Evolution of a large ribosomal RNA multigene family in filamentous fungi: birth and death of a concerted evolution paradigm.

In eukaryotes, the primary components of the ribosome are encoded by multicopy nuclear ribosomal RNA (rRNA) genes: 28/26S, 18S, 5.8S, and 5S. Copies of these genes are typically localized within tandem arrays and homogenized within a genome. As a result, nuclear rRNA gene families have become a paradigm of concerted evolution. In filamentous fungi of the subphylum Pezizomycotina, 5S rRNA genes exist as a large and dispersed multigene family, with between 50 and 100 copies per genome. To determine whether these genes defy the concerted evolution paradigm, we examined the patterns of evolution of these genes by using sequences from the complete genomes of four species. Analyses of these sequences revealed (i) multiple 5S gene types within a genome, (ii) interspecies clustering of gene types, (iii) multiple identical gene types shared among species, (iv) multiple pseudogenes within a genome, and (v) presence/absence variation of individual 5S copies in comparisons of closely related species. These results demonstrate that the 5S family in these species is characterized by birth-and-death evolution under strong purifying selection. Furthermore, our results suggest that birth-and-death evolution occurs at different rates in the genera examined, and that the multiplication and movement of 5S genes across the genome are highly dynamic. As such, we hypothesize that a mechanism resembling retroposition controls 5S rRNA gene amplification, dispersal, and integration in the genomes of filamentous fungi.