Chromosomal Mapping of Repetitive DNAs in Triportheus trifurcatus (Characidae, Characiformes): Insights into the Differentiation of the Z and W Chromosomes

Abstract

Repetitive DNA sequences play an important role in the structural and functional organization of chromosomes, especially in sex chromosome differentiation. The genus Triportheus represents an interesting model for such studies because all of its species analyzed so far contain a ZZ/ZW sex chromosome system. A close relationship has been found between the differentiation of the W chromosome and heterochromatinization, with the involvement of different types of repetitive DNA in this process. This study investigated several aspects of this association in the W chromosome of Triportheus trifurcatus (2n = 52 chromosomes), including the cytogenetic mapping of repetitive DNAs such as telomeric sequences (TTAGGG)n, microsatellites and retrotransposons. A remarkable heterochromatic segment on the W chromosome was observed with a preferential accumulation of (CAC)10, (CAG)10, (CGG)10, (GAA)10 and (TA)15. The retrotransposons Rex1 and Rex3 showed a general distribution pattern in the chromosomes, and Rex6 showed a different distribution on the W chromosome. The telomeric repeat (TTAGGG)n was highly evident in both telomeres of all chromosomes without the occurrence of ITS. Thus, the differentiation of the W chromosome of T. trifurcatus is clearly associated with the formation of heterochromatin and different types of repetitive DNA, suggesting that these elements had a prominent role in this evolutionary process.

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

“…The Z chromosomes have additional heterochromatin in one or both telomeric regions, depending on the species, whereas the W chromosomes were almost entirely heterochromatic, except for the p arms in all species (Figure 1), in agreement with previous studies (Artoni and Bertollo, 2002;Diniz et al, 2009;Yano et al, 2014). The two-color FISH with 18S and 5S rDNA showed that both sites are colocalized on the p arms of the chromosome pair 3 in T. signatus, with an 18S rDNA additional site adjacent to the Wq telomere (Figure 2).…”

“…However, there are few empirical data for W chromosomes. The data presented here suggest that the W chromosomes of Triportheus have evolved during a relative short (~15-25 Myr) divergence time (phylogenetic data from Mariguela et al, 2016), displaying different genomic composition in terms of repetitive DNA sequences, size, and morphology among species, including accumulation of microsatellites, transposable elements and rDNAs on the W chromosomes (Yano et al, 2014), like the situation in the W chromosomes of pyralid moths (Vítková et al, 2007).…”

“…In fact, both techniques were critical to demonstrate the sequences that are still shared by both sex chromosomes or, otherwise, that those are more exclusive to one of them. Noteworthy, it was evidenced that the end of the Wq has a high concentration of female-specific sequences (Figures 2-4), where an 18S rDNA cluster is also located in all Triportheus species so far analyzed (Artoni and Evolution of sex chromosomes in congeneric species CF Yano et al Bertollo, 2002;Nirchio et al, 2007;Diniz et al, 2009;Marquioni et al, 2013;Yano et al, 2014). Sex chromosomes carrying 18S rDNA sequences have already been reported in several other vertebrates, such as Characidium fishes (Scacchetti et al, 2015), cane toad Bufo marinus (Abramyan et al, 2009), Chinese softshell turtle Pelodiscus sinensis (Kawai et al, 2007) and tiger snake Notechis scutatus (O'Meally et al, 2010).…”

“…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).…”

Mapping of the Retrotransposable Elements <b><i>Rex1</i></b> and <b><i>Rex3</i></b> in Chromosomes of <b><i>Eigenmannia</i></b> (Teleostei, Gymnotiformes, Sternopygidae)

“…In all samples of Eigenmannia analyzed here, a dispersed pattern of the elements Rex1 and Rex3 was observed. Similar data were found in 3 species of Hypoptopomatinae [Ferreira et al, 2011b], in Erythrinus erythrinus [Cioffi et al, 2010], in Oreochromis niloticus [Valente et al, 2011], and in Triportheus trifurcatus [Yano et al, 2014] suggesting that this is a common pattern among fish.…”