Academic journal article Genetics

Genomewide Analysis of Box C/D and Box H/ACA snoRNAs in Chlamydomonas Reinhardtii Reveals an Extensive Organization into Intronic Gene Clusters

Academic journal article Genetics

Genomewide Analysis of Box C/D and Box H/ACA snoRNAs in Chlamydomonas Reinhardtii Reveals an Extensive Organization into Intronic Gene Clusters

Article excerpt

ABSTRACT

Chlamydomonas reinhardtii is a unicellular green alga, the lineage of which diverged from that of land plants >1 billion years ago. Using the powerful small nucleolar RNA (snoRNA) mining platform to screen the C. reinhardtii genome, we identified 322 snoRNA genes grouped into 118 families. The 74 box C/D families can potentially guide methylation at 96 sites of ribosomal RNAs (rRNAs) and snRNAs, and the 44 box H/ACA families can potentially guide pseudouridylation at 62 sites. Remarkably, 242 of the snoRNA genes are arranged into 76 clusters, of which 77% consist of homologous genes produced by small local tandem duplications. At least 70 snoRNA gene clusters are found within introns of protein-coding genes. Although not exhaustive, this analysis reveals that C. reinhardtii has the highest number of intronic snoRNA gene clusters among eukaryotes. The prevalence of intronic snoRNA gene clusters in C. reinhardtii is similar to that of rice but in contrast with the one-snoRNA-per-intron organization of vertebrates and fungi and with that of Arabidopsis thaliana in which only a few intronic snoRNA gene clusters were identified. This analysis of C. reinhardtii snoRNA gene organization shows the functional importance of introns in a single-celled organism and provides evolutionary insight into the origin of intron-encoded RNAs in the plant lineage.

SMALL nucleolar RNAs (snoRNA) are one of the largest classes of noncoding RNAs in eukaryotes. They play an essential role in ribosomal RNAs (rRNA) biosynthesis (Maxwell and Fournier 1995). A small fraction of snoRNAs such as U3, U8, U14, U22, U17, and RNaseMRPRNAare involved in the cleavage of pre-rRNAs (Venema and Tollervey 1999). However,most of them guide the 2'-O-ribose methylation and pseudouridylation of rRNAs (Smith and Steitz 1997). On the basis of common sequence motifs and structural features, all snoRNAs except RNase MRP fall into two families: box C/D snoRNAs and box H/ACA snoRNAs, which guide site-specific 2'-O-ribose methylations and pseudouridylations of rRNAs, respectively, via base complementarity (Balakin et al. 1996;Bachellerie et al. 2000;Kiss 2001). The boxC/DsnoRNAs display two conservedmotifs, the 5'-end C box (5'-RUGAUGA-3') and the 3'-end D box (5'-CUGA-3'), usually flanked by short inverted repeats. In addition to theHbox (ANANNA) in the hinge region andanACAmotif 3nucleotides upstreamof the3'-end of the molecule, boxH/ACAsnoRNAsare characterized by a common hairpin-hinge-hairpin-tail secondary structure (Ganot et al. 1997; Ni et al. 1997). The spectrum of snoRNA targets is continuously growing. They are now known to guide post-transcriptional modifications of snRNAs (Tycowski et al. 1998; Zhou et al. 2002) and tRNAs (Clouet d'Orval et al. 2001; Zemann et al. 2006), as well as the alternative splicing of a pre-mRNA (Cavaille et al. 2000;Kishore and Stamm2006). Furthermore, some ''orphan'' snoRNAs with no obvious target of rRNAs and snRNAs have also been reported (Huttenhofer et al. 2001; Chen et al. 2003).

The genomic organization of snoRNA genes displays a great diversity in various organisms. In human, almost all of the snoRNAs are encoded by single genes nested within introns and maturated by a splicing-dependent processing (Tycowski et al. 1993; Kiss and Filipowicz 1995; Bachellerie et al. 2000). A few of them are transcribed independently with their own promoter. In the intron-poor genome of Saccharomyces cerevisiae, only a few of the snoRNA genes are intronic. The majority of the snoRNAs are encoded by single genes, but 17 (20%) snoRNAs are encoded in five gene clusters each driven by an upstream promoter (Lowe and Eddy 1999; Qu et al. 1999). In contrast, snoRNA gene clusters dominate in the plant lineage. More than 80% of the snoRNA genes of Arabidopsis thaliana and Oryza sativa are organized into gene clusters (Leader et al. 1997; Brown et al. 2003a; Chen et al. 2003). Four intronic snoRNA gene clusters were found in A. …

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