A large proportion of functional sequence within mammalian genomes falls outside protein-coding exons and can be transcribed into long RNAs. However, the roles in mammalian biology of long noncoding RNA (lncRNA) are not well understood. Few lncRNAs have experimentally determined roles, with some of these being lineage-specific. Determining the extent by which transcription of lncRNA loci is retained or lost across multiple evolutionary lineages is essential if we are to understand their contribution to mammalian biology and to lineage-specific traits. Here, we experimentally investigated the conservation of lncRNA expression among closely related rodent species, allowing the evolution of DNA sequence to be uncoupled from evolution of transcript expression. We generated total RNA (RNAseq) and H3K4me3-bound (ChIPseq) DNA data, and combined both to construct catalogues of transcripts expressed in the adult liver of Mus musculus domesticus (C57BL/6J), Mus musculus castaneus, and Rattus norvegicus. We estimated the rate of transcriptional turnover of lncRNAs and investigated the effects of their lineage-specific birth or death. LncRNA transcription showed considerably greater gain and loss during rodent evolution, compared with protein-coding genes. Nucleotide substitution rates were found to mirror the in vivo transcriptional conservation of intergenic lncRNAs between rodents: only the sequences of noncoding loci with conserved transcription were constrained. Finally, we found that lineage-specific intergenic lncRNAs appear to be associated with modestly elevated expression of genomically neighbouring protein-coding genes. Our findings show that nearly half of intergenic lncRNA loci have been gained or lost since the last common ancestor of mouse and rat, and they predict that such rapid transcriptional turnover contributes to the evolution of tissue - and lineage-specific gene expression.
Vyšlo v časopise: Rapid Turnover of Long Noncoding RNAs and the Evolution of Gene Expression. PLoS Genet 8(7): e32767. doi:10.1371/journal.pgen.1002841 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002841
1. BertonePStolcVRoyceTERozowskyJSUrbanAE 2004 Global identification of human transcribed sequences with genome tiling arrays. Science 306 2242 2246
2. CarninciPKasukawaTKatayamaSGoughJFrithMC 2005 The transcriptional landscape of the mammalian genome. Science 309 1559 1563
3. CloonanNForrestARKolleGGardinerBBFaulknerGJ 2008 Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 5 613 619
4. OkazakiYFurunoMKasukawaTAdachiJBonoH 2002 Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs. Nature 420 563 573
5. GuttmanMAmitIGarberMFrenchCLinMF 2009 Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458 223 227
6. MercerTRDingerMEMattickJS 2009 Long non-coding RNAs: insights into functions. Nat Rev Genet 10 155 159
7. KatayamaSTomaruYKasukawaTWakiKNakanishiM 2005 Antisense transcription in the mammalian transcriptome. Science 309 1564 1566
8. EngstromPGSuzukiHNinomiyaNAkalinASessaL 2006 Complex Loci in human and mouse genomes. PLoS Genet 2 e47 doi:10.1371/journal.pgen.0020047
9. PontingCPOliverPLReikW 2009 Evolution and functions of long noncoding RNAs. Cell 136 629 641
10. WangKCChangHY 2011 Molecular mechanisms of long noncoding RNAs. Mol Cell 43 904 914
11. HuarteMGuttmanMFeldserDGarberMKoziolMJ 2010 A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142 409 419
12. PonjavicJOliverPLLunterGPontingCP 2009 Genomic and transcriptional co-localization of protein-coding and long non-coding RNA pairs in the developing brain. PLoS Genet 5 e1000617 doi:10.1371/journal.pgen.1000617
13. OromUADerrienTBeringerMGumireddyKGardiniA 2010 Long noncoding RNAs with enhancer-like function in human cells. Cell 143 46 58
14. RinnJLKerteszMWangJKSquazzoSLXuX 2007 Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129 1311 1323
15. WangKCYangYWLiuBSanyalACorces-ZimmermanR 2011 A long noncoding RNA maintains active chromatin to coordinate homeotic gene expression. Nature 472 120 124
16. GuttmanMDonagheyJCareyBWGarberMGrenierJK 2011 lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477 295 300
17. PonjavicJPontingCPLunterG 2007 Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17 556 565
18. MarquesACPontingCP 2009 Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol 10 R124
19. MeaderSPontingCPLunterG 2010 Massive turnover of functional sequence in human and other mammalian genomes. Genome Res 20 1335 1343
20. KutterCBrownGDGoncalvesAWilsonMDWattS 2011 Pol III binding in six mammals shows conservation among amino acid isotypes despite divergence among tRNA genes. Nat Genet 43 948 955
21. BarrettRDHoekstraHE 2011 Molecular spandrels: tests of adaptation at the genetic level. Nat Rev Genet 12 767 780
22. ChurchDMGoodstadtLHillierLWZodyMCGoldsteinS 2009 Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 7 e1000112 doi:10.1371/journal.pbio.1000112
23. CabiliMNTrapnellCGoffLKoziolMTazon-VegaB 2011 Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25 1915 1927
24. ChodroffRAGoodstadtLSireyTMOliverPLDaviesKE 2010 Long noncoding RNA genes: conservation of sequence and brain expression among diverse amniotes. Genome Biol 11 R72
25. TrapnellCPachterLSalzbergSL 2009 TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25 1105 1111
26. KapranovPSt LaurentGRazTOzsolakFReynoldsCP 2010 The majority of total nuclear-encoded non-ribosomal RNA in a human cell is ‘dark matter’ un-annotated RNA. BMC Biol 8 149
27. TrapnellCWilliamsBAPerteaGMortazaviAKwanG 2010 Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28 511 515
28. Santos-RosaHSchneiderRBannisterAJSherriffJBernsteinBE 2002 Active genes are tri-methylated at K4 of histone H3. Nature 419 407 411
29. ZhangYLiuTMeyerCAEeckhouteJJohnsonDS 2008 Model-based analysis of ChIP-Seq (MACS). Genome Biol 9 R137
30. CoreLJWaterfallJJLisJT 2008 Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322 1845 1848
31. WeiWPelechanoVJarvelinAISteinmetzLM 2011 Functional consequences of bidirectional promoters. Trends Genet 27 267 276
32. KongLZhangYYeZQLiuXQZhaoSQ 2007 CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35 W345 349
33. GuttmanMGarberMLevinJZDonagheyJRobinsonJ 2010 Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 28 503 510
34. LeeJTDavidowLSWarshawskyD 1999 Tsix, a gene antisense to Xist at the X-inactivation centre. Nat Genet 21 400 404
35. ChanETQuonGTChuaGBabakTTrochessetM 2009 Conservation of core gene expression in vertebrate tissues. J Biol 8 33.31 .17
36. PauliARinnJLSchierAF 2011 Non-coding RNAs as regulators of embryogenesis. Nat Rev Genet 12 136 149
37. LiTHuangJJiangYZengYHeF 2009 Multi-stage analysis of gene expression and transcription regulation in C57/B6 mouse liver development. Genomics 93 235 242
38. DouzeryEJDelsucFStanhopeMJHuchonD 2003 Local molecular clocks in three nuclear genes: divergence times for rodents and other mammals and incompatibility among fossil calibrations. J Mol Evol 57 S201 213
39. SuAIWiltshireTBatalovSLappHChingKA 2004 A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 101 6062 6067
40. MurphyWJPringleTHCriderTASpringerMSMillerW 2007 Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 17 413 421
41. BrawandDSoumillonMNecsuleaAJulienPCsardiG 2011 The evolution of gene expression levels in mammalian organs. Nature 478 343 348
42. SchwartzSKentWJSmitAZhangZBaertschR 2003 Human-mouse alignments with BLASTZ. Genome Res 13 103 107
43. ChiaromonteFYapVBMillerW 2002 Scoring pairwise genomic sequence alignments. Pac Symp Biocomput 115 126
44. LunterGPontingCPHeinJ 2006 Genome-wide identification of human functional DNA using a neutral indel model. PLoS Comput Biol 2 e5 doi:10.1371/journal.pcbi.0020005
45. KhalilAMGuttmanMHuarteMGarberMRajA 2009 Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci U S A 106 11667 11672
46. DennisGJrShermanBTHosackDAYangJGaoW 2003 DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4 P3
47. de JongeHJFehrmannRSde BontESHofstraRMGerbensF 2007 Evidence based selection of housekeeping genes. PLoS ONE 2 e898 doi:10.1371/journal.pone.0000898
48. FlicekPAmodeMRBarrellDBealKBrentS 2011 Ensembl 2011. Nucleic Acids Res 39 D800 806
49. EbisuyaMYamamotoTNakajimaMNishidaE 2008 Ripples from neighbouring transcription. Nat Cell Biol 10 1106 1113
50. LercherMJUrrutiaAOHurstLD 2002 Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat Genet 31 180 183
51. SchmidtDSchwaliePCWilsonMDBallesterBGoncalvesA 2012 Waves of retrotransposon expansion remodel genome organization and CTCF binding in multiple mammalian lineages. Cell 148 335 348
52. LingGSugathanAMazorTFraenkelEWaxmanDJ 2010 Unbiased, genome-wide in vivo mapping of transcriptional regulatory elements reveals sex differences in chromatin structure associated with sex-specific liver gene expression. Mol Cell Biol 30 5531 5544
53. BlouinABolenderRPWeibelER 1977 Distribution of organelles and membranes between hepatocytes and nonhepatocytes in the rat liver parenchyma. A stereological study. J Cell Biol 72 441 455
54. BourqueGLeongBVegaVBChenXLeeYL 2008 Evolution of the mammalian transcription factor binding repertoire via transposable elements. Genome Res 18 1752 1762
55. KunarsoGChiaNYJeyakaniJHwangCLuX 2010 Transposable elements have rewired the core regulatory network of human embryonic stem cells. Nat Genet 42 631 634
56. SchmidtDWilsonMDBallesterBSchwaliePCBrownGD 2010 Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 328 1036 1040
57. SchmidtDWilsonMDSpyrouCBrownGDHadfieldJ 2009 ChIP-seq: using high-throughput sequencing to discover protein-DNA interactions. Methods 48 240 248
58. KimuraHHayashi-TakanakaYGotoYTakizawaNNozakiN 2008 The organization of histone H3 modifications as revealed by a panel of specific monoclonal antibodies. Cell Struct Funct 33 61 73
59. ParkhomchukDBorodinaTAmstislavskiyVBanaruMHallenL 2009 Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 37 e123
60. LiHRuanJDurbinR 2008 Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18 1851 1858
61. BergerMFBadisGGehrkeARTalukderSPhilippakisAA 2008 Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133 1266 1276
62. GiardineBRiemerCHardisonRCBurhansRElnitskiL 2005 Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15 1451 1455
63. YeTKrebsARChoukrallahMAKeimeCPlewniakF 2011 seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res 39 e35
64. YangZ 1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555 556
65. RobinsonMDOshlackA 2010 A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11 R25
66. R Development Core Team 2011 R: A Language and Environment for Statistical Computing Vienna, Austria
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