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Comparative analysis of regulatory information and circuits across distant species.

ABSTRACT: Despite the large evolutionary distances between metazoan species, they can show remarkable commonalities in their biology, and this has helped to establish fly and worm as model organisms for human biology. Although studies of individual elements and factors have explored similarities in gene regulation, a large-scale comparative analysis of basic principles of transcriptional regulatory features is lacking. Here we map the genome-wide binding locations of 165 human, 93 worm and 52 fly transcription regulatory factors, generating a total of 1,019 data sets from diverse cell types, developmental stages, or conditions in the three species, of which 498 (48.9%) are presented here for the first time. We find that structural properties of regulatory networks are remarkably conserved and that orthologous regulatory factor families recognize similar binding motifs in vivo and show some similar co-associations. Our results suggest that gene-regulatory properties previously observed for individual factors are general principles of metazoan regulation that are remarkably well-preserved despite extensive functional divergence of individual network connections. The comparative maps of regulatory circuitry provided here will drive an improved understanding of the regulatory underpinnings of model organism biology and how these relate to human biology, development and disease.

SUBMITTER: Boyle AP

PROVIDER: S-EPMC4336544 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Comparative analysis of regulatory information and circuits across distant species.

Boyle Alan P AP Araya Carlos L CL Brdlik Cathleen C Cayting Philip P Cheng Chao C Cheng Yong Y Gardner Kathryn K Hillier LaDeana W LW Janette Judith J Jiang Lixia L Kasper Dionna D Kawli Trupti T Kheradpour Pouya P Kundaje Anshul A Li Jingyi Jessica JJ Ma Lijia L Niu Wei W Rehm E Jay EJ Rozowsky Joel J Slattery Matthew M Spokony Rebecca R Terrell Robert R Vafeados Dionne D Wang Daifeng D Weisdepp Peter P Wu Yi-Chieh YC Xie Dan D Yan Koon-Kiu KK Feingold Elise A EA Good Peter J PJ Pazin Michael J MJ Huang Haiyan H Bickel Peter J PJ Brenner Steven E SE Reinke Valerie V Waterston Robert H RH Gerstein Mark M White Kevin P KP Kellis Manolis M Snyder Michael M

Nature 20140801 7515

Despite the large evolutionary distances between metazoan species, they can show remarkable commonalities in their biology, and this has helped to establish fly and worm as model organisms for human biology. Although studies of individual elements and factors have explored similarities in gene regulation, a large-scale comparative analysis of basic principles of transcriptional regulatory features is lacking. Here we map the genome-wide binding locations of 165 human, 93 worm and 52 fly transcri ...[more]

PMID: 25164757

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Project description:BACKGROUND: The basic process of RNA splicing is conserved among eukaryotic species. Three signals (5' and 3' splice sites and branch site) are commonly used to directly conduct splicing, while other features are also related to the recognition of an intron. Although there is experimental evidence pointing to the significant species specificities in the features of intron recognition, a quantitative evaluation of the divergence of these features among a wide variety of eukaryotes has yet to be conducted. RESULTS: To better understand the splicing process from the viewpoints of evolution and information theory, we collected introns from 61 diverse species of eukaryotes and analyzed the properties of the nucleotide sequences relevant to splicing. We found that trees individually constructed from the five features (the three signals, intron length, and nucleotide composition within an intron) roughly reflect the phylogenetic relationships among the species but sometimes extensively deviate from the species classification. The degree of topological deviation of each feature tree from the reference trees indicates the lowest discordance for the 5' splicing signal, followed by that for the 3' splicing signal, and a considerably greater discordance for the other three features. We also estimated the relative contributions of the five features to short intron recognition in each species. Again, moderate correlation was observed between the similarities in pattern of short intron recognition and the genealogical relationships among the species. When mammalian introns were categorized into three subtypes according to their terminal dinucleotide sequences, each subtype segregated into a nearly monophyletic group, regardless of the host species, with respect to the 5' and 3' splicing signals. It was also found that GC-AG introns are extraordinarily abundant in some species with high genomic G + C contents, and that the U12-type spliceosome might make a greater contribution than currently estimated in most species. CONCLUSIONS: Overall, the present study indicates that both splicing signals themselves and their relative contributions to short intron recognition are rather susceptible to evolutionary changes, while some poorly characterized properties seem to be preserved within the mammalian intron subtypes. Our findings may afford additional clues to understanding of evolution of splicing mechanisms.

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Comparative analysis of regulatory information and circuits across distant species.

Publications

Comparative analysis of regulatory information and circuits across distant species.

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