Intron evolution in Neurospora: The role of mutational bias and selection

Genome Research

Volumn 25, Issue 1, 2015, Pages 100-110

  Sun, Yu ^a,b   Whittle, Carrie A ^a   Corcoran, Pádraic ^a   Johannesson, Hanna ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NUCLEOTIDE; FUNGAL DNA; MITOCHONDRIAL DNA;

ARTICLE; DNA END JOINING REPAIR; EUKARYOTE; GENE LOSS; GENETIC GAIN; GENETIC PARAMETERS; GENOME; GENOMICS; INTRON; NATURAL POPULATION; NEUROSPORA; NONHUMAN; PRIORITY JOURNAL; SELECTIVE SWEEP; CLASSIFICATION; DNA SEQUENCE; FUNGAL GENOME; GENE FREQUENCY; GENETIC SELECTION; GENETICS; MOLECULAR EVOLUTION; MUTATION; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM;

EUKARYOTA; NEUROSPORA; NEUROSPORA CRASSA; NEUROSPORA DISCRETA; NEUROSPORA TETRASPERMA;

DNA END-JOINING REPAIR; DNA, FUNGAL; DNA, MITOCHONDRIAL; EVOLUTION, MOLECULAR; GENE FREQUENCY; GENETICS, POPULATION; GENOME, FUNGAL; INTRONS; MUTATION; NEUROSPORA; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, MESSENGER; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA;

EID: 84920685396     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.175653.114     Document Type: Article

References (84)

1. Akashi H, Schaeffer SW. 1997. Natural selection and the frequency distributions of "silent"DNApolymorphism in Drosophila. Genetics 146: 295-307.
2. Amit M, Donyo M, Hollander D, Goren A, Kim E, Gelfman S, Lev-Maor G, Burstein D, Schwartz S, Postolsky B, et al. 2012. Differential GC content between exons and introns establishes distinct strategies of splice-site recognition. Cell Reports 1: 543-556.
3. Basu MK, MakalowskiW, Rogozin IB, Koonin EV. 2008. U12 intron positions are more strongly conserved between animals and plants than U2 intron positions. Biol Direct 3: 19.
4. Berget SM, Moore C, Sharp PA. 1977. Spliced segments at the 59 terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci 74: 3171-3175.
5. Bernstein LB, Mount SM, Weiner AM. 1983. Pseudogenes for human small nuclear RNA U3 appear to arise by integration of self-primed reverse transcripts of the RNA into new chromosomal sites. Cell 32: 461-472.
6. Boeke JD, Garfinkel DJ, Styles CA, Fink GR. 1985. Ty elements transpose through an RNA intermediate. Cell 40: 491-500.
7. Brunner PC, Torriani SF, Croll D, Stukenbrock EH, McDonald BA. 2014. Hitchhiking selection is driving intron gain in a pathogenic fungus. Mol Biol Evol 31: 1741-1749.
8. The C. elegans Sequencing Consortium. 1998. Genome sequence of the nematode C. elegans: A platform for investigating biology. Science 282: 2012-2018.
9. Carmel L, Wolf YI, Rogozin IB, Koonin EV. 2007. Three distinct modes of intron dynamics in the evolution of eukaryotes. Genome Res 17: 1034-1044.
10. Castellana S, Vicario S, Saccone C. 2011. Evolutionary patterns of the mitochondrial genome in Metazoa: Exploring the role of mutation and selection in mitochondrial protein coding genes. Genome Biol Evol 3: 1067-1079.
11. Charlesworth B. 2009. Fundamental concepts in genetics: Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10: 195-205.
12. Chorev M, Carmel L. 2012. The function of introns. Front Genet 3: 55.
13. Chow LT, Gelinas RE, Broker TR, Roberts RJ. 1977. An amazing sequence arrangement at the 59 ends of adenovirus 2 messenger RNA. Cell 12: 1-8.
14. Collemare J, Burgt Avd, de Wit PJ. 2013. At the origin of spliceosomal introns: Is multiplication of introner-like elements the main mechanism of intron gain in fungi? Commun Integr Biol 6: E2314 7.
15. Corcoran P, Dettman J, Sun Y, Luque E, Corrochano L, Taylor J, Lascoux M, Johannesson H. 2014. A global multilocus analysis of the model fungus Neurospora reveals a single recent origin of a novel ge netic system. Mol Phylogenet Evol 78: 136-147.
16. Coulombe-Huntington J,Majewski J. 2007 a . Characterization of intron loss events in mammals. Genome Res 17: 23-32.
17. Coulombe-Huntington J Majewski J. 2007b Intron loss and gain in Drosophila. Mol Biol Evol 24 2842-2850.
18. Croll D, McDonald BA. 2012. Intron gains and losses in the evolution of Fusarium and Cryptococcus fungi. Genome Biol Evol 4: 1148-1161.
19. Csuros M, Rogozin IB, Koonin EV. 2011. A detailed history of intron-rich eukaryotic ancestors inferred from a global survey of 100 complete genomes. PLoS Comput Biol 7: E1002150.
20. Denoeud F, Henriet S, Mungpakdee S, Aury JM, Da Silva C, Brinkmann H, Mikhal eva J, Olsen LC, Jubin C, Canestro C, et al. 2010. Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330: 1381-1385.
21. Derr LK, Strathern JN. 1993 . A role for reverse transcripts in gene conversion. Nature 361: 170-173.
22. Dettman JR, Jacobson DJ, Taylor JW. 2003. A multilocus genealogical approach to phylogenetic species recognition in the model eukaryote Neurospora. Evolution 57: 2703-2720.
23. Dodge BO. 1927. Nuclear phenomena associated with heterothallism and homothallism in the ascomycete Neurospora. J Agric Res 35: 0289-0305.
24. Douglas S, Zauner S, FraunholzM, BeatonM, Penny S, Deng LT,Wu X, Reith M, Cavalier-Smith T, Maier UG. 2001. The highly reduced genome of an enslaved algal nucleus. Nature 410: 1091-1096.
25. Ellison CE, Hall C, Kowbel D,Welch J, Brem RB, Glass NL, Taylor JW. 2011a. Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Natl Acad Sci 108: 2831-2836.
26. Ellison CE, Stajich JE, Jacobson DJ, Natvig DO, Lapidus A, Foster B, Aerts A, Riley R, Lindquist EA, Grigoriev IV, et al. 2011b. Massive changes in genome architecture accompany the transition to self-fertility in the filamentous fungus Neurospora tetrasperma. Genetics 189: 55-69.
27. Evans RM, Fraser N, Ziff E, Weber J, Wilson M, Darnell JE. 1977. The initiation sites for RNA transcription in Ad2 DNA. Cell 12: 733-739.
28. Farlow A, Meduri E, Dolezal M, Hua L, Schlotterer C. 2010. Nonsensemediated decay enables intron gain in Drosophila. PLoS Genet 6: E1000819.
29. Farlow A, Med uri E, Schlotterer C. 2011. DNA double-strand break repair and the evolution of intron density. Trends Genet 27: 1-6. Fink GR. 1987. Pseudogenes in yeast? Cell 49: 5-6.
30. Galagan JE, Calvo SE, Borkovich KA, Selker EU, Read ND, Jaffe D, FitzHugh W, Ma LJ, Smirnov S, Purcell S, et al. 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422: 859-868.
31. Gilbert W. 1987. The exon theory of genes. Cold Spring Harb Sym 52: 901-905.
32. Goldberg S, Schwartz H, Darnell JE Jr. 1977. Evidence from UV transcription mapping in HeLa cells that heterogeneous nuclear RNA is the messenger RNA precursor. Proc Natl Acad Sci 74: 4520-4523.
33. Ha ddrill PR, Bachtrog D, Andolfatto P. 2008. Positive and negative selection on noncoding DNA in Drosophila simulans. Mol Biol Evol 25: 1825-1834.
34. Harris RS. 2007. " Improved pairwise alignment of ge nomic DNA." PhD thesis, The Pennsylvania State University, State College, P.A.
35. Hudson RR, Boos DD, Kaplan NL. 1992. A statistical test for detecting geographic subdivision. Mol Biol Evol 9: 138-151.
36. Jackson DA, Pombo A, Iborra F. 2000. The balance sheet for transcription: An analysis of nuclear RNA metabolism in mammalian cells. FASEB J 14: 242-254.
37. Jeffares DC, Mourier T, Penny D. 2006. The biology of intron gain and loss. Trends Genet 22: 16-22.
38. Johnson RD, Jasin M. 2000. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J 19: 3398-3407.
39. Kasuga T, White TJ, Taylor JW. 2002. Estimation of nucleotide substitution rates in Eurotiomycete fungi. Mol Biol Evol 19: 2318-2324.
40. Katinka MD Duprat S Cornillot E Metenier G Thomarat F Prensier G Barbe V Peyretaillade E Brottier P Wincker Pet al. 2001 Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi Nature 414 450-453
41. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
42. Kent WJ. 2002. BLAT-The BLAST-like alignment tool. Genome Res 12: 656-664.
43. Leushkin EV, Bazykin GA, Kondrashov AS. 2013. Strong mutational bias toward deletions in the Drosophila melanogaster genome is compensated by selection. Genome Biol Evol 5: 514-524.
44. Lewin R. 1983. How mammalian RNA returns to its genome. Science 219: 1052-1054.
45. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
46. Li W, Tucker AE, Sung W, Thomas WK, Lynch M. 2009. Extensive, recent intron gains in Daphnia populations. Science 326: 1260-1262.
47. Li R, Zhu H, Ruan J, QianW, Fang X, Shi Z, Li Y, Li S, Shan G, Kristiansen K, et al. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20: 26 5-272.
48. Llopart A, Comeron JM, Brunet FG, Lachaise D, Long M. 2002. Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection. Proc Natl Acad Sci 99: 8121-8126.
49. Logsdon JM. 1998. The recent origins of spliceosomal introns revisited. Curr Opin Genet Dev 8: 637-648.
50. Lynch M. 2002. Intron evolution as a population-genetic process. Proc Natl Acad Sci 99: 6118-6123.
51. Lynch M. 2007. The origins of genome architecture. Sinauer Associates, Sunderland, MA.
52. Lynch M, Conery JS. 2003. The origins of genome complexity. Science 302: 1401-1404.
53. Mao Z, Bozzella M, Seluanov A, Gorbunova V. 2008. Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair (Amst) 7: 1765-1771.
54. Marais G, Nouvellet P, Keightley PD, Charlesworth B. 2005. Intron size and exon evolution in Drosophila. Genetics 170: 481-485.
55. Menkis A, Jacobson DJ, Gustafsson T, Johannesson H. 2008. T he matingtype chromosome in the filamentous ascomycete Neurospora tetrasperma represents a model for early evolution of sex chromosomes. PLoS Genet 4: E1000030.
56. Menkis A, Bastiaans E, Jacobson DJ, Johannesson H. 2009. Phylogenetic and biological species diversity within the Neurospora tetrasperma complex. J Evol Biol 22: 1923-1936.
57. Mourier T, Jeffares DC. 2003. Eukaryotic intron loss. Science 300: 1393.
58. Nielsen CB, Friedman B, Birren B, Burge CB, Galagan JE. 2004. Patterns of intron gain and loss in fungi. PLoS Biol 2: E422.
59. Nygren K, Strandberg R, Wallberg A, Nabholz B, Gustafsson T, Garcia D, Cano J, Guarro J, Johannesson H. 2011. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Mol Phylogenet Evol 59: 649-663.
60. Preston CR, Flores CC, Engels WR. 2006. Differential usage of alternative pathways of double-strand break repair in Drosophila. Genetics 172: 1055-1068.
61. Przeworski M Charlesworth B Wall JD. 1999. Genealogies and weak purifying selection. Mol Biol Evol 16 246-252.
62. Rebuzzini P, Khoriauli L, Azzalin CM,Magnani E, MondelloC,Giulotto E. 2005. New mammalian cellular systems to study mutations introduced at the break site by non-homologous end-joining. DNA Repair (Amst) 4: 546-555.
63. Rogozin IB, Wolf YI, Sorokin AV, Mirkin BG, Koonin EV . 2003. Remarkable interkingdom conservation of intron positions and massive, lineagespecific intron loss and gain in eukaryotic evolution. Curr Biol 13: 1512-1517.
64. Rogozin IB, Carmel L, Csuros M, Koonin EV. 2012. Origin and evolution of spliceosomal introns. Biol Direct 7: 11.
65. Roy SW,GilbertW. 2005. Rates of intron loss and gain: Implications for early eukaryotic evolution. Proc Natl Acad Sci 102: 5773-5778.
66. Roy SW, Gilbert W. 2006. The evolution of spliceosomal introns: Patterns, puzzles and progress. Nat Rev Genet 7: 211-221.
67. Roy SW, Irimia M. 2012. Genome evolution: Where do new introns come from? Curr Biol 22: R529-R531.
68. Roy SW, Fedorov A, Gilbert W. 2003. Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc Natl Acad Sci 100: 7158-7162.
69. Sharpton TJ, Neafsey DE, Galagan JE, Taylor JW. 2008. Mechanisms of intron gain and loss in Cryptococcus. Genome Biol 9: R24.
70. Shimizu K, Li HM, Virtudazo EV, Watanabe A, Kamei K, Yamaguchi M, Kawamoto S. 2010. Deletion of CnLIG4 DNA ligase gene in the fungal pathogen Cryptococcus neoformans elevates homologous recombination efficiency. M ycoscience 51: 28-33.
71. Smit AFA,Hubley R,Green P. 1996-2010. RepeatMaskerOpen-3.0. http://www. repeatmasker.org.
72. Stamatakis A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.
73. Sun Y, Corcoran P, Menkis A, Whittle CA, Andersson SG, Johannesson H. 2012. Large-scale introgression shapes the evolution of the mating-type chromosomes of the filamentous ascomycete Neurospora tetrasperma. PLoS Genet 8: E1002820.
74. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
75. Torriani SF, Stukenbrock EH, Brunner PC, McDonald BA, Croll D. 2011. Evidence for extensive recent intron transposition in closely related fungi. Curr Biol 21: 2017-2022.
76. van der Burgt A, Severing E, de Wit PJ, Collemare J. 2012. Birth of new spliceosomal introns in fungi by multiplication of introner-like elements. Curr Biol 22: 1260-1265.
77. Wang D, Yu J. 2011. Both size and GC-content of minimal introns are selected in human populations. PLoS ONE 6: E17945.
78. Whittle CA, Sun Y, Johannesson H. 2011a. Deg eneration in codon usage within the young segment of suppressed recombination in themating type chromosomes of Neurospora tetrasperma. Eukaryot Cell 10: 594-603.
79. Whittle CA, Sun Y, Johannesson H. 2011b. Evolution of synonymous codon usage in Neurospora tetrasperma and Neurospora discreta. Genome Biol Evol 3: 332-343.
80. Whittle CA, Sun Y, Johannesson H. 2012. Genome-wide selection on codon usage at the population level in the fungal model organism Neurospora crassa. Mol Biol Evol 29: 1975 -1986.
81. Wood V, Gwilliam R, Rajandream MA, Lyne M, Lyne R, Stewart A, Sgouros J, Peat N, Hayles J, Baker S, et al. 2002. The genome sequence of Schizosaccharomyces pombe. Nature 415: 871-880.
82. Yenerall P Zhou L 2012 Identifying the mechanisms of intron gain: Progress and trends. Biol Direct 7 29.
83. Y enerall P, Krupa B, Zhou L. 2011. Mechanisms of intron gain and loss in Drosophila. BMC Evol Biol 11: 364.
84. Zhang LY, Yang YF, Niu DK. 2010. Evaluation of models of the mechanisms underlying intron loss and gain in Aspergillus fungi. J Mol Evol 71: 364-373.