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Systematic identification and evolutionary features of rhesus monkey small nucleolar RNAs.

ABSTRACT: BACKGROUND: Recent studies have demonstrated that non-protein-coding RNAs (npcRNAs/ncRNAs) play important roles during eukaryotic development, species evolution, and in the etiology of disease. Rhesus macaques are the most widely used primate model in both biomedical research and primate evolutionary studies. However, most reports on these animals focus on the functional roles of protein-coding sequences, whereas very little is known about macaque ncRNAs. RESULTS: In the present study, we performed the first systematic profiling of intermediate-size ncRNAs (50 to 500 nt) from the rhesus monkey by constructing a cDNA library. We identified 117 rhesus monkey ncRNAs, including 80 small nucleolar RNAs (snoRNAs), 29 other types of known RNAs (snRNAs, Y RNA, and others), and eight unclassified ncRNAs. Comparative genomic analysis and northern blot hybridizations demonstrated that some snoRNAs were lineage- or species-specific. Paralogous sequences were found for most rhesus monkey snoRNAs, the expression of which might be attributable to extensive duplication within the rhesus monkey genome. Further investigation of snoRNA flanking sequences showed that some rhesus monkey snoRNAs are retrogenes derived from L1-mediated integration. Finally, phylogenetic analysis demonstrated that birds and primates share some snoRNAs and host genes thereof, suggesting that both the relevant host genes and the snoRNAs contained therein may be inherited from a common ancestor. However, some rhesus monkey snoRNAs hosted by non-ribosome-related genes appeared after the evolutionary divergence between birds and mammals. CONCLUSIONS: We provide the first experimentally-derived catalog of rhesus monkey ncRNAs and uncover some interesting genomic and evolutionary features. These findings provide important information for future functional characterization of snoRNAs during primate evolution.

SUBMITTER: Zhang Y

PROVIDER: S-EPMC2832892 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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Systematic identification and evolutionary features of rhesus monkey small nucleolar RNAs.

Zhang Yong Y Liu Jun J Jia Chunshi C Li Tingting T Wu Rimao R Wang Jie J Chen Ying Y Zou Xiaoting X Chen Runsheng R Wang Xiu-Jie XJ Zhu Dahai D

BMC genomics 20100125

<h4>Background</h4>Recent studies have demonstrated that non-protein-coding RNAs (npcRNAs/ncRNAs) play important roles during eukaryotic development, species evolution, and in the etiology of disease. Rhesus macaques are the most widely used primate model in both biomedical research and primate evolutionary studies. However, most reports on these animals focus on the functional roles of protein-coding sequences, whereas very little is known about macaque ncRNAs.<h4>Results</h4>In the present stu ...[more]

PMID: 20100322

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Project description:BackgroundSmall nucleolar (sno)RNAs are required for posttranscriptional processing and modification of ribosomal, spliceosomal and messenger RNAs. Their presence in both eukaryotes and archaea indicates that snoRNAs are evolutionarily ancient. The location of some snoRNAs within the introns of ribosomal protein genes has been suggested to belie an RNA world origin, with the exons of the earliest protein-coding genes having evolved around snoRNAs after the advent of templated protein synthesis. Alternatively, this intronic location may reflect more recent selection for coexpression of snoRNAs and ribosomal components, ensuring rRNA modification by snoRNAs during ribosome synthesis. To gain insight into the evolutionary origins of this genetic organization, we examined the antiquity of snoRNA families and the stability of their genomic location across 44 eukaryote genomes.ResultsWe report that dozens of snoRNA families are traceable to the Last Eukaryotic Common Ancestor (LECA), but find only weak similarities between the oldest eukaryotic snoRNAs and archaeal snoRNA-like genes. Moreover, many of these LECA snoRNAs are located within the introns of host genes independently traceable to the LECA. Comparative genomic analyses reveal the intronic location of LECA snoRNAs is not ancestral however, suggesting the pattern we observe is the result of ongoing intragenomic mobility. Analysis of human transcriptome data indicates that the primary requirement for hosting intronic snoRNAs is a broad expression profile. Consistent with ongoing mobility across broadly-expressed genes, we report a case of recent migration of a non-LECA snoRNA from the intron of a ubiquitously expressed non-LECA host gene into the introns of two LECA genes during the evolution of primates.ConclusionsOur analyses show that snoRNAs were a well-established family of RNAs at the time when eukaryotes began to diversify. While many are intronic, this association is not evolutionarily stable across the eukaryote tree; ongoing intragenomic mobility has erased signal of their ancestral gene organization, and neither introns-first nor evolved co-expression adequately explain our results. We therefore present a third model - constrained drift - whereby individual snoRNAs are intragenomically mobile and may occupy any genomic location from which expression satisfies phenotype.

Dataset Information

Systematic identification and evolutionary features of rhesus monkey small nucleolar RNAs.

Publications

Systematic identification and evolutionary features of rhesus monkey small nucleolar RNAs.

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