The life cycle of Drosophila orphan genes

eLife

Volumn 2014, Issue 3, 2014, Pages

  Palmieri, Nicola ^a   Kosiol, Carolin ^a   Schlötterer, Christian ^a  

^a Institute of Populationsgenetik   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ARTHROPOD LIFE CYCLE STAGE; ARTICLE; DNA STRUCTURE; DROSOPHILA; FEMALE; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; GENETIC POLYMORPHISM; MALE; MICROSATELLITE; NONHUMAN; ORPHAN GENE; TRANSPOSON;

EID: 84896504155     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.01311.001     Document Type: Article

References (63)

1. Abraham I, Lucchesi JC. 1974. Dosage compensation of genes on the left and right arms of the X chromosome of Drosophila pseudoobscura and Drosophila willistoni. Genetics 78:1119-1126.
2. Anders S, Huber W. 2010. Differential expression analysis for sequence count data. Genome Biology 11:R106. doi: 10.1186/gb-2010-11-10-r106.
3. Beckenbach AT, Wei YW, Liu H. 1993. Relationships in the Drosophila obscura species group, inferred from mitochondrial cytochrome oxidase II sequences. Molecular Biology and Evolution 10:619-634.
4. Begun DJ, Lindfors HA, Kern AD, Jones CD. 2007. Evidence for de novo evolution of testis-expressed genes in the Drosophila yakuba/Drosophila erecta clade. Genetics 176:1131-1137. doi: 10.1534/genetics.106.069245.
5. Cai J, Zhao R, Jiang H, Wang W. 2008. De novo origination of a new protein-coding gene in Saccharomyces cerevisiae. Genetics 179:487-496. doi: 10.1534/genetics.107.084491.
6. Cai JJ, Petrov DA. 2010. Relaxed purifying selection and possibly high rate of adaptation in primate lineage-specific genes. Genome Biology and Evolution 2:393-409. doi: 10.1093/gbe/evq019.
7. Capra JA, Pollard KS, Singh M. 2010. Novel genes exhibit distinct patterns of function acquisition and network integration. Genome Biology 11:R127. doi: 10.1186/gb-2010-11-12-r127.
8. Carvunis AR, Rolland T, Wapinski I, Calderwood MA, Yildirim MA, Simonis N, Charloteaux B, Hidalgo CA, Barbette J, Santhanam B, Brar GA, Weissman JS, Regev A, Thierry-Mieg N, Cusick ME, Vidal M. 2012. Proto-genes and de novo gene birth. Nature 487:370-374. doi: 10.1038/nature11184.
9. Chen S, Zhang YE, Long M. 2010. New genes in Drosophila quickly become essential. Science 330:1682-1685. doi: 10.1126/science.1196380.
10. Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC, Kellis M, Gelbart W, Iyer VN, Pollard DA, Sackton TB, Larracuente AM, Singh ND, Abad JP, Abt DN, Adryan B, Aguade M, Akashi H, Anderson WW, Aquadro CF, Ardell DH, Arguello R, Artieri CG, Barbash DA, Barker D, Barsanti P, Batterham P, Batzoglou S, Begun D, Bhutkar A, Blanco E, Bosak SA, Bradley RK, Brand AD, Brent MR, Brooks AN, Brown RH, Butlin RK, Caggese C, Calvi BR, Bernardo de Carvalho A, Caspi A, Castrezana S, Celniker SE, Chang JL, Chapple C, Chatterji S, Chinwalla A, Civetta A, Clifton SW, Comeron JM, Costello JC, Coyne JA, Daub J, David RG, Delcher AL, Delehaunty K, Do CB, Ebling H, Edwards K, Eickbush T, Evans JD, Filipski A, Findeiss S, Freyhult E, Fulton L, Fulton R, Garcia AC, Gardiner A, Garfield DA, Garvin BE, Gibson G, Gilbert D, Gnerre S, Godfrey J, Good R, Gotea V, Gravely B, Greenberg AJ, Griffiths-Jones S, Gross S, Guigo R, Gustafson EA, Haerty W, Hahn MW, Halligan DL, Halpern AL, Halter GM, Han MV, Heger A, Hillier L, Hinrichs AS, Holmes I, Hoskins RA, Hubisz MJ, Hultmark D, Huntley MA, Jaffe DB, Jagadeeshan S, Jeck WR, Johnson J, Jones CD, Jordan WC, Karpen GH, Kataoka E, Keightley PD, Kheradpour P, Kirkness EF, Koerich LB, Kristiansen K, Kudrna D, Kulathinal RJ, Kumar S, Kwok R, Lander E, Langley CH, Lapoint R, Lazzaro BP, Lee SJ, Levesque L, Li R, Lin CF, Lin MF, Lindblad-Toh K, Llopart A, Long M, Low L, Lozovsky E, Lu J, Luo M, Machado CA, Makalowski W, Marzo M, Matsuda M, Matzkin L, McAllister B, McBride CS, McKernan B, McKernan K, Mendez-Lago M, Minx P, Mollenhauer MU, Montooth K, Mount SM, Mu X, Myers E, Negre B, Newfeld S, Nielsen R, Noor MA, O'Grady P, Pachter L, Papaceit M, Parisi MJ, Parisi M, Parts L, Pedersen JS, Pesole G, Phillippy AM, Ponting CP, Pop M, Porcelli D, Powell JR, Prohaska S, Pruitt K, Puig M, Quesneville H, Ram KR, Rand D, Rasmussen MD, Reed LK, Reenan R, Reily A, Remington KA, Rieger TT, Ritchie MG, Robin C, Rogers YH, Rohde C, Rozas J, Rubenfield MJ, Ruiz A, Russo S, Salzberg SL, Sanchez-Gracia A, Saranga DJ, Sato H, Schaeffer SW, Schatz MC, Schlenke T, Schwartz R, Segarra C, Singh RS, Sirot L, Sirota M, Sisneros NB, Smith CD, Smith TF, Spieth J, Stage DE, Stark A, Stephan W, Strausberg RL, Strempel S, Sturgill D, Sutton G, Sutton GG, Tao W, Teichmann S, Tobari YN, Tomimura Y, Tsolas JM, Valente VL, Venter E, Venter JC, Vicario S, Vieira FG, Vilella AJ, Villasante A, Walenz B, Wang J, Wasserman M, Watts T, Wilson D, Wilson RK, Wing RA, Wolfner MF, Wong A, Wong GK, Wu CI, Wu G, Yamamoto D, Yang HP, Yang SP, Yorke JA, Yoshida K, Zdobnov E, Zhang P, Zhang Y, Zimin AV, Baldwin J, Abdouelleil A, Abdulkadir J, Abebe A, Abera B, Abreu J, Acer SC, Aftuck L, Alexander A, An P, Anderson E, Anderson S, Arachi H, Azer M, Bachantsang P, Barry A, Bayul T, Berlin A, Bessette D, Bloom T, Blye J, Boguslavskiy L, Bonnet C, Boukhgalter B, Bourzgui I, Brown A, Cahill P, Channer S, Cheshatsang Y, Chuda L, Citroen M, Collymore A, Cooke P, Costello M, D'Aco K, Daza R, De Haan G, DeGray S, DeMaso C, Dhargay N, Dooley K, Dooley E, Doricent M, Dorje P, Dorjee K, Dupes A, Elong R, Falk J, Farina A, Faro S, Ferguson D, Fisher S, Foley CD, Franke A, Friedrich D, Gadbois L, Gearin G, Gearin CR, Giannoukos G, Goode T, Graham J, Grandbois E, Grewal S, Gyaltsen K, Hafez N, Hagos B, Hall J, Henson C, Hollinger A, Honan T, Huard MD, Hughes L, Hurhula B, Husby ME, Kamat A, Kanga B, Kashin S, Khazanovich D, Kisner P, Lance K, Lara M, Lee W, Lennon N, Letendre F, LeVine R, Lipovsky A, Liu X, Liu J, Liu S, Lokyitsang T, Lokyitsang Y, Lubonja R, Lui A, MacDonald P, Magnisalis V, Maru K, Matthews C, McCusker W, McDonough S, Mehta T, Meldrim J, Meneus L, Mihai O, Mihalev A, Mihova T, Mittelman R, Mlenga V, Montmayeur A, Mulrain L, Navidi A, Naylor J, Negash T, Nguyen T, Nguyen N, Nicol R, Norbu C, Norbu N, Novod N, O'Neill B, Osman S, Markiewicz E, Oyono OL, Patti C, Phunkhang P, Pierre F, Priest M, Raghuraman S, Rege F, Reyes R, Rise C, Rogov P, Ross K, Ryan E, Settipalli S, Shea T, Sherpa N, Shi L, Shih D, Sparrow T, Spaulding J, Stalker J, Stange-Thomann N, Stavropoulos S, Stone C, Strader C, Tesfaye S, Thomson T, Thoulutsang Y, Thoulutsang D, Topham K, Topping I, Tsamla T, Vassiliev H, Vo A, Wangchuk T, Wangdi T, Weiand M, Wilkinson J, Wilson A, Yadav S, Young G, Yu Q, Zembek L, Zhong D, Zimmer A, Zwirko Z, Jaffe DB, Alvarez P, Brockman W, Butler J, Chin C, Gnerre S, Grabherr M, Kleber M, Mauceli E, MacCallum I. 2007. Evolution of genes and genomes on the Drosophila phylogeny. Nature 450:203-218. doi: 10.1038/nature06341.
11. Colbourne JK, Pfrender ME, Gilbert D, Thomas WK, Tucker A, Oakley TH, Tokishita S, Aerts A, Arnold GJ, Basu MK, Bauer DJ, Cáceres CE, Carmel L, Casola C, Choi JH, Detter JC, Dong Q, Dusheyko S, Eads BD, Fröhlich T, Geiler-Samerotte KA, Gerlach D, Hatcher P, Jogdeo S, Krijgsveld J, Kriventseva EV, Kültz D, Laforsch C, Lindquist E, Lopez J, Manak JR, Muller J, Pangilinan J, Patwardhan RP, Pitluck S, Pritham EJ, Rechtsteiner A, Rho M, Rogozin IB, Sakarya O, Salamov A, Schaack S, Shapiro H, Shiga Y, Skalitzky C, Smith Z, Souvorov A, Sung W, Tang Z, Tsuchiya D, Tu H, Vos H, Wang M, Wolf YI, Yamagata H, Yamada T, Ye Y, Shaw JR, Andrews J, Crease TJ, Tang H, Lucas SM, Robertson HM, Bork P, Koonin EV, Zdobnov EM, Grigoriev IV, Lynch M, Boore JL. 2011. The ecoresponsive genome of Daphnia pulex. Science 331:555-561. doi: 10.1126/science.1197761.
12. Domazet-Loso T, Brajkovic J, Tautz D. 2007. A phylostratigraphy approach to uncover the genomic history of major adaptations in metazoan lineages. Trends in Genetics 23:533-539. doi: 10.1016/j.tig.2007.08.014.
13. Domazet-Loso T, Tautz D. 2003. An evolutionary analysis of orphan genes in Drosophila. Genome Research 13:2213-2219. doi: 10.1101/gr.1311003.
14. Gallach M, Arnau V, Marín I. 2007. Global patterns of sequence evolution in Drosophila. BMC Genomics 8:408. doi: 10.1186/1471-2164-8-408.
15. Gao JJ, Watabe HA, Aotsuka T, Pang JF, Zhang YP. 2007. Molecular phylogeny of the Drosophila obscura species group, with emphasis on the Old World species. BMC Evolutionary Biology 7:87. doi: 10.1186/1471-2148-7-87.
16. Guo WJ, Li P, Ling J, Ye SP. 2007. Significant comparative characteristics between orphan and nonorphan genes in the rice (Oryza sativa L.) genome. Comparative and Functional Genomics 2007:21676. doi: 10.1155/2007/21676.
17. Hahn MW, Han MV, Han SG. 2007. Gene family evolution across 12 Drosophila genomes. PLOS Genetics 3:e197. doi: 10.1371/journal.pgen.0030197.
18. Heinen TJ, Staubach F, Häming D, Tautz D. 2009. Emergence of a new gene from an intergenic region. Current Biology 19:1527-1531. doi: 10.1016/j.cub.2009.07.049.
19. Hoehn KB, McGaugh SE, Noor MA. 2012. Effects of premature termination codon polymorphisms in the Drosophila pseudoobscura Subclade. Journal of Molecular Evolution 75:141-150. doi: 10.1007/s00239-012-9528-x.
20. Kaessmann H. 2010. Origins, evolution, and phenotypic impact of new genes. Genome Research 20:1313-1326. doi: 10.1101/gr.101386.109.
21. Khalturin K, Anton-Erxleben F, Sassmann S, Wittlieb J, Hemmrich G, Bosch TC. 2008. A novel gene family controls species-specific morphological traits in Hydra. PLOS Biology 6:e278. doi: 10.1371/journal.pbio.0060278.
22. Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch TC. 2009. More than just orphans: are taxonomically-restricted genes important in evolution? Trends in Genetics 25:404-413. doi: 10.1016/j.tig.2009.07.006.
23. Kleene KC. 2005. Sexual selection, genetic conflict, selfish genes, and the atypical patterns of gene expression in spermatogenic cells. Developmental Biology 277:16-26. doi: 10.1016/j.ydbio.2004.09.031.
24. Knowles DG, McLysaght A. 2009. Recent de novo origin of human protein-coding genes. Genome Research 19:1752-1759. doi: 10.1101/gr.095026.109.
25. Kofler R, Orozco-terWengel P, De Maio N, Pandey RV, Nolte V, Futschik A, Kosiol C, Schlötterer C. 2011. PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLOS ONE 6:e15925. doi: 10.1371/journal.pone.0015925.
26. Kofler R, Schlötterer C, Lelley T. 2007. SciRoKo: a new tool for whole genome microsatellite search and investigation. Bioinformatics 23:1683-1685. doi: 10.1093/bioinformatics/btm157.
27. Krylov DM, Wolf YI, Rogozin IB, Koonin EV. 2003. Gene loss, protein sequence divergence, gene dispensability, expression level, and interactivity are correlated in eukaryotic evolution. Genome Research 13:2229-2235. doi: 10.1101/gr.1589103.
28. Lee YC, Reinhardt JA. 2012. Widespread polymorphism in the positions of stop codons in Drosophila melanogaster. Genome Biological Evolution 4:533-549. doi: 10.1093/gbe/evr113.
29. Lemos B, Bettencourt BR, Meiklejohn CD, Hartl DL. 2005. Evolution of proteins and gene expression levels are coupled in Drosophila and are independently associated with mRNA abundance, protein length, and number of protein-protein interactions. Molecular Biology and Evolution 22:1345-1354. doi: 10.1093/molbev/msi122.
30. Levine MT, Jones CD, Kern AD, Lindfors HA, Begun DJ. 2006. Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression. Proceedings of the National Academy of Sciences of the United States of America 103:9935-9939. doi: 10.1073/pnas.0509809103.
31. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. doi: 10.1093/bioinformatics/btp324.
32. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup. 2009. The sequence alignment/map (SAM) format and SAMtools. Bioinformatics 25:2078-2079. doi: 10.1093/bioinformatics/btp352.
33. Li W, Godzik A. 2006. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658-1659. doi: 10.1093/bioinformatics/btl158.
34. Lipman DJ, Souvorov A, Koonin EV, Panchenko AR, Tatusova TA. 2002. The relationship of protein conservation and sequence length. BMC Evolutionary Biology 2:20. doi: 10.1186/1471-2148-2-20.
35. Loytynoja A, Goldman N. 2005. An algorithm for progressive multiple alignment of sequences with insertions. Proceedings of the National Academy of Sciences of the United States of America 102:10557-10562. doi: 10.1073/pnas.0409137102.
36. McGaugh SE, Heil CS, Manzano-Winkler B, Loewe L, Goldstein S, Himmel TL, Noor MA. 2012. Recombination modulates how selection affects linked sites in Drosophila. PLOS Biology 10:e1001422. doi: 10.1371/journal.pbio.1001422.
37. Meisel RP, Han MV, Hahn MW. 2009. A complex suite of forces drives gene traffic from Drosophila X chromosomes. Genome Biology and Evolution 1:176-188. doi: 10.1093/gbe/evp018.
38. Metta M, Schlötterer C. 2008. Male-biased genes are overrepresented among novel Drosophila pseudoobscura sex-biased genes. BMC Evolutionary Biology 8:182. doi: 10.1186/1471-2148-8-182.
39. Neme R, Tautz D. 2013. Phylogenetic patterns of emergence of new genes support a model of frequent de novo evolution. BMC Genomics 14:117. doi: 10.1186/1471-2164-14-117.
40. Obbard DJ, Maclennan J, Kim KW, Rambaut A, O'Grady PM, Jiggins FM. 2012. Estimating divergence dates and substitution rates in the Drosophila phylogeny. Molecular Biology and Evolution 29:3459-3473. doi: 10.1093/molbev/mss150.
41. Palmieri N, Kosiol C, Schlötterer C. 2014. Data from: the life cycle of Drosophila orphan genes. Dryad Digital Repository. doi: 10.5061/dryad.hq564.
42. Palmieri N, Nolte V, Suvorov A, Kosiol C, Schlötterer C. 2012. Evaluation of different reference based annotation Strategies using RNA-seq-a case study in Drosophila pseudoobscura. PLOS ONE 7:e46415. doi: 10.1371/journal.pone.0046415.
43. Pandey RV, Schlötterer C. 2013. DistMap: a toolkit for distributed short read mapping on a Hadoop cluster. PLOS ONE 8:e72614. doi: 10.1371/journal.pone.0072614.
44. Richards S, Liu Y, Bettencourt BR, Hradecky P, Letovsky S, Nielsen R, Thornton K, Hubisz MJ, Chen R, Meisel RP, Couronne O, Hua S, Smith MA, Zhang P, Liu J, Bussemaker HJ, van Batenburg MF, Howells SL, Scherer SE, Sodergren E, Matthews BB, Crosby MA, Schroeder AJ, Ortiz-Barrientos D, Rives CM, Metzker ML, Muzny DM, Scott G, Steffen D, Wheeler DA, Worley KC, Havlak P, Durbin KJ, Egan A, Gill R, Hume J, Morgan MB, Miner G, Hamilton C, Huang Y, Waldron L, Verduzco D, Clerc-Blankenburg KP, Dubchak I, Noor MA, Anderson W, White KP, Clark AG, Schaeffer SW, Gelbart W, Weinstock GM, Gibbs RA. 2005. Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution. Genome Research 15:1-18. doi: 10.1101/gr.3059305.
45. Sassone-Corsi P. 2002. Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science 296:2176-2178. doi: 10.1126/science.1070963.
46. Sharp PM, Li WH. 1987. The codon Adaptation Index-a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Research 15:1281-1295. doi: 10.1093/nar/15.3.1281.
47. Tautz D, Domazet-Loso T. 2011. The evolutionary origin of orphan genes. Nature Review Genetics 12:692-702. doi: 10.1038/nrg3053.
48. Toll-Riera M, Bosch N, Bellora N, Castelo R, Armengol L, Estivill X, Albà MM. 2009. Origin of primate orphan genes: a comparative genomics approach. Molecular Biology and Evolution 26:603-612. doi: 10.1093/molbev/msn281.
49. Toll-Riera M, Castelo R, Bellora N, Albà MM. 2009. Evolution of primate orphan proteins. Biochemical Society Transactions 37:778-782. doi: 10.1042/BST0370778.
50. Toll-Riera M, Rado-Trilla N, Martys F, Albà MM. 2012. Role of low-complexity sequences in the formation of novel protein coding sequences. Molecular Biology and Evolution 29:883-886. doi: 10.1093/molbev/msr263.
51. Wang X, Grus WE, Zhang J. 2006. Gene losses during human origins. PLOS Biology 4:e52. doi: 10.1371/journal.pbio.0040052.
52. Warnefors M, Eyre-Walker A. 2011. The accumulation of gene regulation through time. Genome Biology and Evolution 3:667-673. doi: 10.1093/gbe/evr019.
53. Wissler L, Gadau J, Simola DF, Helmkampf M, Bornberg-Bauer E. 2013. Mechanisms and dynamics of orphan gene emergence in insect genomes. Genome Biology and Evolution 5:439-455. doi: 10.1093/gbe/evt009.
54. Wolf YI, Novichkov PS, Karev GP, Koonin EV, Lipman DJ. 2009. Inaugural article: the universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages. Proceedings of the National Academy of Sciences of the United States of America 106:7273-7280. doi: 10.1073/pnas.0901808106.
55. Wu DD, Irwin DM, Zhang YP. 2011. De novo origin of human protein-coding genes. PLOS Genetics 7:e1002379. doi: 10.1371/journal.pgen.1002379.
56. Wu DD, Zhang YP. 2013. Evolution and function of de novo originated genes. Molecular Phylogenetics and Evolution 67:541-545. doi: 10.1016/j.ympev.2013.02.013.
57. Wu TD, Nacu S. 2010. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26:873-881. doi: 10.1093/bioinformatics/btq057.
58. Xie C, Zhang YE, Chen JY, Liu CJ, Zhou WZ, Li Y, Zhang M, Zhang R, Wei L, Li CY. 2012. Hominoid-specific de novo protein-coding genes originating from long non-coding RNAs. PLOS Genetics 8:e1002942. doi: 10.1371/journal.pgen.1002942.
59. Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24:1586-1591. doi: 10.1093/molbev/msm088.
60. Yang Z, Huang J. 2011. De novo origin of new genes with introns in Plasmodium vivax. FEBS Letters 585:641-644. doi: 10.1016/j.febslet.2011.01.017.
61. Zhang YE, Vibranovski MD, Krinsky BH, Long M. 2010. Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Research 20:1526-1533. doi: 10.1101/gr.107334.110.
62. Zhou Q, Bachtrog D. 2012. Sex-specific adaptation drives early sex chromosome evolution in Drosophila. Science 337:341-345. doi: 10.1126/science.1225385.
63. Zhou Q, Zhang G, Zhang Y, Xu S, Zhao R, Zhan Z, Li X, Ding Y, Yang S, Wang W. 2008. On the origin of new genes in Drosophila. Genome Research 18:1446-1455. doi: 10.1101/gr.076588.108.