An integrative atlas of chicken long non-coding genes and their annotations across 25 tissues.

Frédéric Jehl, Kévin Muret, Maria Bernard, Morgane Boutin, Laetitia Lagoutte, Colette Désert, Patrice Dehais, Diane Esquerré, Hervé Acloque, Elisabetta Giuffra, Sarah Djebali, Sylvain Foissac, Thomas Derrien, Frédérique Pitel, Tatiana Zerjal, Christophe Klopp, Sandrine Lagarrigue
Author Information
  1. Frédéric Jehl: PEGASE UMR 1348, INRA, AGROCAMPUS OUEST, 35590, Saint-Gilles, France.
  2. Kévin Muret: PEGASE UMR 1348, INRA, AGROCAMPUS OUEST, 35590, Saint-Gilles, France.
  3. Maria Bernard: SIGENAE Platform, INRA, 31326, Castanet-Tolosan, France.
  4. Morgane Boutin: PEGASE UMR 1348, INRA, AGROCAMPUS OUEST, 35590, Saint-Gilles, France.
  5. Laetitia Lagoutte: PEGASE UMR 1348, INRA, AGROCAMPUS OUEST, 35590, Saint-Gilles, France.
  6. Colette Désert: PEGASE UMR 1348, INRA, AGROCAMPUS OUEST, 35590, Saint-Gilles, France.
  7. Patrice Dehais: SIGENAE Platform, INRA, 31326, Castanet-Tolosan, France.
  8. Diane Esquerré: Genotoul, INRA, US 1426 GeT PlaGe, Castanet-Tolosan, France.
  9. Hervé Acloque: GenPhySE UMR 1388, INRA, INPT, ENVT, Université de Toulouse, 31326, Castanet-Tolosan, France.
  10. Elisabetta Giuffra: GABI UMR 1313, INRA, AgroParisTech, Université Paris-Saclay, 78350, Jouy-en-Josas, France.
  11. Sarah Djebali: IRSD, Université de Toulouse, INSERM, INRA, ENVT, UPS, Toulouse, France.
  12. Sylvain Foissac: GenPhySE UMR 1388, INRA, INPT, ENVT, Université de Toulouse, 31326, Castanet-Tolosan, France.
  13. Thomas Derrien: IGDR UMR 6290, Univ Rennes, CNRS, 35000, Rennes, France.
  14. Frédérique Pitel: GenPhySE UMR 1388, INRA, INPT, ENVT, Université de Toulouse, 31326, Castanet-Tolosan, France.
  15. Tatiana Zerjal: GABI UMR 1313, INRA, AgroParisTech, Université Paris-Saclay, 78350, Jouy-en-Josas, France.
  16. Christophe Klopp: SIGENAE Platform, INRA, 31326, Castanet-Tolosan, France. christophe.klopp@inrae.fr.
  17. Sandrine Lagarrigue: PEGASE UMR 1348, INRA, AGROCAMPUS OUEST, 35590, Saint-Gilles, France. sandrine.lagarrigue@agrocampus-ouest.fr.

Abstract

Long non-coding RNAs (LNC) regulate numerous biological processes. In contrast to human, the identification of LNC in farm species, like chicken, is still lacunar. We propose a catalogue of 52,075 chicken genes enriched in LNC ( http://www.fragencode.org/ ), built from the Ensembl reference extended using novel LNC modelled here from 364 RNA-seq and LNC from four public databases. The Ensembl reference grew from 4,643 to 30,084 LNC, of which 59% and 41% with expression ≥ 0.5 and ≥ 1 TPM respectively. Characterization of these LNC relatively to the closest protein coding genes (PCG) revealed that 79% of LNC are in intergenic regions, as in other species. Expression analysis across 25 tissues revealed an enrichment of co-expressed LNC:PCG pairs, suggesting co-regulation and/or co-function. As expected LNC were more tissue-specific than PCG (25% vs. 10%). Similarly to human, 16% of chicken LNC hosted one or more miRNA. We highlighted a new chicken LNC, hosting miR155, conserved in human, highly expressed in immune tissues like miR155, and correlated with immunity-related PCG in both species. Among LNC:PCG pairs tissue-specific in the same tissue, we revealed an enrichment of divergent pairs with the PCG coding transcription factors, as for example LHX5, HXD3 and TBX4, in both human and chicken.

References

  1. PLoS Genet. 2016 Dec 29;12(12):e1006482 [PMID: 28033318]
  2. BMC Biol. 2019 Dec 30;17(1):108 [PMID: 31884969]
  3. BMC Biol. 2013 Nov 13;11:111 [PMID: 24225400]
  4. Genet Sel Evol. 2017 Jan 10;49(1):6 [PMID: 28073357]
  5. Sci Rep. 2018 Sep 7;8(1):13444 [PMID: 30194329]
  6. Nature. 2009 Mar 12;458(7235):223-7 [PMID: 19182780]
  7. Sci Rep. 2018 Jun 5;8(1):8630 [PMID: 29872091]
  8. BMC Genomics. 2018 Mar 7;19(1):187 [PMID: 29514634]
  9. Mol Cell. 2015 Aug 20;59(4):698-711 [PMID: 26236012]
  10. BMC Genomics. 2019 Dec 30;20(1):1033 [PMID: 31888468]
  11. Genes Dev. 2009 Aug 15;23(16):1831-42 [PMID: 19684108]
  12. Nat Med. 2008 Jul;14(7):723-30 [PMID: 18587408]
  13. Genes Dev. 2011 Sep 15;25(18):1915-27 [PMID: 21890647]
  14. Physiol Genomics. 2005 May 11;21(3):389-95 [PMID: 15769908]
  15. PLoS Biol. 2017 Sep 5;15(9):e2002887 [PMID: 28873399]
  16. Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11667-72 [PMID: 19571010]
  17. Genes Dev. 2008 Mar 15;22(6):756-69 [PMID: 18347095]
  18. Nucleic Acids Res. 2015 Jan;43(Database issue):D146-52 [PMID: 25378301]
  19. Genome Biol. 2015 Mar 25;16:57 [PMID: 25854118]
  20. Nucleic Acids Res. 2015 Jan;43(Database issue):D447-52 [PMID: 25352553]
  21. Nucleic Acids Res. 2017 Jan 4;45(D1):D12-D17 [PMID: 27899561]
  22. Nature. 2015 May 14;521(7551):232-6 [PMID: 25915022]
  23. J Pediatr. 2019 Mar;206:286-292.e1 [PMID: 30413314]
  24. J Mol Neurosci. 2019 Feb;67(2):282-294 [PMID: 30478755]
  25. Proc Natl Acad Sci U S A. 2017 Oct 31;114(44):E9290-E9299 [PMID: 29042517]
  26. Cell Microbiol. 2019 Aug;21(8):e13036 [PMID: 31045320]
  27. Nat Rev Genet. 2018 Sep;19(9):535-548 [PMID: 29795125]
  28. Nat Immunol. 2013 Oct;14(10):996-1006 [PMID: 24048121]
  29. Science. 2007 Apr 27;316(5824):608-11 [PMID: 17463290]
  30. Nucleic Acids Res. 2019 Sep 5;47(15):7842-7856 [PMID: 31350901]
  31. Trends Genet. 2011 Jul;27(7):267-76 [PMID: 21601935]
  32. Nat Commun. 2018 Aug 29;9(1):3516 [PMID: 30158538]
  33. Neural Dev. 2009 Nov 02;4:40 [PMID: 19883498]
  34. Nat Biotechnol. 2012 Mar 25;30(5):453-9 [PMID: 22446693]
  35. Bioinformatics. 2012 Oct 1;28(19):2520-2 [PMID: 22908215]
  36. PLoS Genet. 2007 Dec;3(12):e232 [PMID: 18159948]
  37. BMC Biol. 2012 Nov 15;10:90 [PMID: 23153189]
  38. Sci Rep. 2018 Dec 21;8(1):18038 [PMID: 30575756]
  39. J Hepatol. 2014 Sep;61(3):564-74 [PMID: 24798621]
  40. Science. 1999 May 14;284(5417):1155-8 [PMID: 10325223]
  41. Front Immunol. 2018 Oct 29;9:2512 [PMID: 30420860]
  42. Nucleic Acids Res. 2018 Jan 4;46(D1):D296-D302 [PMID: 29126174]
  43. Genome Res. 2012 Sep;22(9):1775-89 [PMID: 22955988]
  44. Nat Biotechnol. 2014 Mar;32(3):217-9 [PMID: 24727769]
  45. Brief Bioinform. 2017 Mar 1;18(2):205-214 [PMID: 26891983]
  46. Nat Neurosci. 2009 Apr;12(4):399-408 [PMID: 19287386]
  47. Front Immunol. 2015 Jan 30;5:676 [PMID: 25688240]
  48. Annu Rev Anim Biosci. 2019 Feb 15;7:65-88 [PMID: 30427726]
  49. Nat Commun. 2015 Jul 24;6:7743 [PMID: 26205790]
  50. Nucleic Acids Res. 2017 May 5;45(8):e57 [PMID: 28053114]
  51. Nat Struct Mol Biol. 2012 Jun 03;19(7):664-70 [PMID: 22659877]
  52. Proc Natl Acad Sci U S A. 2014 Apr 29;111(17):6131-8 [PMID: 24753594]
  53. Nat Rev Genet. 2003 Feb;4(2):87-98 [PMID: 12560806]
  54. Science. 2004 Feb 27;303(5662):1378-81 [PMID: 14988562]
  55. Cancer Res. 2011 Jun 1;71(11):3852-62 [PMID: 21558391]
  56. Nucleic Acids Res. 2018 Jan 4;46(D1):D308-D314 [PMID: 29140524]
  57. BMC Bioinformatics. 2011 Aug 04;12:323 [PMID: 21816040]
  58. BMC Genomics. 2003 Jul 29;4(1):31 [PMID: 12885301]
  59. Development. 1998 May;125(10):1967-78 [PMID: 9550729]
  60. Database (Oxford). 2019 Jan 1;2019: [PMID: 31210271]
  61. BMC Genomics. 2017 Jul 4;18(1):511 [PMID: 28676104]
  62. Bioinformatics. 2005 Mar 1;21(5):650-9 [PMID: 15388519]
  63. BMC Genomics. 2019 Nov 21;20(1):882 [PMID: 31752679]
  64. EMBO J. 2012 Feb 1;31(3):522-33 [PMID: 22193719]
  65. Bioinformatics. 2005 May 1;21(9):1859-75 [PMID: 15728110]
  66. Cell Rep. 2015 May 19;11(7):1110-22 [PMID: 25959816]
  67. J Cell Physiol. 2019 Aug;234(10):18361-18370 [PMID: 30887511]
  68. Genome Res. 2012 Sep;22(9):1760-74 [PMID: 22955987]
  69. Genome Biol. 2007;8(3):R43 [PMID: 17386095]
  70. Physiol Rev. 1998 Oct;78(4):921-47 [PMID: 9790566]
  71. Bioinformatics. 2013 Jan 1;29(1):15-21 [PMID: 23104886]
  72. F1000Res. 2020 Apr 28;9:304 [PMID: 32489650]
  73. Genome Res. 2005 Jan;15(1):111-9 [PMID: 15590946]
  74. Int J Tryptophan Res. 2017 Mar 15;10:1178646917691938 [PMID: 28469468]
  75. Nat Rev Mol Cell Biol. 2014 Aug;15(8):509-24 [PMID: 25027649]
  76. Cell Rep. 2018 Apr 3;23(1):297-312.e12 [PMID: 29617668]
  77. Nat Commun. 2017 Oct 4;8(1):783 [PMID: 28978906]
  78. Science. 2015 May 8;348(6235):660-5 [PMID: 25954002]
  79. Nat Struct Mol Biol. 2012 Nov;19(11):1068-75 [PMID: 23132386]
  80. Cell Stem Cell. 2016 May 5;18(5):637-52 [PMID: 26996597]
  81. Science. 2015 May 8;348(6235):648-60 [PMID: 25954001]
  82. Am J Hum Genet. 2019 Feb 7;104(2):213-228 [PMID: 30639323]
  83. Cell. 1992 Oct 30;71(3):515-26 [PMID: 1423610]
  84. Cell. 2018 Apr 19;173(3):649-664.e20 [PMID: 29677511]
  85. Bioinformatics. 2010 Mar 15;26(6):841-2 [PMID: 20110278]
  86. PLoS One. 2015 Apr 08;10(4):e0124003 [PMID: 25853886]
  87. Mol Cell. 2012 Aug 24;47(4):648-55 [PMID: 22841487]
  88. Mol Cell Biol. 1990 Jan;10(1):28-36 [PMID: 1688465]
  89. Nat Struct Mol Biol. 2015 Apr;22(4):319-27 [PMID: 25730776]
  90. BMC Genomics. 2018 Sep 18;19(1):684 [PMID: 30227846]
  91. Nat Rev Nephrol. 2018 Aug;14(8):479-492 [PMID: 29789704]

MeSH Term

Animals
Atlases as Topic
Avian Proteins
Chickens
Computational Biology
Gene Expression Profiling
Gene Expression Regulation
Gene Regulatory Networks
MicroRNAs
Molecular Sequence Annotation
Organ Specificity
RNA, Long Noncoding
Sequence Analysis, RNA
Tissue Distribution

Chemicals

Avian Proteins
MicroRNAs
RNA, Long Noncoding

Word Cloud

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