Recurrent Loss of Specific Introns during Angiosperm Evolution
The spliceosomal introns are nucleotide sequences that interrupt coding regions of eukaryotic genes and are removed by RNA splicing after transcription. Recent studies have reported several examples of possible recurrent intron loss or gain, i.e., introns that are independently removed from or inserted into the identical sites more than once in an investigated phylogeny. However, the frequency, evolutionary patterns or other characteristics of recurrent intron turnover remain unknown. We provide results for the first comprehensive analysis of recurrent intron turnover within a plant family and show that recurrent intron loss represents a considerable portion of all intron losses identified and intron loss events far outnumber intron gain events. We also demonstrate that recurrent intron loss is non-random, affecting only a small number of introns that are repeatedly lost, and that different lineages show significantly different rates of intron loss. Our results suggest a possible role of DNA methylation in the process of intron loss. Moreover, this study provides strong support for the model of intron loss by reverse transcriptase mediated conversion of genes by their processed mRNA transcripts.
Vyšlo v časopise:
Recurrent Loss of Specific Introns during Angiosperm Evolution. PLoS Genet 10(12): e32767. doi:10.1371/journal.pgen.1004843
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1004843
Souhrn
The spliceosomal introns are nucleotide sequences that interrupt coding regions of eukaryotic genes and are removed by RNA splicing after transcription. Recent studies have reported several examples of possible recurrent intron loss or gain, i.e., introns that are independently removed from or inserted into the identical sites more than once in an investigated phylogeny. However, the frequency, evolutionary patterns or other characteristics of recurrent intron turnover remain unknown. We provide results for the first comprehensive analysis of recurrent intron turnover within a plant family and show that recurrent intron loss represents a considerable portion of all intron losses identified and intron loss events far outnumber intron gain events. We also demonstrate that recurrent intron loss is non-random, affecting only a small number of introns that are repeatedly lost, and that different lineages show significantly different rates of intron loss. Our results suggest a possible role of DNA methylation in the process of intron loss. Moreover, this study provides strong support for the model of intron loss by reverse transcriptase mediated conversion of genes by their processed mRNA transcripts.
Zdroje
1. FedorovA, MericanAF, GilbertW (2002) Large-scale comparison of intron positions among animal, plant, and fungal genes. Proc Natl Acad Sci U S A 99: 16128–16133.
2. RogozinIB, WolfYI, SorokinAV, MirkinBG, KooninEV (2003) Remarkable interkingdom conservation of intron positions and massive, lineage-specific intron loss and gain in eukaryotic evolution. Curr Biol 13: 1512–1517.
3. RogozinIB, CarmelL, CsurosM, KooninEV (2012) Origin and evolution of spliceosomal introns. Biol Direct 7: 11.
4. Rodriguez-TrellesF, TarrioR, AyalaFJ (2006) Origins and evolution of spliceosomal introns. Annu Rev Genet 40: 47–76.
5. RoySW, GilbertW (2006) The evolution of spliceosomal introns: patterns, puzzles and progress. Nat Rev Genet 7: 211–221.
6. JeffaresDC, MourierT, PennyD (2006) The biology of intron gain and loss. Trends Genet 22: 16–22.
7. CsurosM, RogozinIB, KooninEV (2008) Extremely intron-rich genes in the alveolate ancestors inferred with a flexible maximum-likelihood approach. Mol Biol Evol 25: 903–911.
8. CsurosM, RogozinIB, KooninEV (2011) A detailed history of intron-rich eukaryotic ancestors inferred from a global survey of 100 complete genomes. PLoS Comput Biol 7: e1002150.
9. KrzywinskiJ, BesanskyNJ (2002) Frequent intron loss in the white gene: a cautionary tale for phylogeneticists. Mol Biol Evol 19: 362–366.
10. Coulombe-HuntingtonJ, MajewskiJ (2007) Characterization of intron loss events in mammals. Genome Res 17: 23–32.
11. ZhanLL, DingZ, QianYH, ZengQT (2012) Convergent intron loss of MRP1 in Drosophila and mosquito species. J Hered 103: 147–151.
12. LiW, TuckerAE, SungW, ThomasWK, LynchM (2009) Extensive, recent intron gains in Daphnia populations. Science 326: 1260–1262.
13. TarrioR, Rodriguez-TrellesF, AyalaFJ (2003) A new Drosophila spliceosomal intron position is common in plants. Proc Natl Acad Sci U S A 100: 6580–6583.
14. HankelnT, FriedlH, EbersbergerI, MartinJ, SchmidtER (1997) A variable intron distribution in globin genes of Chironomus: evidence for recent intron gain. Gene 205: 151–160.
15. DibbNJ, NewmanAJ (1989) Evidence that introns arose at proto-splice sites. EMBO J 8: 2015–2021.
16. QiuWG, SchislerN, StoltzfusA (2004) The evolutionary gain of spliceosomal introns: sequence and phase preferences. Mol Biol Evol 21: 1252–1263.
17. SverdlovAV, RogozinIB, BabenkoVN, KooninEV (2005) Conservation versus parallel gains in intron evolution. Nucleic Acids Res 33: 1741–1748.
18. CarmelL, RogozinIB, WolfYI, KooninEV (2007) Patterns of intron gain and conservation in eukaryotic genes. BMC Evol Biol 7: 192.
19. RoySW, FedorovA, GilbertW (2003) Large-scale comparison of intron positions in mammalian genes shows intron loss but no gain. Proc Natl Acad Sci U S A 100: 7158–7162.
20. ChoS, JinSW, CohenA, EllisRE (2004) A phylogeny of caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14: 1207–1220.
21. StajichJE, DietrichFS, RoySW (2007) Comparative genomic analysis of fungal genomes reveals intron-rich ancestors. Genome Biol 8: R223.
22. JaillonO, AuryJM, NoelB, PolicritiA, ClepetC, et al. (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449: 463–467.
23. DerrLK (1998) The involvement of cellular recombination and repair genes in RNA-mediated recombination in Saccharomyces cerevisiae. Genetics 148: 937–945.
24. BrosiusJ (1991) Retroposons—seeds of evolution. Science 251: 753.
25. McCarreyJR, ThomasK (1987) Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326: 501–505.
26. BennetzenJL, FreelingM (1997) The unified grass genome: synergy in synteny. Genome Res 7: 301–306.
27. GaleMD, DevosKM (1998) Comparative genetics in the grasses. Proc Natl Acad Sci U S A 95: 1971–1974.
28. IlicK, SanMiguelPJ, BennetzenJL (2003) A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes. Proc Natl Acad Sci U S A 100: 12265–12270.
29. LaiJ, MaJ, SwigonovaZ, RamakrishnaW, LintonE, et al. (2004) Gene loss and movement in the maize genome. Genome Res 14: 1924–1931.
30. WickerT, BuchmannJP, KellerB (2010) Patching gaps in plant genomes results in gene movement and erosion of colinearity. Genome Res 20: 1229–1237.
31. WangH, BennetzenJL (2012) Centromere retention and loss during the descent of maize from a tetraploid ancestor. Proc Natl Acad Sci U S A 109: 21004–21009.
32. LinH, ZhuW, SilvaJC, GuX, BuellCR (2006) Intron gain and loss in segmentally duplicated genes in rice. Genome Biol 7: R41.
33. Castillo-DavisCI, MekhedovSL, HartlDL, KooninEV, KondrashovFA (2002) Selection for short introns in highly expressed genes. Nat Genet 31: 415–418.
34. YuJ, HuS, WangJ, WongGK, LiS, et al. (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296: 79–92.
35. ZhuL, ZhangY, ZhangW, YangS, ChenJQ, et al. (2009) Patterns of exon-intron architecture variation of genes in eukaryotic genomes. BMC Genomics 10: 47.
36. CarelsN, HateyP, JabbariK, BernardiG (1998) Compositional properties of homologous coding sequences from plants. J Mol Evol 46: 45–53.
37. CampbellWH, GowriG (1990) Codon usage in higher plants, green algae, and cyanobacteria. Plant Physiol 92: 1–11.
38. KawabeA, MiyashitaNT (2003) Patterns of codon usage bias in three dicot and four monocot plant species. Genes Genet Syst 78: 343–352.
39. GruenbaumY, SzyfM, CedarH, RazinA (1983) Methylation of replicating and post-replicated mouse L-cell DNA. Proc Natl Acad Sci U S A 80: 4919–4921.
40. SanMiguelP, GautBS, TikhonovA, NakajimaY, BennetzenJL (1998) The paleontology of intergene retrotransposons of maize. Nat Genet 20: 43–45.
41. FengS, CokusSJ, ZhangX, ChenPY, BostickM, et al. (2010) Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci U S A 107: 8689–8694.
42. SharpPA, BurgeCB (1997) Classification of introns: U2-type or U12-type. Cell 91: 875–879.
43. YenerallP, KrupaB, ZhouL (2011) Mechanisms of intron gain and loss in Drosophila. BMC Evol Biol 11: 364.
44. RoySW, GilbertW (2005) Complex early genes. Proc Natl Acad Sci U S A 102: 1986–1991.
45. RoySW, GilbertW (2005) Rates of intron loss and gain: implications for early eukaryotic evolution. Proc Natl Acad Sci U S A 102: 5773–5778.
46. NielsenCB, FriedmanB, BirrenB, BurgeCB, GalaganJE (2004) Patterns of intron gain and loss in fungi. PLoS Biol 2: e422.
47. RoySW, PennyD (2007) 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 24: 171–181.
48. FawcettJA, RouzeP, Van de PeerY (2011) Higher intron loss rate in Arabidopsis thaliana than A. lyrata is consistent with stronger selection for a smaller genome. Mol Biol Evol 29: 849–859.
49. CohenNE, ShenR, CarmelL (2011) The role of reverse transcriptase in intron gain and loss mechanisms. Mol Biol Evol 29: 179–186.
50. RogersJH (1989) How were introns inserted into nuclear genes? Trends Genet 5: 213–216.
51. IrimiaM, RukovJL, PennyD, VintherJ, Garcia-FernandezJ, et al. (2008) Origin of introns by 'intronization' of exonic sequences. Trends Genet 24: 378–381.
52. CataniaF, LynchM (2008) Where do introns come from? PLoS Biol 6: e283.
53. WesslerSR, BaranG, VaragonaM (1987) The maize transposable element Ds is spliced from RNA. Science 237: 916–918.
54. FridellRA, PretAM, SearlesLL (1990) A retrotransposon 412 insertion within an exon of the Drosophila melanogaster vermilion gene is spliced from the precursor RNA. Genes Dev 4: 559–566.
55. GirouxMJ, ClancyM, BaierJ, InghamL, McCartyD, et al. (1994) De novo synthesis of an intron by the maize transposable element Dissociation. Proc Natl Acad Sci U S A 91: 12150–12154.
56. FarlowA, MeduriE, DolezalM, HuaL, SchlottererC (2010) Nonsense-mediated decay enables intron gain in Drosophila. PLoS Genet 6: e1000819.
57. Cavalier-SmithT (1985) Selfish DNA and the origin of introns. Nature 315: 283–284.
58. SharpPA (1985) On the origin of RNA splicing and introns. Cell 42: 397–400.
59. RoySW, IrimiaM (2009) Mystery of intron gain: new data and new models. Trends Genet 25: 67–73.
60. ZhangLY, YangYF, NiuDK (2010) Evaluation of models of the mechanisms underlying intron loss and gain in Aspergillus fungi. J Mol Evol 71: 364–373.
61. WordenAZ, LeeJH, MockT, RouzeP, SimmonsMP, et al. (2009) Green evolution and dynamic adaptations revealed by genomes of the marine picoeukaryotes Micromonas. Science 324: 268–272.
62. TorrianiSF, StukenbrockEH, BrunnerPC, McDonaldBA, CrollD (2011) Evidence for extensive recent intron transposition in closely related fungi. Curr Biol 21: 2017–2022.
63. van der BurgtA, SeveringE, de WitPJ, CollemareJ (2012) Birth of new spliceosomal introns in fungi by multiplication of introner-like elements. Curr Biol 22: 1260–1265.
64. VerhelstB, Van de PeerY, RouzeP (2013) The complex intron landscape and massive intron invasion in a picoeukaryote provides insights into intron evolution. Genome Biol Evol 5: 2393–2401.
65. KassSU, PrussD, WolffeAP (1997) How does DNA methylation repress transcription? Trends Genet 13: 444–449.
66. JonesPA, TaylorSM (1980) Cellular differentiation, cytidine analogs and DNA methylation. Cell 20: 85–93.
67. RobertsonHM (1998) Two large families of chemoreceptor genes in the nematodes Caenorhabditis elegans and Caenorhabditis briggsae reveal extensive gene duplication, diversification, movement, and intron loss. Genome Res 8: 449–463.
68. LlopartA, ComeronJM, BrunetFG, LachaiseD, LongM (2002) Intron presence-absence polymorphism in Drosophila driven by positive Darwinian selection. Proc Natl Acad Sci U S A 99: 8121–8126.
69. DerrLK, StrathernJN (1993) A role for reverse transcripts in gene conversion. Nature 361: 170–173.
70. FinkGR (1987) Pseudogenes in yeast? Cell 49: 5–6.
71. DenoeudF, HenrietS, MungpakdeeS, AuryJM, Da SilvaC, et al. (2010) Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330: 1381–1385.
72. FeiberAL, RangarajanJ, VaughnJC (2002) The evolution of single-copy Drosophila nuclear 4f-rnp genes: spliceosomal intron losses create polymorphic alleles. J Mol Evol 55: 401–413.
73. NiuDK, HouWR, LiSW (2005) mRNA-mediated intron losses: evidence from extraordinarily large exons. Mol Biol Evol 22: 1475–1481.
74. SharptonTJ, NeafseyDE, GalaganJE, TaylorJW (2008) Mechanisms of intron gain and loss in Cryptococcus. Genome Biol 9: R24.
75. ZhuT, NiuDK (2013) Frequency of intron loss correlates with processed pseudogene abundance: a novel strategy to test the reverse transcriptase model of intron loss. BMC Biol 11: 23.
76. FangW, LandweberLF (2013) RNA-mediated genome rearrangement: hypotheses and evidence. Bioessays 35: 84–87.
77. VogelJP, GarvinDF, MocklerTC, SchmutzJ, RokhsarD, et al. (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463: 763–768.
78. BennetzenJL, SchmutzJ, WangH, PercifieldR, HawkinsJ, et al. (2012) Reference genome sequence of the model plant Setaria. Nat Biotechnol 30: 555–561.
79. PatersonAH, BowersJE, BruggmannR, DubchakI, GrimwoodJ, et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457: 551–556.
80. SchnablePS, WareD, FultonRS, SteinJC, WeiF, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112–1115.
81. WolfgruberTK, SharmaA, SchneiderKL, AlbertPS, KooDH, et al. (2009) Maize centromere structure and evolution: sequence analysis of centromeres 2 and 5 reveals dynamic Loci shaped primarily by retrotransposons. PLoS Genet 5: e1000743.
82. LiL, StoeckertCJJr, RoosDS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178–2189.
83. AbascalF, ZardoyaR, TelfordMJ (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38: W7–13.
84. BennetzenJL, ColemanC, LiuR, MaJ, RamakrishnaW (2004) Consistent over-estimation of gene number in complex plant genomes. Curr Opin Plant Biol 7: 732–736.
85. StoltzfusA, LogsdonJMJr, PalmerJD, DoolittleWF (1997) Intron "sliding" and the diversity of intron positions. Proc Natl Acad Sci U S A 94: 10739–10744.
86. ChawSM, ChangCC, ChenHL, LiWH (2004) Dating the monocot-dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58: 424–441.
87. WolfeKH, GouyM, YangYW, SharpPM, LiWH (1989) Date of the monocot-dicot divergence estimated from chloroplast DNA sequence data. Proc Natl Acad Sci U S A 86: 6201–6205.
88. ChalupskaD, LeeHY, FarisJD, EvrardA, ChalhoubB, et al. (2008) Acc homoeoloci and the evolution of wheat genomes. Proc Natl Acad Sci U S A 105: 9691–9696.
89. SwigonovaZ, LaiJ, MaJ, RamakrishnaW, LlacaV, et al. (2004) Close split of sorghum and maize genome progenitors. Genome Res 14: 1916–1923.
90. DuZ, ZhouX, LingY, ZhangZ, SuZ (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38: W64–70.
91. BenjaminiY, YekutieliD (2001) The control of the false discovery rate in multiple testing under dependency. Annals of Statistics 29: 1165–1188.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
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