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. 2006 May 19;34(9):2676-85.
doi: 10.1093/nar/gkl359. Print 2006.

Evolution of small nucleolar RNAs in nematodes

Anja Zemann  1 , Anja op de Bekke, Martin Kiefmann, Jürgen Brosius, Jürgen Schmitz
Affiliations

Evolution of small nucleolar RNAs in nematodes

Anja Zemann et al. Nucleic Acids Res. .

Abstract

In contrast to mRNAs, which are templates for translating proteins, non-protein coding (npc) RNAs (also known as 'non-coding' RNA, ncRNA), exhibit various functions in different compartments and developmental stages of the cell. Small nucleolar RNAs (snoRNAs), one of the largest classes of npcRNAs, guide post-transcriptional modifications of other RNAs that are crucial for appropriate RNA folding as well as for RNA-RNA and RNA-protein interactions. Although snoRNA genes comprise a significant fraction of the eutherian genome, identifying and characterizing large numbers of them is not sufficiently accessible by classical computer searches alone. Furthermore, most previous investigations of snoRNAs yielded only limited indications of their evolution. Using data obtained by a combination of high-throughput cDNA library screening and computational search strategies based on a modified DNAMAN program, we characterized 151 npcRNAs, and in particular 121 snoRNAs, from Caenorhabditis elegans and extensively compared them with those in the related, Caenorhabditis briggsae. Detailed comparisons of paralog snoRNAs in the two nematodes revealed, in addition to trans-duplication, a novel, cis-duplication distribution strategy with insertions near to the original loci. Some snoRNAs coevolved with their modification _target sites, demonstrating the close interaction of complementary regions. Some _target sites modified by snoRNAs were changed, added or lost, documenting a high degree of evolutionary plasticity of npcRNAs.

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Figures

Figure 1
Figure 1
Grouping of experimentally and computationally identified npcRNAs. (I) Novel npcRNAs and (II) npcRNAs also confirmed recently (23,24). (III) Known snoRNAs (additional snoRNAs experimentally identified by Deng et al. (23) (CeN) or Wachi et al. (24) (CeR), but not revealed in our screen; included for completeness). Our computationally identified snoRNAs were derived from specific search profiles (com) or retrieved via BLAST searches (bl). snoRNAs were subdivided into C/D-box and H/ACA-box snoRNAs and were found in intronic, intergenic or unidentified (not analyzed = na) regions. npcRNAs found in C.elegans (Ce) as well as at orthologous positions in C.briggsae (Cb) are shown in boldface. Asterisks denote verification by northern blot analysis. Owing to the large number of spliceosomal RNA paralogs, we were not able to identify the true orthologs of the respective U1–U6 snRNAs in C.briggsae. RPG, ribosomal protein genes; U1–U6, spliceosomal RNAs; TE, npcRNAs homologous to transposed elements; Others, uncategorized npcRNAs. Additional, known npcRNAs that were experimentally verified and then excluded from further analysis are listed in Supplementary Data. Note: The group of experimentally identified spliceosomal RNAs were also detected (23), but incorrectly classified as already known. Careful examination, however, shows that all of them are novel spliceosomal RNA isoforms.
Figure 2
Figure 2
Possible C/D-box snoRNA modification _targets in tRNAs. The modified nucleotides are circled. Computationally (com) and experimentally identified C.elegans snoRNAs (Ce) correspond to those listed in Figure 1.
Figure 3
Figure 3
snoRNAs and their paralogs in C.elegans and C.briggsae. (a) Compilation of snoRNAs and their paralogs in C.elegans and C.briggsae prior to (base of the tree), and after the two species split (branches). Cis-duplication is shown in boldface, trans-duplication in regular letters. (b) Evolutionary scenario for Ce254 in C.elegans and C.briggsae. This snoRNA trans-duplicated to yield a novel paralog located on a different chromosome in the common ancestor of C.elegans and C.briggsae. After the two species split, both paralogs retained their functionality in both species. Asterisks denote the modified nucleotide of 26S rRNA (top) or the corresponding complementary sequence positions in the snoRNA antisense regions (bottom). Chr II and Chr III indicate the snoRNA location on chromosomes II and III.
Figure 4
Figure 4
Examples of H/ACA-box snoRNAs. Cis-duplication characterized by presence/absence analyses in two or three nematode species (Ce, C.elegans; Cb, C.briggsae; Cr, C.remanei). Protein-coding regions are indicated by thick gray boxes, 5′- and 3′-UTRs are shown as intermediate-sized gray bars and introns as black lines. The framed white areas represent the snoRNAs with their orientation indicated by arrows. (a) Cis-duplication of comCe12 in C.elegans (Ce236) and not in C.briggsae. (b) Cis-duplication of comCe7 in C.elegans (Ce80) but not in C.briggsae or C.remanei. (c) Duplication of comCe14 in C.elegans (comCe15) but not in C.briggsae or C.remanei. Only a partial sequence of C.remanei was available. Several additional snoRNAs exist in neighboring introns of K07C5. Note that in C.elegans, C.briggsae and C.remanei the C/D-box snoRNA comCe4 located in intron 3 occupies the entire intron with the exception of two additional guanosine residues that are part of the functional splice sites.
Figure 5
Figure 5
Trans-duplication of snoRNAs. (a and b) Represent trans-duplication of snoRNAs along with the flanking parts of their host genes. Note, that the outer flanks of the pseudogene sequences are highly diverged or deleted, and thus not alignable to the hypothetical protein genes C06A1.3 or Y53F4B.12. (a) Ce173-1 is diverged in the Ce pseudogene. (c and d) Represent trans-duplication of snoRNAs lacking their original flanking regions. Integration took place in new host genes (shown as light gray boxes and lines). Symbols are analogous to those in Figure 4.
Figure 6
Figure 6
Coevolution of snoRNAs and their _target sites. (a) The antisense region of snoRNA Ce138 differs by one nucleotide compared with Cb138. This change is a response to a base change in 26S rRNA of C.elegans (A→U) compared with 26S rRNA of C.japonica and C.briggsae. (b) A specific change in the 26S rRNA sequence of C.briggsae (A→G) compared with C.japonica and C.elegans is followed by a corresponding complementary change in snoRNA Cb234.2. Numbers above and below sequences denote the nucleotide positions in the 26S rRNAs.
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