Ribosomal intergenic spacers are filled with transposon remnants

Abstract

Eukaryotic ribosomal DNA (rDNA) comprises tandem units of highly-conserved coding genes separated by rapidly-evolving spacer DNA. The spacers of all 12 species examined were filled with short direct repeats (DRs) and multiple long tandem repeats (TRs), completing the rDNA maps that previously contained unannotated and inadequately studied sequences. The external transcribed spacers also were filled with DRs and some contained TRs. We infer that the spacers arose from transposon insertion, followed by their imprecise excision, leaving short DRs characteristic of transposon visitation. The spacers provided a favored location for transposon insertion because they occupy loci containing hundreds to thousands of gene repeats. The spacers primary cellular function may be to link one rRNA transcription unit to the next, whereas transposons flourish here because they have colonized the most frequently-used part of the genome. Author SummaryThe DNA loci containing the ribosomal RNA genes (the rDNA) in eukaryotes are puzzling. The sections encoding the rRNA are so highly conserved that they can be used to assess evolutionary relationships among diverse eukaryotes, yet the rDNA sequences between the rRNA genes (the intergenic spacer sequences; IGS) are among the most rapidly evolving in the genome, including varying within and between species and between individuals of a species, and within cells of an individual. Here we report the presence of large numbers of direct repeats (DRs) throughout the IGSs of a diverse set of organisms. Parasitic DNA and RNA elements often leave short DRs when they are excised resulting in "molecular scars" in the DNA. These "scars" are absent from the coding sections of the rDNA repeats, indicating that the IGSs have long been targets for integration of these parasitic elements that have been eliminated from the coding sections by selection. While these integration events are mostly detrimental to the organism, occasionally they have caused beneficial changes in eukaryotes, thus allowing both the parasites and the hosts to survive and co-evolve.