes. Notably, the W chromosomes have evolved to different shapes and sequence contents within~15-25 Myr of divergence time. Such differentiation highlights a dynamic process of W-chromosome evolution within congeneric species of Triportheus.

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Section: Introductionmentioning

confidence: 99%

Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

et al. 2016

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“…phases of fish [Schmid et al, 2015a], amphibians [Schmid and Steinlein, 2016], birds [Schmid et al, 2015b;Schmid and Steinlein, 2017], and mammals [Schmid et al, 2015c]. However, to our knowledge, no cytogenetic analyses on the occurrence of 5-methylcytosine-rich regions have been carried out in nonavian reptiles.…”

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confidence: 99%

5-Methylcytosine-Rich Heterochromatin in Reptiles

Schmid

Steinlein

Reiter

et al. 2019

Cytogenet Genome Res

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An experimental approach using monoclonal anti-5-methylcytosine antibodies and indirect immunofluorescence was elaborated for detecting 5-methylcytosine-rich chromosome regions in reptilian chromosomes. This technique was applied to conventionally prepared mitotic metaphases of 2 turtle species and 12 squamate species from 8 families. The hypermethylation patterns were compared with C-banding patterns obtained by conventional banding techniques. The hypermethylated DNA sequences are species-specific and are located in constitutive heterochromatin. They are highly reproducible and often found in centromeric, pericentromeric, and interstitial positions of the chromosomes. Heterochromatic regions in differentiated sex chromosomes are particularly hypermethylated.

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“…Indeed, the transposable sequences in the human genome are highly methylated ( Kricker et al 1992 ). Fishes have shown hypermethylated regions confined to constitutive heterochromatin, particularly in heteromorphic sex chromosomes, demonstrating that several hypermethylated regions are co-localized with repetitive elements ( Schmid et al 2016 ).…”

Section: Discussionmentioning

confidence: 99%

“…Although the knowledge of the methylation patterns is growing among vertebrates, it is still restricted in fishes, especially in relation to repetitive DNA regions (transcriptional and non-transcriptional), which are apparently limited to the heterochromatic regions and sex chromosomes ( Schmid et al 2016 ). Repetitive sequences have been the target of intense investigation in several fish groups ( Vicari et al 2008 ; Cioffi et al 2010b ; Costa et al 2014 , 2016 ; Barbosa et al 2015 ), showing extreme complexity in some species ( Costa et al 2015 ).…”

Section: Introductionmentioning

confidence: 99%

Differential hypomethylation of the repetitive Tol2/Alu-rich sequences in the genome of Bodianus species (Labriformes, Labridae)

Motta-Neto

Marques

Costa

et al. 2018

CCG

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Representatives of the order Labriformes show karyotypes of extreme conservatism together with others with high chromosomal diversification. However, the cytological characterization of epigenetic modifications remains unknown for the majority of the species. In the family Labridae, the most abundant fishes on tropical reefs, the genomes of the genus Bodianus Bloch, 1790 have been characterized by the occurrence of a peculiar chromosomal region, here denominated BOD. This region is exceptionally decondensed, heterochromatic, argentophilic, GC-neutral and, in contrast to classical secondary constrictions, shows no signals of hybridization with 18S rDNA probes. In order to characterize the BOD region, the methylation pattern, the distribution of Alu and Tol2 retrotransposons and of 18S and 5S rDNA sites, respectively, were analyzed by Fluorescence In Situ Hybridization (FISH) on metaphase chromosomes of two Bodianus species, B. insularis Gomon & Lubbock, 1980 and B. pulchellus (Poey, 1860). Immunolocalization of the 5-methylcytosine revealed hypermethylated chromosomal regions, dispersed along the entire length of the chromosomes of both species, while the BOD regions exhibited a hypomethylated pattern. Hypomethylation of the BOD region is associated with the precise co-location of Tol2 and Alu elements, suggesting their active participation in the regulatory epigenetic process. This evidence underscores a probable differential methylation action during the cell cycle, as well as the role of Tol2/Alu elements in functional processes of fish genomes.

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Hypermethylated Chromosome Regions in Nine Fish Species with Heteromorphic Sex Chromosomes

Cited by 14 publications

References 44 publications

Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

Highly conserved Z and molecularly diverged W chromosomes in the fish genus Triportheus (Characiformes, Triportheidae)

5-Methylcytosine-Rich Heterochromatin in Reptiles

Differential hypomethylation of the repetitive Tol2/Alu-rich sequences in the genome of Bodianus species (Labriformes, Labridae)

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