Molecular structure of the rDNA intergenic spacer (IGS) in Triturus: implications for the hypervariability of rDNA loci

Abstract

Ribosomal DNA (rDNA) variation in the species Triturus vulgaris meridionalis (Amphibia, Urodela) is remarkable because of unusually high intraspecific variability in the number and distribution of ribosomal loci in the karyotype; in addition, portions of the intergenic spacer (IGS) are clustered at chromosomal loci where they are not associated with ribosomal 18S and 28S RNA genes. These clusters are referred to as extraribosomal, and they appear to consist mostly of repetitive BamHI elements. In this paper, we report the complete nucleotide sequence of an IGS of T. v. meridionalis; this structural analysis is aimed to get insight into the molecular mechanism(s) of spreading of the ribosomal cistrons as well as its possible functional significance. We found that the IGS of T. vulgaris has a modular structure: modular repetitive elements contain sequences possibly related to the regulation of transcription of the ribosomal units. In particular, both ribosomal and extraribosomal IGS elements contain presumptive enhancers. Interestingly, the enhancer-containing region is mostly conserved between ribosomal and extraribosomal elements, while mutations accumulate in a region characterized by repetitions of a simple sequence motif, that we consider as a possible recombination hotspot. Our data suggest that extraribosomal elements most probably originated from ribosomal enhancer-containing elements able to move independently from the ribosomal unit at novel chromosomal positions, perhaps with the aid of the simple repetitive motif. We argue that a similar mechanism may lead to the spreading of complete repetition units as well, giving rise to multiple, and variable, ribosomal sites. We propose that hypervariability in the number and distribution of the rDNA loci, as seen in T. vulgaris, is a further mechanism to ensure redundancy, which seems to be an intrinsic property of rDNA biology, the occurrence of IGS elements independently clustered at separate chromosomal loci being a by-product of this mechanism.

First cytogenetic characterization of the sub-arctic marine fish Mallotus villosus (Müller, 1776), Osmeriformes, Osmeridae

“…This phenomenon has also been observed in a variety of organisms including other animals and plants (e.g. De Lucchini et al, 1997;Reed and Phillips, 2000;Pedrosa-Harand et al, 2006). The present ribosomal gene mapping for the osmerid capelin indicated that both the major and the 5S ribosomal genes are organized in multiple chromosomal loci, thus confirming the heterogeneous chromosomal organization of such sequences in fish species.…”

Contrast between extensive variation of 28S rDNA and stability of 5S rDNA and telomeric repeats in the diploid-polyploid Squalius alburnoides complex and in its maternal ancestor Squalius pyrenaicus (Teleostei, Cyprinidae)

“…Some of the observed 28S rDNA sites may correspond to genes that were displaced from tandem clusters to other areas of the genome by: virus, transposons, loop excision, and RNA transcription-mediated dispersal of genes (Rosenthal & Doering 1983). Tandemly repeated rDNA sequences located outside the rDNA loci are referred to as extra-ribosomal (De Lucchini et al 1988) and were already found in mouse (Arnheim et al 1980b) and in Triturus (Morgan et al 1980, De Lucchini et al 1997. The hybrid and polyploid genome of S. alburnoides increases the probability of occurrence of some the mechanisms referred to above.…”

Satellite DNA Derived from 5S rDNA in <i>Physalaemus cuvieri</i> (Anura, Leiuperidae)

“…Some cases have also been reported in animals, such as the fish Hoplias malabaricus , in which a satellite DNA with high similarity to 5S rDNA is found in the centromeric regions of various chromosomes, suggesting that this satellite DNA originates from 5S rDNA . The amphibian Triturus vulgaris provides another example in which a portion of the 40S rDNA intergenic spacer was detected in chromosome sites other than the NORs [De Lucchini et al, 1997].…”