The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families.

Abstract

We review all instances in which the nuclear 5S rRNA genes of fungi, protist, nematode, and arthropod species have been reported to be linked to the tandemly repeated units of the rDNA, trans-spliced leader, and histone multigene families. The evolution of these gene arrangements is analyzed by mapping them to independently derived phylogenies. These analyses show that 5S rRNA genes have repeatedly become linked to diverse tandemly repeated gene families and that such linkages have also been subsequently inverted or lost in some species. These variable gene linkages are probably the result of stochastic gains and losses of variant repeat units, where functional 5S rRNA had transposed, by the mechanisms which are responsible for the concerted evolution of tandemly repeated multigene families. We discuss the possible mechanisms of 5S rRNA gene transposition and suggest that the characteristics of their promoter elements, transcription, and termination signals may allow functional copies of these genes to be fortuitously transposed through an RNA intermediate. We also review the evidence which shows that the linked 5S rRNA gene copies are transcribed. We conclude that the observed patterns of 5S rRNA gene linkages to the repeat units of other tandemly repeated multigene families have likely arisen due to fortuitous recombination events and are unlikely to represent the remnants of an eubacterial-like arrangement of rDNA operons or to have been established due to selective pressures.

Evolutionary Dynamics of rDNA Clusters in Chromosomes of Five Clam Species Belonging to the Family Veneridae (Mollusca, Bivalvia)

“…Additionally, the occurrence of alternate 5S and major rDNA signals on extended chromatin fibers of R. decussatus suggests that these sequences are intercalated. Our results showing the existence of linkage between major and 5S rDNA sequences in R. decussatus but not in its congeneric species, R. philippinarum , or in any of the other species within the subfamily Tapetinae, Polititapes aureus , Venerupis corrugata, and P. rhomboides, support the suggestion that 5S and major rRNA gene linkages have been repeatedly established and lost during the evolution of eukaryotic genomes [1, 2]. These data are also in agreement with previous results reported in a wide analysis of metazoan genomes [32] in which, though 5S rDNA was found to be linked to various noncoding RNA genes in several clades, no evidence of evolutionary-conserved linkage among them was detected.…”

“…Minor rDNA repeats consist of a sequence which codes for the 5S rRNA and a nontranscribed spacer (NTS). Although in most eukaryotes in which the organization of these genes is known the two types of rDNAs are located on different chromosome pairs, an increasing number of studies have reported the existence of clusters of both major and minor rRNA genes mapping to the same chromosomal position in many species [1, 2]. Furthermore, the changes in both number and chromosomal position of the rDNA clusters have helped to solve some uncertainties in the phylogenies of some groups of organisms [3, 4].…”

Karyotypic diversification in Mytilus mussels (Bivalvia: Mytilidae) inferred from chromosomal mapping of rRNA and histone gene clusters

“…Therefore, the interspersed organization of linker histone genes and 5S rDNA described here is the first report of such an association in a marine organism. Given that 5S rRNA and linker histone genes are transcribed by different RNA polymerases, this linkage does not suppose any obvious functional advantage [36] and may represent another example of the reported invasion of different tandemly repeated gene families by 5S rRNA genes through transposition events [37]. …”

The nucleolus: a raft adrift in the nuclear sea or the keystone in nuclear structure?

“…Aside from RNAP I transcription, RNAP II transcription appears to be widespread in eukaryote rDNA (27, 51–55). Furthermore, RNAP III-transcribed 5S rDNA genes are located within the rDNA repeat in several species, including yeast (Figure 1; (56)). Moreover, around thirty s mall i nterspersed n uclear e lement (SINE) retrotransposons that derive from RNAP III-transcribed genes are found scattered throughout the human rDNA intergenic spacer (57).…”

“…crustaceans, and dinoflagellates), or entirely linearly dispersed ( e.g. Neurospora crassa and Schizosaccharomyces pombe ) (56, 65–70). However, these differences in the linear organization of the 5S genes between species belie commonalities in their spatial localization.…”