Frequency of intron loss correlates with processed pseudogene abundance: A novel strategy to test the reverse transcriptase model of intron loss

BMC Biology

Volumn 11, Issue , 2013, Pages

  Zhu, Tao ^a   Niu, Deng Ke ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

Author keywords

Free cytoplasmic ribosomes; Genomic deletion model; Intron loss; Long interspersed element; Muridae; Processed pseudogene; Reverse transcription

Indexed keywords

MURIDAE; MUS; RATTUS;

MESSENGER RNA; PROTEIN; RNA DIRECTED DNA POLYMERASE; SIGNAL PEPTIDE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; GENOME; INTRON; LONG INTERSPERSED REPEAT; MAMMAL; METABOLISM; MOUSE; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN TERTIARY STRUCTURE; PSEUDOGENE; RAT; SOLUBILITY;

ANIMALS; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION; GENOME; INTRONS; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MAMMALS; MICE; MODELS, GENETIC; PHYLOGENY; PROTEIN SORTING SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEINS; PSEUDOGENES; RATS; RNA, MESSENGER; RNA-DIRECTED DNA POLYMERASE; SEQUENCE DELETION; SOLUBILITY;

EID: 84874470305     PISSN: None     EISSN: 17417007     Source Type: Journal    
DOI: 10.1186/1741-7007-11-23     Document Type: Article

References (78)

1. Rogozin IB, Wolf YI, Sorokin AV, Mirkin BG, Koonin EV. Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution. Curr Biol 2003, 13:1512-1517. 10.1016/S0960-9822(03)00558-X, 12956953.
2. Roy SW, Fedorov A, Gilbert W. Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc Natl Acad Sci USA 2003, 100:7158-7162. 10.1073/pnas.1232297100, 165846, 12777620.
3. Kiontke K, Gavin NP, Raynes Y, Roehrig C, Piano F, Fitch DHA. Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci USA 2004, 101:9003-9008. 10.1073/pnas.0403094101, 428462, 15184656.
4. Roy SW, Penny D. Large-scale intron conservation and order-of-magnitude variation in intron loss/gain rates in apicomplexan evolution. Genome Res 2006, 16:1270-1275. 10.1101/gr.5410606, 1581436, 16963708.
5. Carmel L, Rogozin IB, Wolf YI, Koonin EV. Evolutionarily conserved genes preferentially accumulate introns. Genome Res 2007, 17:1045-1050. 10.1101/gr.5978207, 1899115, 17495009.
6. Nguyen HD, Yoshihama M, Kenmochi N. The evolution of spliceosomal introns in Alveolates. Mol Biol Evol 2007, 24:1093-1096. 10.1093/molbev/msm037, 17331959.
7. Roy SW, Penny D. Widespread intron loss suggests retrotransposon activity in ancient apicomplexans. Mol Biol Evol 2007, 24:1926-1933. 10.1093/molbev/msm102, 17522085.
8. Slamovits CH, Keeling PJ. Evolution of ultrasmall spliceosomal introns in highly reduced nuclear genomes. Mol Biol Evol 2009, 26:1699-1705. 10.1093/molbev/msp081, 19380463.
9. Csuros M, Rogozin IB, Koonin EV. A detailed history of intron-rich eukaryotic ancestors inferred from a global survey of 100 complete genomes. PLoS Comput Biol 2011, 7:e1002150. 10.1371/journal.pcbi.1002150, 3174169, 21935348.
10. Rogozin I, Carmel L, Csuros M, Koonin E. Origin and evolution of spliceosomal introns. Biol Direct 2012, 7:11. 10.1186/1745-6150-7-11, 3488318, 22507701.
11. Jeffares DC, Mourier T, Penny D. The biology of intron gain and loss. Trends Genet 2006, 22:16-22. 10.1016/j.tig.2005.10.006, 16290250.
12. Fink GR. Pseudogenes in yeast?. Cell 1987, 49:5-6. 10.1016/0092-8674(87)90746-X, 3549000.
13. Mourier T, Jeffares DC. Eukaryotic intron loss. Science 2003, 300:1393. 10.1126/science.1080559, 12775832.
14. Rodriguez-Trelles F, Tarro R, Ayala FJ. Origins and evolution of spliceosomal introns. Annu Rev Genet 2006, 40:47-76. 10.1146/annurev.genet.40.110405.090625, 17094737.
15. Roy SW, Gilbert W. The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 2006, 7:211-221.
16. Loh Y-H, Brenner S, Venkatesh B. Investigation of loss and gain of introns in the compact genomes of Pufferfishes (Fugu and Tetraodon). Mol Biol Evol 2008, 25:526-535. 10.1093/molbev/msm278, 18089580.
17. Farlow A, Meduri E, Schlotterer C. DNA double-strand break repair and the evolution of intron density. Trends Genet 2011, 27:1-6. 10.1016/j.tig.2010.10.004, 3020277, 21106271.
18. Derr LK, Strathern JN. A role for reverse transcripts in gene conversion. Nature 1993, 361:170-173. 10.1038/361170a0, 8380627.
19. Derr LK, Strathern JN, Garfinkel DJ. RNA-mediated recombination in S. cerevisiae. Cell 1991, 67:355-364. 10.1016/0092-8674(91)90187-4, 1655280.
20. Roy SW, Gilbert W. The pattern of intron loss. Proc Natl Acad Sci USA 2005, 102:713-718. 10.1073/pnas.0408274102, 545554, 15642949.
21. Coulombe-Huntington J, Majewski J. Intron loss and gain in Drosophila. Mol Biol Evol 2007, 24:2842-2850.
22. Stajich JE, Dietrich FS. Evidence of mRNA-mediated intron loss in the human-pathogenic fungus Cryptococcus neoformans. Eukaryot Cell 2006, 5:789-793. 10.1128/EC.5.5.789-793.2006, 1459680, 16682456.
23. Zhang LY, Yang YF, Niu DK. Evaluation of models of the mechanisms underlying intron loss and gain in Aspergillus fungi. J Mol Evol 2010, 71:364-373. 10.1007/s00239-010-9391-6, 20862581.
24. Yenerall P, Krupa B, Zhou L. Mechanisms of intron gain and loss in Drosophila. BMC Evol Biol 2011, 11:364. 10.1186/1471-2148-11-364, 3296678, 22182367.
25. Sharpton TJ, Neafsey DE, Galagan JE, Taylor JW. Mechanisms of intron gain and loss in Cryptococcus. Genome Biol 2008, 9:R24. 10.1186/gb-2008-9-1-r24, 2395259, 18234113.
26. Roy SW, Penny D. Patterns of intron loss and gain in plants: intron loss-dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Mol Biol Evol 2007, 24:171-181.
27. Fawcett JA, Rouzé P, Van de Peer Y. Higher intron loss rate in Arabidopsis thaliana than A. lyrata is consistent with stronger selection for a smaller genome. Mol Biol Evol 2012, 29:849-859. 10.1093/molbev/msr254, 21998273.
28. Cho S, Jin S-W, Cohen A, Ellis RE. A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 2004, 14:1207-1220. 10.1101/gr.2639304, 442136, 15231741.
29. Roy SW, Hartl DL. Very little intron loss/gain in Plasmodium: intron loss/gain mutation rates and intron number. Genome Res 2006, 16:750-756. 10.1101/gr.4845406, 1473185, 16702411.
30. Coulombe-Huntington J, Majewski J. Characterization of intron loss events in mammals. Genome Res 2007, 17:23-32. 1716263, 17108319.
31. Cohen NE, Shen R, Carmel L. The role of reverse transcriptase in intron gain and loss mechanisms. Mol Biol Evol 2012, 29:179-186. 10.1093/molbev/msr192, 21804076.
32. Sverdlov AV, Babenko VN, Rogozin IB, Koonin EV. Preferential loss and gain of introns in 3' portions of genes suggests a reverse-transcription mechanism of intron insertion. Gene 2004, 338:85-91. 10.1016/j.gene.2004.05.027, 15302409.
33. Knowles DG, McLysaght A. High rate of recent intron gain and loss in simultaneously duplicated Arabidopsis genes. Mol Biol Evol 2006, 23:1548-1557. 10.1093/molbev/msl017, 16720694.
34. Nielsen CB, Friedman B, Birren B, Burge CB, Galagan JE. Patterns of intron gain and loss in fungi. PLoS Biol 2004, 2:e422. 10.1371/journal.pbio.0020422, 532390, 15562318.
35. Lin H, Zhu W, Silva J, Gu X, Buell CR. Intron gain and loss in segmentally duplicated genes in rice. Genome Biol 2006, 7:R41. 10.1186/gb-2006-7-5-r41, 1779517, 16719932.
36. Denoeud F, Henriet S, Mungpakdee S, Aury J-M, Da Silva C, Brinkmann H, Mikhaleva J, Olsen LC, Jubin C, Canestro C, Bouquet J-M, Danks G, Poulain J, Campsteijn C, Adamski M, Cross I, Yadetie F, Muffato M, Louis A, Butcher S, Tsagkogeorga G, Konrad A, Singh S, Jensen MF, Cong EH, Eikeseth-Otteraa H, Noel B, Anthouard V, Porcel BM, Kachouri-Lafond R, et al. Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 2010, 330:1381-1385. 10.1126/science.1194167, 21097902.
37. Feiber AL, Rangarajan J, Vaughn JC. The evolution of single-copy Drosophila nuclear 4f-rnp genes: spliceosomal intron losses create polymorphic alleles. J Mol Evol 2002, 55:401-413. 10.1007/s00239-002-2336-y, 12355261.
38. Niu D-K, Hou W-R, Li S-W. mRNA-mediated intron losses: evidence from extraordinarily large exons. Mol Biol Evol 2005, 22:1475-1481. 10.1093/molbev/msi138, 15788745.
39. Esnault C, Maestre J, Heidmann T. Human LINE retrotransposons generate processed pseudogenes. Nat Genet 2000, 24:363-367. 10.1038/74184, 10742098.
40. Goncalves I, Duret L, Mouchiroud D. Nature and structure of human genes that generate retropseudogenes. Genome Res 2000, 10:672-678. 10.1101/gr.10.5.672, 310883, 10810090.
41. Zhang ZL, Harrison P, Gerstein M. Identification and analysis of over 2000 ribosomal protein pseudogenes in the human genome. Genome Res 2002, 12:1466-1482. 10.1101/gr.331902, 187539, 12368239.
42. Pavlicek A, Gentles AJ, Paces J, Paces V, Jurka J. Retroposition of processed pseudogenes: the impact of RNA stability and translational control. Trends Genet 2006, 22:69-73. 10.1016/j.tig.2005.11.005, 1379630, 16356584.
43. McDonell L, Drouin G. The abundance of processed pseudogenes derived from glycolytic genes is correlated with their expression level. Genome 2012, 55:147-151. 10.1139/g2012-002, 22309162.
44. Karro JE, Yan YP, Zheng DY, Zhang ZL, Carriero N, Cayting P, Harrrison P, Gerstein M. Pseudogene.org: a comprehensive database and comparison platform for pseudogene annotation. Nucleic Acids Res 2007, 35:D55-D60. 10.1093/nar/gkl851, 1669708, 17099229.
45. Finnegan DJ. Retrotransposons. Curr Biol 2012, 22:R432-R437. 10.1016/j.cub.2012.04.025, 22677280.
46. Ensembl BioMart. , http://www.ensembl.org/biomart/martview
47. Friedel CC, Doelken L, Ruzsics Z, Koszinowski UH, Zimmer R. Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res 2009, 37:e115. 10.1093/nar/gkp542, 2761256, 19561200.
48. BioGPS. , http://biogps.org
49. Sakurai A, Fujimori S, Kochiwa H, Kitamura-Abe S, Washio T, Saito R, Carninci P, Hayashizaki Y, Tomita M. On biased distribution of introns in various eukaryotes. Gene 2002, 300:89-95. 10.1016/S0378-1119(02)01035-1, 12468090.
50. Lin K, Zhang D-Y. The excess of 5' introns in eukaryotic genomes. Nucleic Acids Res 2005, 33:6522-6527. 10.1093/nar/gki970, 1292992, 16314314.
51. Shee C, Gibson JL, Darrow MC, Gonzalez C, Rosenberg SM. Impact of a stress-inducible switch to mutagenic repair of DNA breaks on mutation in Escherichia coli. Proc Natl Acad Sci USA 2011, 108:13659-13664. 10.1073/pnas.1104681108, 3158223, 21808005.
52. Kim N, Jinks-Robertson S. Transcription as a source of genome instability. Nat Rev Genet 2012, 13:204-214. 3376450, 22330764.
53. Lippert MJ, Kim N, Cho J-E, Larson RP, Schoenly NE, O'Shea SH, Jinks-Robertson S. Role for topoisomerase 1 in transcription-associated mutagenesis in yeast. Proc Natl Acad Sci USA 2011, 108:698-703. 10.1073/pnas.1012363108, 3021083, 21177427.
54. Takahashi T, Burguiere-Slezak G, Van der Kemp PA, Boiteux S. Topoisomerase 1 provokes the formation of short deletions in repeated sequences upon high transcription in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 2011, 108:692-697. 10.1073/pnas.1012582108, 3021075, 21177431.
55. Balasubramanian S, Zheng DY, Liu YJ, Fang G, Frankish A, Carriero N, Robilotto R, Cayting P, Gerstein M. Comparative analysis of processed ribosomal protein pseudogenes in four mammalian genomes. Genome Biol 2009, 10:R2. 10.1186/gb-2009-10-1-r2, 2687790, 19123937.
56. Podlaha O, Zhang J. Processed pseudogenes: the 'fossilized footprints' of past gene expression. Trends Genet 2009, 25:429-434. 10.1016/j.tig.2009.09.002, 2764836, 19796837.
57. Castillo-Davis CI, Mekhedov SL, Hartl DL, Koonin EV, Kondrashov FA. Selection for short introns in highly expressed genes. Nat Genet 2002, 31:415-418.
58. Li SW, Feng L, Niu DK. Selection for the miniaturization of highly expressed genes. Biochem Biophys Res Commun 2007, 360:586-592. 10.1016/j.bbrc.2007.06.085, 17610841.
59. Seoighe C, Gehring C, Hurst LD. Gametophytic selection in Arabidopsis thaliana supports the selective model of intron length reduction. PLoS Genet 2005, 1:e13. 10.1371/journal.pgen.0010013, 1186733, 16110339.
60. Carmel L, Koonin EV. A universal nonmonotonic relationship between gene compactness and expression levels in multicellular eukaryotes. Genome Biol Evol 2009, 1:382-390. 2817431, 20333206.
61. Huang Y-F, Niu D-K. Evidence against the energetic cost hypothesis for the short introns in highly expressed genes. BMC Evol Biol 2008, 8:154. 10.1186/1471-2148-8-154, 2424036, 18492248.
62. Pickrell JK, Pai AA, Gilad Y, Pritchard JK. Noisy splicing drives mRNA isoform diversity in human cells. PLoS Genet 2010, 6:e1001236. 10.1371/journal.pgen.1001236, 3000347, 21151575.
63. Eickbush TH, Furano AV. Fruit flies and humans respond differently to retrotransposons. Curr Opin Genet Dev 2002, 12:669-674. 10.1016/S0959-437X(02)00359-3, 12433580.
64. Farlow A, Meduri E, Dolezal M, Hua L, Schlotterer C. Nonsense-mediated decay enables intron gain in Drosophila. PLoS Genet 2010, 6:e1000819. 10.1371/journal.pgen.1000819, 2809761, 20107520.
65. Lynch M. Intron evolution as a population-genetic process. Proc Natl Acad Sci USA 2002, 99:6118-6123. 10.1073/pnas.092595699, 122912, 11983904.
66. Llopart A, Comeron JM, Brunet FG, Lachaise D, Long M. Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection. Proc Natl Acad Sci USA 2002, 99:8121-8126. 10.1073/pnas.122570299, 123031, 12060758.
67. Niu DK. Exon definition as a potential negative force against intron losses in evolution. Biol Direct 2008, 3:46. 10.1186/1745-6150-3-46, 2614967, 19014515.
68. Carmel L, Wolf YI, Rogozin IB, Koonin EV. Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Res 2007, 17:1034-1044. 10.1101/gr.6438607, 1899114, 17495008.
69. Ensembl. , http://www.ensembl.org
70. NCBI. , ftp://ftp.ncbi.nih.gov/genomes/
71. Pseudogene.org. , http://www.pseudogene.org
72. Ng M-P, Vergara I, Frech C, Chen Q, Zeng X, Pei J, Chen N. OrthoClusterDB: an online platform for synteny blocks. BMC Bioinformatics 2009, 10:192. 10.1186/1471-2105-10-192, 2711082, 19549318.
73. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and clustal X version 2.0. Bioinformatics 2007, 23:2947-2948. 10.1093/bioinformatics/btm404, 17846036.
74. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011, 7:539. 3261699, 21988835.
75. Kaessmann H, Vinckenbosch N, Long MY. RNA-based gene duplication: mechanistic and evolutionary insights. Nat Rev Genet 2009, 10:19-31.
76. Bourque G, Pevzner PA, Tesler G. Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. Genome Res 2004, 14:507-516. 10.1101/gr.1975204, 383294, 15059991.
77. Fablet M, Bueno M, Potrzebowski L, Kaessmann H. Evolutionary origin and functions of retrogene introns. Mol Biol Evol 2009, 26:2147-2156. 10.1093/molbev/msp125, 19553367.
78. Repbase. , http://www.girinst.org/repbase/