A combined computational and experimental analysis of two families of snoRNA genes from Caenorhabditis elegans, revealing the expression and evolution pattern of snoRNAs in nematodes

Small nucleolar RNAs (snoRNAs) are an abundant group of noncoding RNAs mainly involved in the posttranscriptional modifications of rRNAs in eukaryotes. Prior to this study, only 28 snoRNA genes had been identified from Caenorhabditis elegans, indicating that most snoRNA genes are hidden in the worm genome, which represents a simple multicellular metazoan. In this study, a genome-wide analysis of the two major families of snoRNA genes in C. elegans was performed using the snoscan and snoGPS programs incorporating comparative genome analyses. Seventy gene variants, including 36 box C/D and 34 box H/ACA snoRNA genes, were identified, of which 50 are novel. Two families of snoRNAs showed a characteristic genomic organization. Notably, 6 box C/D snoRNA genes were located in the antisense orientation of introns. In contrast to insect and mammal, the distances between many intronic snoRNAs and 3′ splice sites of introns were less than 50 nt in the worm, an unexpected finding as intron-encoded snoRNAs in C. elegans are supposed to be expressed in a splicing-dependent pathway. Interestingly, a canonical H/ACA snoRNA, ΨCeU5-48, was revealed to be partially homologous to small Cajal body-specific RNA (scaRNA) U85 and U89 in fly and human, indicating a possible evolutionary relationship between snoRNAs and scaRNAs.