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Comparative analysis of the transcriptome across distant species.

ABSTRACT: The transcriptome is the readout of the genome. Identifying common features in it across distant species can reveal fundamental principles. To this end, the ENCODE and modENCODE consortia have generated large amounts of matched RNA-sequencing data for human, worm and fly. Uniform processing and comprehensive annotation of these data allow comparison across metazoan phyla, extending beyond earlier within-phylum transcriptome comparisons and revealing ancient, conserved features. Specifically, we discover co-expression modules shared across animals, many of which are enriched in developmental genes. Moreover, we use expression patterns to align the stages in worm and fly development and find a novel pairing between worm embryo and fly pupae, in addition to the embryo-to-embryo and larvae-to-larvae pairings. Furthermore, we find that the extent of non-canonical, non-coding transcription is similar in each organism, per base pair. Finally, we find in all three organisms that the gene-expression levels, both coding and non-coding, can be quantitatively predicted from chromatin features at the promoter using a 'universal model' based on a single set of organism-independent parameters.

SUBMITTER: Gerstein MB

PROVIDER: S-EPMC4155737 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

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Comparative analysis of the transcriptome across distant species.

Gerstein Mark B MB Rozowsky Joel J Yan Koon-Kiu KK Wang Daifeng D Cheng Chao C Brown James B JB Davis Carrie A CA Hillier LaDeana L Sisu Cristina C Li Jingyi Jessica JJ Pei Baikang B Harmanci Arif O AO Duff Michael O MO Djebali Sarah S Alexander Roger P RP Alver Burak H BH Auerbach Raymond R Bell Kimberly K Bickel Peter J PJ Boeck Max E ME Boley Nathan P NP Booth Benjamin W BW Cherbas Lucy L Cherbas Peter P Di Chao C Dobin Alex A Drenkow Jorg J Ewing Brent B Fang Gang G Fastuca Megan M Feingold Elise A EA Frankish Adam A Gao Guanjun G Good Peter J PJ Guigó Roderic R Hammonds Ann A Harrow Jen J Hoskins Roger A RA Howald Cédric C Hu Long L Huang Haiyan H Hubbard Tim J P TJ Huynh Chau C Jha Sonali S Kasper Dionna D Kato Masaomi M Kaufman Thomas C TC Kitchen Robert R RR Ladewig Erik E Lagarde Julien J Lai Eric E Leng Jing J Lu Zhi Z MacCoss Michael M May Gemma G McWhirter Rebecca R Merrihew Gennifer G Miller David M DM Mortazavi Ali A Murad Rabi R Oliver Brian B Olson Sara S Park Peter J PJ Pazin Michael J MJ Perrimon Norbert N Pervouchine Dmitri D Reinke Valerie V Reymond Alexandre A Robinson Garrett G Samsonova Anastasia A Saunders Gary I GI Schlesinger Felix F Sethi Anurag A Slack Frank J FJ Spencer William C WC Stoiber Marcus H MH Strasbourger Pnina P Tanzer Andrea A Thompson Owen A OA Wan Kenneth H KH Wang Guilin G Wang Huaien H Watkins Kathie L KL Wen Jiayu J Wen Kejia K Xue Chenghai C Yang Li L Yip Kevin K Zaleski Chris C Zhang Yan Y Zheng Henry H Brenner Steven E SE Graveley Brenton R BR Celniker Susan E SE Gingeras Thomas R TR Waterston Robert R

Nature 20140801 7515

The transcriptome is the readout of the genome. Identifying common features in it across distant species can reveal fundamental principles. To this end, the ENCODE and modENCODE consortia have generated large amounts of matched RNA-sequencing data for human, worm and fly. Uniform processing and comprehensive annotation of these data allow comparison across metazoan phyla, extending beyond earlier within-phylum transcriptome comparisons and revealing ancient, conserved features. Specifically, we ...[more]

PMID: 25164755

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Project description:BackgroundDefining the transcriptome and the genetic pathways of pancreatic cells is of great interest for elucidating the molecular attributes of pancreas disorders such as diabetes and cancer. As the function of the different pancreatic cell types has been maintained during vertebrate evolution, the comparison of their transcriptomes across distant vertebrate species is a means to pinpoint genes under strong evolutionary constraints due to their crucial function, which have therefore preserved their selective expression in these pancreatic cell types.ResultsIn this study, RNA-sequencing was performed on pancreatic alpha, beta, and delta endocrine cells as well as the acinar and ductal exocrine cells isolated from adult zebrafish transgenic lines. Comparison of these transcriptomes identified many novel markers, including transcription factors and signaling pathway components, specific for each cell type. By performing interspecies comparisons, we identified hundreds of genes with conserved enriched expression in endocrine and exocrine cells among human, mouse, and zebrafish. This list includes many genes known as crucial for pancreatic cell formation or function, but also pinpoints many factors whose pancreatic function is still unknown. A large set of endocrine-enriched genes can already be detected at early developmental stages as revealed by the transcriptomic profiling of embryonic endocrine cells, indicating a potential role in cell differentiation. The actual involvement of conserved endocrine genes in pancreatic cell differentiation was demonstrated in zebrafish for myt1b, whose invalidation leads to a reduction of alpha cells, and for cdx4, selectively expressed in endocrine delta cells and crucial for their specification. Intriguingly, comparison of the endocrine alpha and beta cell subtypes from human, mouse, and zebrafish reveals a much lower conservation of the transcriptomic signatures for these two endocrine cell subtypes compared to the signatures of pan-endocrine and exocrine cells. These data suggest that the identity of the alpha and beta cells relies on a few key factors, corroborating numerous examples of inter-conversion between these two endocrine cell subtypes.ConclusionThis study highlights both evolutionary conserved and species-specific features that will help to unveil universal and fundamental regulatory pathways as well as pathways specific to human and laboratory animal models such as mouse and zebrafish.

Project description:BACKGROUND: Planarians are considered to be among the extant animals close to one of the earliest groups of organisms that acquired a central nervous system (CNS) during evolution. Planarians have a bilobed brain with nine lateral branches from which a variety of external signals are projected into different portions of the main lobes. Various interneurons process different signals to regulate behavior and learning/memory. Furthermore, planarians have robust regenerative ability and are attracting attention as a new model organism for the study of regeneration. Here we conducted large-scale EST analysis of the head region of the planarian Dugesia japonica to construct a database of the head-region transcriptome, and then performed comparative analyses among related species. RESULTS: A total of 54,752 high-quality EST reads were obtained from a head library of the planarian Dugesia japonica, and 13,167 unigene sequences were produced by de novo assembly. A new method devised here revealed that proteins related to metabolism and defense mechanisms have high flexibility of amino-acid substitutions within the planarian family. Eight-two CNS-development genes were found in the planarian (cf. C. elegans 3; chicken 129). Comparative analysis revealed that 91% of the planarian CNS-development genes could be mapped onto the schistosome genome, but one-third of these shared genes were not expressed in the schistosome. CONCLUSIONS: We constructed a database that is a useful resource for comparative planarian transcriptome studies. Analysis comparing homologous genes between two planarian species showed that the potential of genes is important for accumulation of amino-acid substitutions. The presence of many CNS-development genes in our database supports the notion that the planarian has a fundamental brain with regard to evolution and development at not only the morphological/functional, but also the genomic, level. In addition, our results indicate that the planarian CNS-development genes already existed before the divergence of planarians and schistosomes from their common ancestor.

Project description:The Lolium-Festuca complex incorporates species from the Lolium genera and the broad leaf fescues, both belonging to the subfamily Pooideae. This subfamily also includes wheat, barley, oat and rye, making it extremely important to world agriculture. Species within the Lolium-Festuca complex show very diverse phenotypes, and many of them are related to agronomically important traits. Analysis of sequenced transcriptomes of these non-model species may shed light on the molecular mechanisms underlying this phenotypic diversity.We have generated de novo transcriptome assemblies for four species from the Lolium-Festuca complex, ranging from 52,166 to 72,133 transcripts per assembly. We have also predicted a set of proteins and validated it with a high-confidence protein database from three closely related species (H. vulgare, B. distachyon and O. sativa). We have obtained gene family clusters for the four species using OrthoMCL and analyzed their inferred phylogenetic relationships. Our results indicate that VRN2 is a candidate gene for differentiating vernalization and non-vernalization types in the Lolium-Festuca complex. Grouping of the gene families based on their BLAST identity enabled us to divide ortholog groups into those that are very conserved and those that are more evolutionarily relaxed. The ratio of the non-synonumous to synonymous substitutions enabled us to pinpoint protein sequences evolving in response to positive selection. These proteins may explain some of the differences between the more stress tolerant Festuca, and the less stress tolerant Lolium species.Our data presents a comprehensive transcriptome sequence comparison between species from the Lolium-Festuca complex, with the identification of potential candidate genes underlying some important phenotypical differences within the complex (such as VRN2). The orthologous genes between the species have a very high %id (91,61%) and the majority of gene families were shared for all of them. It is likely that the knowledge of the genomes will be largely transferable between species within the complex.

Dataset Information

Comparative analysis of the transcriptome across distant species.

Publications

Comparative analysis of the transcriptome across distant species.

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