Finely Orchestrated Movements: Evolution of the Ribosomal RNA Genes

Abstract

Evolution of the tandemly repeated ribosomal RNA (rRNA) genes is intriguing because in each species all units within the array are highly uniform in sequence but that sequence differs between species. In this review we summarize the origins of the current models to explain this process of concerted evolution, emphasizing early studies of recombination in yeast and more recent studies in Drosophila and mammalian systems. These studies suggest that unequal crossover is the major driving force in the evolution of the rRNA genes with sister chromatid exchange occurring more often than exchange between homologs. Gene conversion is also believed to play a role; however, direct evidence for its involvement has not been obtained. Remarkably, concerted evolution is so well orchestrated that even transposable elements that insert into a large fraction of the rRNA genes appear to have little effect on the process. Finally, we summarize data that suggest that recombination in the rDNA locus of higher eukaryotes is sufficiently frequent to monitor changes within a few generations.

Investigating the diversity of the 18S SSU rRNA hyper-variable region of Theileria in cattle and Cape buffalo (Syncerus caffer) from southern Africa using a next generation sequencing approach

“…There is therefore no reason to postulate that the extensive genetic diversity observed is due to more than two 18S rRNA copies, as found in Babesia and Plasmodium (Gunderson et al 1987;Lau, 2009;Laughery et al 2009). The two gene copies are also conserved due to concerted evolution (Eickbush and Eickbush, 2007). If the genotypes existed as multiple genes in the genome, they should be co-detected in samples and their quantitative ratio relative to each other would represent their gene copy number.…”

R2 dynamics in Triops cancriformis (Bosc, 1801) (Crustacea, Branchiopoda, Notostraca): turnover rate and 28S concerted evolution

“…Sequence specificity of insertion is considered an ancient strategy used by transposable elements to survive in the host genome by limiting their ability to disrupt essential genes . Ribosomal DNA represents a niche well exploited by non-LTR retrotransposons, and eight rDNA-specific families have been so far identified, with six of them inserting into the 28S gene (R1, R2, R4, R5, R6, RT; Eickbush and Eickbush, 2007).…”

“…In Drosophila simulans, in particular, a high turnover rate, together with transposition-mediated deletions, is responsible of the elimination of earlier generated truncation variants (Zhang et al, 2008). Moreover, the selective pressure against non-functional rDNA units tends to eliminate the R2-inserted copies through the unequal DNA exchanges acting in the concerted evolution of the ribosomal locus (reviewed in Nei and Rooney, 2005;Eickbush and Eickbush, 2007). Concerted evolution explains the variability pattern observed for repeated sequence families (such as ribosomal genes): the observed sequence variability within an evolutionary unit (a species, a subspecies or a population) is significantly lower than between different evolutionary units of the same rank.…”

Intragenomic polymorphism and intergenomic recombination in the ribosomal RNA genes of strains belonging to a yeast speciesPichia membranifaciens

“…It is generally believed that all the copies of the rRNA unit are identical or nearly identical in nucleotide sequence within the genome of a given organism because of the highly stringent functional constraints on rRNA molecules (Long and Dawid 1980; Hillis and Dixon 1991). A “concerted evolution” model has been proposed to explain the observed lack of sequence variation among rRNA gene copies in many different species (Zimmer et al 1980; Coen et al 1982; Liao 1999, 2000; Eickbush and Eickbush 2007). …”

“…Compared to the tandem-arrayed organisation of eukaryotic rRNA genes in high copy number (generally over 100; in some cases >1000), prokaryotic rRNA genes are generally dispersed throughout a genome in limited copy numbers (generally <10) (Liao 2000). Since the concerted evolution theory has been proposed mainly based on sequence homogeneity in tandemly repeated multigene families (Eickbush and Eickbush 2007), the findings of intragenomic rRNA gene polymorphisms in eukaryotes are more challenging.…”