• Open Access

Chromosomal evolution in Mugilidae (Pisces, Mugiliformes): FISH mapping of the (TTAGGG)n telomeric repeat in the six Mediterranean mullets

Authors

  • E. GORNUNG,

  • M. E. MANNARELLI,

  • A. R. ROSSI,

  • L. SOLA


Department of Animal and Human Biology, University of Rome I “La Sapienza”, Via A. Borelli 50, 00161 Rome, Italy. E-mail: luciana.sola@uniroma1.it

The family Mugilidae includes more than 60 species (Thomson 1997) which inhabit coastal and brackish waters of all tropical and temperate regions of the world. Six species, Mugil cephalus, Liza aurata, L. ramada, L. saliens, Chelon labrosus and Oedalechilus labeo, are commonly found in the Mediterranean. In our previous karyological studies on the Mediterranean mullets (Rossi et al. 1996, 1997, 2000; Gornung et al. 2001), we found that their morphologically conservative karyotype – corresponding to the 48 uni-armed-chromosome type considered ancestral for all Teleosts (Ohno 1974) – revealed the occurrence of finer differentiated features.

More specifically, M. cephalus shows an all-acrocentric karyotype, while the three species of Liza,C. labrosus and O. labeo show one subtelocentric chromosome pair (chromosome pair 24 in the Liza-Chelon group and chromosome pair 9 in the latter species) among the remaining acrocentric chromosomes. When analysed by FISH, using major and minor ribosomal genes as probes (Gornung et al. 2001), these differences led to the identification of a possible karyoevolutive pattern. The presence of this subtelocentric chromosome pair was found to be related to the location of the major ribosomal genes on its short arms. Thus, a translocation of NORs, from the terminal region of chromosomes 1 to the short arms of chromosomes 24 or chromosomes 9, was hypothesized to have occurred in an ancestor with a karyotype similar to the one presently found in M. cephalus. Interestingly, the 5S rDNA site in M. cephalus is located on the same chromosome pair, chromosome pair 24, which bears NORs, though in a different position, in the Liza-Chelon group. All the other mullet species share a 5S rDNA location in a subcentromeric position of chromosome pair 8, but L. saliens also shows an additional 5S rDNA site in a location close to the one shown by major ribosomal genes in M. cephalus, i.e. the subtelomeric region of chromosomes 1. In consideration of this, a further event of reciprocal translocation for these two sets of genes with respect to a common ancestral karyotype has been hypothesized (Gornung et al. 2001). In this context, it seemed interesting to investigate the possible presence of interstitial telomeric sites, which might be useful in detecting chromosomal rearrangements (Meyne et al. 1990). In addition, this is the first report on the chromosomal distribution of the telomeric repeats in the family.

The telomeric sequence motif was synthesized as two 42-base complementary heptameres (GGGTTA)7/(TAACCC)7 end-labelled with biotin at both 3’ and 5’ positions (M-Medical, Genenco). Conventional procedures for fluorescence in situ hybridization (FISH) of repetitive sequences (Lichter et al. 1992) were applied to metaphase preparations.

In all six species, under both high and low stringency conditions, the telomeric repeats hybridized at natural telomeres. Additional hybridization signals were observed scattered along the NORs in all three cytotypes, both at NORs located in the terminal region of chromosomes 1 in M. cephalus (1a) and along the whole short arms of chromosome pair 24 in the Liza-Chelon group (1b) or of chromosome pair 9 in O. labeo (1c).

Figure 1(a–c).

FISH with a telomeric probe on metaphase plates of (a)M. cephalus, (b) L. ramada (chosen as representative of the cytotype of the Liza-Chelon group), (c)O. labeo. In all six species the hybridization signals can be observed to the end of all chromosomes and also scattered along the NORs (arrows and selected samples in the insets); scale bar =5 μm.

Multiple telomeric sites have been found scattered along NORs in other fish species, such as Anguilla anguilla and A. rostrata (Salvadori et al. 1995), Oncorhynchus mykiss (Abuín et al. 1996) and Rhodeus ocellatus kurumeus (Sola et al. 2003). There is a limited number of species showing such an interspersion compared to the approximately 30 species of teleosts (Sola et al. 2003) investigated for the chromosomal localization of the telomeric repeats, a fact which supports the original hypothesis (Salvadori et al. 1995) that such a feature might be species-specific and might constitute a hot spot of recombination for NORs in respective taxa. Similarly, the abundance of these sites within NORs might have constituted the basis of the hypothesized translocation events in the Mediterranean mullets (Gornung et al. 2001).

Acknowledgements

This work was supported by research grants from MURST to L. Sola.

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