Gene model annotations for Drosophila melanogaster: The rule-benders

G3: Genes, Genomes, Genetics

Volumn 5, Issue 8, 2015, Pages 1737-1749

  Crosby, Madeline A ^a   Sian Gramates, L ^a   dos Santos, Gilberto ^a   Matthews, Beverley B ^a   St Pierre, Susan E ^a   Zhou, Pinglei ^a   Schroeder, Andrew J ^a   Falls, Kathleen ^a   Emmert, David B ^a   Russo, Susan M ^a   Gelbart, William M ^a   Gelbart, William ^a   Brown, Nicholas H ^b   Kaufman, Thomas ^c   Werner Washburne, Maggie ^d   Cripps, Richard ^d   Broll, Kris ^a   Crosby, Madeline ^a   Russo, Susan ^a   Schroeder, Andrew ^a   Zytkovicz, Mark ^a   Adryan, Boris ^b   Antonazzo, Giulia ^b   Attrill, Helen ^b   Costa, Marta ^b   Marygold, Steven ^b   McQuilton, Peter ^b   Millburn, Gillian ^b   Ponting, Laura ^b   Rey, Alix ^b   Staudt, Nicole ^b   Stefancsik, Raymund ^b   Goodman, Josh ^c   Grumbling, Gary ^c   Strelets, Victor ^c   Thurmond, Jim ^c   Baker, Phillip ^d   more..

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c INDIANA UNIVERSITY   (United States)

^d UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Bicistronic; Multiphasic exon; Non AUG translation start; Shared promoter; Stop codon suppression

Indexed keywords

DNA BINDING PROTEIN; SELENOCYSTEINE; SELENOPROTEIN; SMALL UNTRANSLATED RNA; RNA SPLICING; STOP CODON;

ARTICLE; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE ONTOLOGY; GENE SEQUENCE; GENETIC CODE; GENETIC MODEL; HIGH THROUGHPUT SEQUENCING; MITOCHONDRION; MOLECULAR CLONING; MOLECULAR GENETICS; NONHUMAN; OPEN READING FRAME; OVERLAPPING GENE; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; RIBOSOMAL FRAMESHIFTING; RNA EDITING; SPLICEOSOME; STOP CODON; TRANSCRIPTION INITIATION SITE; TRANSLATION INITIATION; UNFOLDED PROTEIN RESPONSE; ANIMAL; BIOLOGICAL MODEL; GENETIC DATABASE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN SYNTHESIS; RNA SPLICING;

DROSOPHILA MELANOGASTER;

ANIMALS; BASE SEQUENCE; CODON, TERMINATOR; DATABASES, GENETIC; DROSOPHILA MELANOGASTER; MITOCHONDRIA; MODELS, GENETIC; MOLECULAR SEQUENCE ANNOTATION; PROTEIN BIOSYNTHESIS; RNA EDITING; RNA SPLICE SITES;

EID: 84938871278     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.018937     Document Type: Article

References (83)

1. Alioto, T. S., 2007 U12DB: a database of orthologous U12-type spliceosomal introns. Nucleic Acids Res. 35(Database issue): D110-D115.
2. Andjelkovic, M., P. F. Jones, U. Grossniklaus, P. Cron, A. F. Schier et al., 1995 Developmental regulation of expression and activity of multiple forms of the Drosophila RAC protein kinase. J. Biol. Chem. 270: 4066-4075.
3. Andrews, J., M. Smith, J. Merakovsky, M. Coulson, F. Hannan et al., 1996 The stoned locus of Drosophila melanogaster produces a dicistronic transcript and encodes two distinct polypeptides. Genetics 143: 1699-1711.
4. Bainton, R. J., L. T. Y. Tsai, T. Schwabe, M. DeSalvo, U. Gaul et al., 2005 moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell 123: 145-156.
5. Batut, P., A. Dobin, C. Plessy, P. Carninci, and T. R. Gingeras, 2013 Highfidelity promoter profiling reveals widespread alternative promoter usage and transposon-driven developmental gene expression. Genome Res. 23: 169-180.
6. Beerman, R. W., and T. A. Jongens, 2011 A non-canonical start codon in the Drosophila fragile X gene yields two functional isoforms. Neuroscience 181: 48-66.
7. Ben-Shahar, Y., K. Nannapaneni, T. L. Casavant, T. E. Scheetz, and M. J. Welsh, 2007 Eukaryotic operon-like transcription of functionally related genes in Drosophila. Proc. Natl. Acad. Sci. USA 104: 222-227.
8. Bergstrom, D. E., C. A. Merli, J. A. Cygan, R. Shelby, and R. K. Blackman, 1995 Regulatory autonomy and molecular characterization of the Drosophila out at first gene. Genetics 139: 1331-1346.
9. Bertram, G., S. Innes, O. Minella, J. Richardson, and I. Stansfield, 2001 Endless possibilities: translation termination and stop codon recognition. Microbiology 147: 255-269.
10. Boyd, L., and C. S. Thummel, 1993 Selection of CUG and AUG initiator codons for translation depends on downstream sequences. Proc. Natl. Acad. Sci. USA 90: 9164-9167.
11. Brogna, S., and M. Ashburner, 1997 The Adh-related gene of Drosophila melanogaster is expressed as a functional dicistronic messenger RNA:Multigenic transcription in higher organisms. EMBO J. 16: 2023-2031.
12. Brown, J. B., N. Boley, R. Eisman,G. E.May,M.H. Stoiber et al., 2014 Diversity and dynamics of the Drosophila transcriptome. Nature 512: 393-399.
13. Castellano, S., N. Morozova, M. Morey, M. J. Berry, F. Serras et al., 2001 In silico identification of novel selenoproteins in the Drosophila melanogaster genome. EMBO Rep. 2: 697-702.
14. Celniker, S. E., D. A. Wheeler, B. Kronmiller, J. W. Carlson, A. Halpern et al., 2002 Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence. Genome Biol. 3: RESEARCH0079.
15. Cheng, Y., and H. A. Nash, 2007 Drosophila TRP channels require a protein with a distinctive motif encoded by the inaF locus. Proc. Natl. Acad. Sci. USA 104: 17730-17734.
16. Daines, B., H. Wang, L. Wang, Y. Li, Y. Han et al., 2011 The Drosophila melanogaster transcriptome by paired-end RNA sequencing. Genome Res. 21: 315-324.
17. de Simone, S. M., and K. White, 1993 The Drosophila erect wing gene, which is important for both neuronal and muscle development, encodes a protein which is similar to the sea urchin P3A2 DNA binding protein. Mol. Cell. Biol. 13: 3641-3649.
18. Dorn, R., G. Reuter, and A. Loewendorf, 2001 Transgene analysis proves mRNA trans-splicing at the complex mod(mdg4) locus in Drosophila. Proc. Natl. Acad. Sci. USA 98: 9724-9729.
19. dos Santos, G., A. J. Schroeder, J. L. Goodman, V. B. Strelets, M. A. Crosby et al., 2015 FlyBase: Introduction of the Drosophila melanogaster Release 6 reference genome assembly and large-scale migration of genome annotations. Nucleic Acids Res. 43(Database issue): D690-D697.
20. Driscoll, D. L., and L. Chavatte, 2004 Finding needles in a haystack. In silico identification of eukaryotic selenoprotein genes. EMBO Rep. 5: 140-141.
21. Dunn, J. G., C. K. Foo, N. G. Belletier, E. R. Gavis, and J. S. Weissman, 2013 Ribosome profiling reveals pervasive and regulated stop codon readthrough in Drosophila melanogaster. eLife 2: e01179.
22. Eilbeck, K., S. E. Lewis, C. J. Mungall, M. Yandell, L. Stein et al., 2005 The Sequence Ontology: a tool for the unification of genome annotations. Genome Biol. 6: R44.
23. Gabler, M., M. Volkmar, S. Weinlich, A. Herbst, P. Dobberthien et al., 2005 Trans-splicing of the mod(mdg4) complex locus is conserved between the distantly related species Drosophila melanogaster and D. virilis. Genetics 169: 723-736.
24. Gao, J. L., Y. J. Fan, X. Y. Wang, Y. Zhang, J. Pu et al., 2015 A conserved intronic U1 snRNP-binding sequence promotes trans-splicing in Drosophila. Genes Dev. 29: 760-771.
25. Gawron, D., K. Gevaert, and P. Van Damme, 2014 The proteome under translational control. Proteomics 14: 2647-2662.
26. Graveley, B. R., A. N. Brooks, J. W. Carlson, M. O. Duff, J. M. Landolin et al., 2011 The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479.
27. Gray, T. A., and R. D. Nicholls, 2000 Diverse splicing mechanisms fuse the evolutionarily conserved bicistronic MOCS1A and MOCS1B open reading frames. RNA 6: 928-936.
28. Hayden, C. A., and G. Bosco, 2008 Comparative genomic analysis of novel conserved peptide upstream open reading frames in Drosophila melanogaster and other dipteran species. BMC Genomics 9: 61.
29. Hellen, C. U., and P. Sarnow, 2001 Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15: 1593-1612.
30. Hooks, K. B., and S. Griffiths-Jones, 2011 Conserved RNA structures in the non-canonical Hac1/Xbp1 intron. RNA Biol. 8: 552-556.
31. Horiuchi, T., E. Giniger, and T. Aigaki, 2003 Alternative trans-splicing of constant and variable exons of a Drosophila axon guidance gene, lola. Genes Dev. 17: 2496-2501.
32. Horiuchi, T., and T. Aigaki, 2006 Alternative trans-splicing: A novel mode of pre- mRNA processing. Biol. Cell 98: 135-140.
33. Hoskins, R. A., J. W. Carlson, C. Kennedy, D. Acevedo, M. Evans-Holm et al., 2007 Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 316: 1625-1628.
34. Hoskins, R. A., J. M. Landolin, J. B. Brown, J. E. Sandler, H. Takahashi et al., 2011 Genome-wide analysis of promoter architecture in Drosophila melanogaster. Genome Res. 21: 182-192.
35. Hoskins, R. A., J. W. Carlson, K. H. Wan, S. Park, and I. Mendez, 2015 The Release 6 reference sequence of the Drosophila melanogaster genome. Genome Res. 25: 445-458.
36. Hu, Y., C. Roesel, I. Flockhart, L. Perkins, N. Perrimon et al., 2013 UPTORR:Online Tool for Accurate and Up-to-Date Annotation of RNAi Reagents. Genetics 195: 37-45.
37. Ibnsouda, S., P. Ferrer, and A. Vincent, 1998 Conservation of read-through transcription of the Drosophila serendipity genes during evolution is gratuitous. Mol. Gen. Genet. 259: 484-490.
38. Ingolia, N. T., L. F. Lareau, and J. S. Weissman, 2011 Ribosome profiling of mouse embryonic stem cells reveals the complexity and dynamics of mammalian proteomes. Cell 147: 789-802.
39. Ivanov, I. P., K. Simin, A. Letsou, J. F. Atkins, and R. F. Gesteland, 1998 The Drosophila gene for antizyme requires ribosomal frameshifting for expression and contains an intronic gene for snRNP Sm D3 on the opposite strand. Mol. Cell. Biol. 18: 1533-1561.
40. Ivanov, I. P., R. F. Gesteland, and J. F. Atkins, 2000 Antizyme expression:a subversion of triplet decoding, which is remarkably conserved by evolution, is a sensor for an autoregulatory circuit. Nucleic Acids Res. 28: 3185-3196.
41. Ivanov, I. P., A. E. Firth, A. M. Michel, J. F. Atkins, and P. V. Baranov, 2011 Identification of evolutionarily conserved non-AUG-initiated N-terminal extensions in human coding sequences. Nucleic Acids Res. 39: 4220-4234.
42. Jungreis, I., M. F. Lin, R. Spokony, C. S. Chan, N. Negre et al., 2011 Evidence of abundant stop codon readthrough in Drosophila and other metazoa. Genome Res. 21: 2096-2113.
43. Klagges, B. R. E., G. Heimbeck, T. A. Godenschwege, A. Hofbauer, G. O. Pflugfelder et al., 1996 Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J. Neurosci. 16: 3154-3165.
44. Krauss, V., and R. Dorn, 2004 Evolution of the trans-splicing Drosophila locus mod(mdg4) in several species of Diptera and Lepidoptera. Gene 331: 165-176.
45. Krauss, V., A. Fassl, P. Fiebig, I. Patties, and H. Sass, 2006 The evolution of the histone methyltransferase gene Su(var)3-9 in metazoans includes a fusion with and a re-fission from a functionally unrelated gene. BMC Evol. Biol. 6: 18.
46. Labrador, M., F. Mongelard, P. Plata-Rengifo, E. M. Baxter, V. G. Corces et al., 2001 Protein encoding by both DNA strands. Nature 409: 1000.
47. Lasda, E. L., and T. Blumenthal, 2011 Trans-splicing. Wiley Interdiscip. Rev. RNA 2: 417-434.
48. Lin, C. F., S. M. Mount, A. Jarmołowski, and W. Makałowski, 2010 Evolutionary dynamics of U12-type spliceosomal introns. BMC Evol. Biol. 10: 47.
49. Lin, M. F., J. W. Carlson, M. A. Crosby, B. B. Matthews, C. Yu et al., 2007 Revisiting the protein-coding gene catalog of Drosophila melanogaster using 12 fly genomes. Genome Res. 17: 1823-1836.
50. Lin, M. F., I. Jungreis, and M. Kellis, 2011 PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions. Bioinformatics 27: i275-i282.
51. Liu, H., J. K. Jang, J. Graham, K. Nycz, and K. S. McKim, 2000 Two genes required for meiotic recombination in Drosophila are expressed from a dicistronic message. Genetics 154: 1735-1746.
52. Madigan, S. J., P. Edeen, J. Esnayra, and M. McKeown, 1996 att, a target for regulation by tra2 in the testes of Drosophila melanogaster, encodes alternative RNAs and alternative proteins. Mol. Cell. Biol. 16: 4222-4230.
53. Mallela, A., and K. Nishikura, 2012 A-to-I editing of protein coding and noncoding RNAs. Crit. Rev. Biochem. Mol. Biol. 47: 493-501.
54. Martin-Romero, F. J., G. V. Kryukov, A. V. Lobanov, B. A. Carlson, B. J. Lee et al., 2001 Selenium metabolism in Drosophila: selenoproteins, selenoprotein mRNA expression, fertility, and mortality. J. Biol. Chem. 276: 29798-29804.
55. Matthews, B. B., G. dos Santos, M. A. Crosby, D. B. Emmert, S. E. St. Pierre et al., 2015 FlyBase Gene Model Annotations for Drosophila melanogaster. Impact of High-throughput Data G3 (Bethesda) 1721-1736.
56. McManus, C. J., M. O. Duff, J. Eipper-Mains, and B. R. Graveley, 2010 Global analysis of trans-splicing in Drosophila. Proc. Natl. Acad. Sci. USA 107: 12975-12979.
57. Megy, K., S. J. Emrich, D. Lawson, D. Campbell, E. Dialynas et al., 2012 VectorBase: improvements to a bioinformatics resource for invertebrate vector genomics. Nucleic Acids Res. 40(Database issue): D729-D734.
58. Menschaert, G., W. Van Criekinge, T. Notelaers, A. Koch, J. Crappe et al., 2013 Deep proteome coverage based on ribosome profiling aids mass spectrometry-based protein and peptide discovery and provides evidence of alternative translation products and near-cognate translation initiation events. Mol. Cell. Proteomics 12: 1780-1790.
59. Mészáros, B., and I. Simon, Z. Dosztányi, 2011 The expanding view of protein-protein interactions: complexes involving intrinsically disordered proteins. Phys. Biol. 8: 035003.
60. Misra, S., M. A. Crosby, C. J. Mungall, B. B. Matthews, K. S. Campbell et al., 2002 Annotation of the Drosophila melanogaster euchromatic genome:a systematic review. Genome Biol. 3: RESEARCH0083.
61. Nechaev, S., D. C. Fargo, G. dos Santos, L. Liu, Y. Gao et al., 2010 Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 327: 335-338.
62. Niimi, T., H. Yokoyama, A. Goto, K. Beck, and Y. Kitagawa, 1999 A Drosophila gene encoding multiple splice variants of Kazal-type serine protease inhibitor-like proteins with potential destinations of mitochondria, cytosol and the secretory pathway. Eur. J. Biochem. 266: 282-292.
63. Olsen, R. R., and B. R. Zetter, 2011 Evidence of a role for antizyme and antizyme inhibitor as regulators of human cancer. Mol. Cancer Res. 9: 1285-1293.
64. Pankotai, T., N. Zsindely, E. E. Vamos, L. Komonyi, L. Bodai et al., 2013 Functional characterization and gene expression profiling of Drosophila melanogaster short dADA2b isoform-containing dSAGA complexes. BMC Genomics 14: 44.
65. Parada, G. E., R. Munita, C. A. Cerda, and K. Gysling, 2014 A comprehensive survey of non-canonical splice sites in the human transcriptome. Nucleic Acids Res. 42: 10564-10578.
66. Pauli, D., C. H. Tonka, and A. Ayme-Southgate, 1988 An unusual split Drosophila heat shock gene expressed during embryogenesis, pupation and in testis. J. Mol. Biol. 200: 47-53.
67. Peabody, D. S., 1989 Translation initiation at non-AUG triplets in mammalian cells. J. Biol. Chem. 264: 5031-5035.
68. Phillips, A. M., M. Smith, M. Ramaswami, and L. E. Kelly, 2000 The products of the Drosophila stoned locus interact with synaptic vesicles via synaptotagmin. J. Neurosci. 20: 8254-8261.
69. Plongthongkum, N., N. Kullawong, S. Panyim, and W. Tirasophon, 2007 Ire1 regulated XBP1 mRNA splicing is essential for the unfolded protein response (UPR) in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 354: 789-794.
70. Robinson, D. N., and L. Cooley, 1997 Examination of the function of two kelch proteins generated by stop codon suppression. Development 124: 1405-1417.
71. Rodriguez, J., J. S. Menet, and M. Rosbash, 2012 Nascent-seq indicates widespread cotranscriptional RNA editing in Drosophila. Mol. Cell 47: 27-37.
72. Ryoo, H. D., P. M. Domingos, M. J. Kang, and H. Steller, 2007 Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J. 26: 242-252.
73. Schneider, C., C. L. Will, J. Brosius, M. J. Frilander, and R. Luhrmann, 2004 Identification of an evolutionarily divergent U11 small nuclear ribonucleoprotein particle in Drosophila. Proc. Natl. Acad. Sci. USA 101: 9584-9589.
74. Schulz, R. A., J. L. Miksch, X. L. Xie, J. A. Cornish, and S. Galewsky, 1990 Expression of the Drosophila gonadal gene: alternative promoters control the germ-line expression of monocistronic and bicistronic gene transcripts. Development 108: 613-622.
75. Sidrauski, C., and P. Walter, 1997 The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90: 1031-1039.
76. Steneberg, P., C. Englund, J. Kronhamn, T. A. Weaver, and C. Samakovlis, 1998 Translational readthrough in the hdc mRNA generates a novel branching inhibitor in the Drosophila trachea. Genes Dev. 12: 956-967.
77. St Laurent, G., M. R. Tackett, S. Nechkin, D. Shtokalo, D. Antonets et al., 2013 Genome-wide analysis of A-to-I RNA editing by single-molecule sequencing in Drosophila. Nat. Struct. Mol. Biol. 20: 1333-1339.
78. Sugihara, H., V. Andrisani, and P. M. Salvaterra, 1990 Drosophila choline acetyltransferase uses a non-AUG initiation codon and full length RNA is inefficiently translated. J. Biol. Chem. 265: 21714-21719.
79. Szafranski, K., S. Schindler, S. Taudien, M. Hiller, K. Huse et al., 2007 Violating the splicing rules: TG dinucleotides function as alternative 39 splice sites in U2-dependent introns. Genome Biol. 8: R154.
80. von der Haar, T., and M. F. Tuite, 2007 Regulated translational bypass of stop codons in yeast. Trends Microbiol. 15: 78-86.
81. Walker, D. L., D. Wang, Y. Jin, U. Rath, Y. Wang et al., 2000 Skeletor, a novel chromosomal protein that redistributes during mitosis provides evidence for the formation of a spindle matrix. J. Cell Biol. 151: 1401-1412.
82. Wall, A. A., A. M. Phillips, and L. E. Kelly, 2005 Effective translation of the second cistron in two Drosophila dicistronic transcripts is determined by the absence of in-frame AUG codons in the first cistron. J. Biol. Chem. 280: 27670-27678.
83. Xue, F., and L. Cooley, 1993 kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell 72: 681-693.