Evolution of small nuclear RNAs in S. cerevisiae, C. albicans, and other hemiascomycetous yeasts

Abstract

The spliceosome is a large, dynamic ribonuclear protein complex, required for the removal of intron sequences from newly synthesized eukaryotic RNAs. The spliceosome contains five essential small nuclear RNAs (snRNAs): U1, U2, U4, U5, and U6. Phylogenetic comparisons of snRNAs from protists to mammals have long demonstrated remarkable conservation in both primary sequence and secondary structure. In contrast, the snRNAs of the hemiascomycetous yeast Saccharomyces cerevisiae have highly unusual features that set them apart from the snRNAs of other eukaryotes. With an emphasis on the pathogenic yeast Candida albicans, we have now identified and compared snRNAs from newly sequenced yeast genomes, providing a perspective on spliceosome evolution within the hemiascomycetes. In addition to tracing the origins of previously identified snRNA variations present in Saccharomyces cerevisiae, we have found numerous unexpected changes occurring throughout the hemiascomycetous lineages. Our observations reveal interesting examples of RNA and protein coevolution, giving rise to altered interaction domains, losses of deeply conserved snRNA-binding proteins, and unique snRNA sequence changes within the catalytic center of the spliceosome. These same yeast lineages have experienced exceptionally high rates of intron loss, such that modern hemiascomycetous genomes contain introns in only ;5% of their genes. Also, the splice site sequences of those introns that remain adhere to an unusually strict consensus. Some of the snRNA variations we observe may thus reflect the altered intron landscape with which the hemiascomycetous spliceosome must contend.

Evolutionarily divergent spliceosomal snRNAs and a conserved non-coding RNA processing motif in Giardia lamblia

“…This contrasts to the previously identified U1 candidate (24) that has an atypical predicted secondary structure lacking a recognisable U1A binding site (compare Figure 4A and Supplementary Figure S8). We mapped the 3′ end of the new U1 RNA candidate as directly downstream of the predicted Sm site, similar to the C andida albicans U1 snRNA, which also lacks the SL IV structure (43) that is commonly found in the U1 RNAs of other eukaryotes (Figures 4A and 5A). Another noteworthy feature of the Giardia U1 RNA is the lack of a conserved U1-70 kDa protein binding site sequence in SL I.…”

Ribosomal RNA processing in Candida albicans

“…However, comparative studies with other fungi including C. albicans reveal variations that suggest S. cerevisiae to be atypical. For instance, splicesomal RNA domains defined as ''fungal-specific'' in U2 and U5 RNAs are actually unique to Saccharomyces spp (Mitrovich and Guthrie 2007). On the other hand, the NME1 RNA in C. albicans is unusually long when compared with other fungi and metazoans (Piccinelli et al 2005).…”

Evolution of Spliceosomal snRNA Genes in Metazoan Animals

“…These structures have received substantial interest in the past, as explified by the following non-exhaustive list of references covering a diverse set of animal species: Homo sapiens U1 [54], U2 [25], U4 [37], U5 [6,79], U6 [25], U11 [66,51,82], U12 [66,51,82] and U4atac [72], Rattus norvegicus U1 [37], U4 [37], U5 [37], Gallus gallus U4 [37], U5 [6], Xenopus laevis U1 [18], U2 [47], Caenorhabditis elegans U1, U2, U5, U4/U6 [84], Drosophila melanogaster U1 [54,56], U2 [56], U4 [56], U5 [56], U4atac/U6atac, U6atac/U12 [59], Bombyx mori U1 [76], U2 [75], Asselus aquaticus U1 [3], Ascaris lumbricoides U1, U2, U5, U4/U6 [70]. Large changes in snRNA structures over evolutionary time were recently reported for hemiascomycetous yeasts [50]. The comprehensive survey of snRNA sequences throughout metazoa set the stage for a comparably detailed analysis of metazoan snRNA structures.…”