Nonsense-Mediated Decay Enables Intron Gain in
Intron number varies considerably among genomes, but despite their fundamental importance, the mutational mechanisms and evolutionary processes underlying the expansion of intron number remain unknown. Here we show that Drosophila, in contrast to most eukaryotic lineages, is still undergoing a dramatic rate of intron gain. These novel introns carry significantly weaker splice sites that may impede their identification by the spliceosome. Novel introns are more likely to encode a premature termination codon (PTC), indicating that nonsense-mediated decay (NMD) functions as a backup for weak splicing of new introns. Our data suggest that new introns originate when genomic insertions with weak splice sites are hidden from selection by NMD. This mechanism reduces the sequence requirement imposed on novel introns and implies that the capacity of the spliceosome to recognize weak splice sites was a prerequisite for intron gain during eukaryotic evolution.
Vyšlo v časopise:
Nonsense-Mediated Decay Enables Intron Gain in. PLoS Genet 6(1): e32767. doi:10.1371/journal.pgen.1000819
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1000819
Souhrn
Intron number varies considerably among genomes, but despite their fundamental importance, the mutational mechanisms and evolutionary processes underlying the expansion of intron number remain unknown. Here we show that Drosophila, in contrast to most eukaryotic lineages, is still undergoing a dramatic rate of intron gain. These novel introns carry significantly weaker splice sites that may impede their identification by the spliceosome. Novel introns are more likely to encode a premature termination codon (PTC), indicating that nonsense-mediated decay (NMD) functions as a backup for weak splicing of new introns. Our data suggest that new introns originate when genomic insertions with weak splice sites are hidden from selection by NMD. This mechanism reduces the sequence requirement imposed on novel introns and implies that the capacity of the spliceosome to recognize weak splice sites was a prerequisite for intron gain during eukaryotic evolution.
Zdroje
1. TarrioR
AyalaFJ
Rodriguez-TrellesF
2008 Alternative splicing: a missing piece in the puzzle of intron gain. Proc Natl Acad Sci U S A 105 7223 7228
2. Coulombe-HuntingtonJ
MajewskiJ
2007 Intron Loss and Gain in Drosophila. Molecular Biology and Evolution 24 2842 2850
3. IrimiaM
RukovJL
PennyD
VintherJ
Garcia-FernandezJ
2008 Origin of introns by ‘intronization’ of exonic sequences. Trends Genet 24 378 381
4. RaggH
KumarA
KosterK
BenteleC
WangY
2009 Multiple gains of spliceosomal introns in a superfamily of vertebrate protease inhibitor genes. BMC Evol Biol 9 208
5. Cavalier-SmithT
1991 Intron phylogeny: a new hypothesis. Trends Genet 7 145 148
6. ToorN
KeatingK
TaylorS
PyleA
2008 Crystal Structure of a Self-Spliced Group II Intron. Science 77 82
7. CataniaF
LynchM
2008 Where do introns come from? PLoS Biol 6 e283 doi:10.1371/journal.pbio.0060283
8. ZhangC
LiWH
KrainerAR
ZhangMQ
2008 RNA landscape of evolution for optimal exon and intron discrimination. Proc Natl Acad Sci U S A 105 5797 5802
9. WahlMC
WillCL
LuhrmannR
2009 The spliceosome: design principles of a dynamic RNP machine. Cell 136 701 718
10. Cavalier-SmithT
1985 Selfish DNA and the origin of introns. Nature 315 283 284
11. RoySW
IrimiaM
2009 Mystery of intron gain: new data and new models. Trends Genet 25 67 73
12. PavesiG
ZambelliF
CaggeseC
PesoleG
2008 Exalign: a new method for comparative analysis of exon-intron gene structures. Nucleic Acids Res 36 e47
13. GaoX
LynchM
2009 Ubiquitous internal gene duplication and intron creation in eukaryotes. Proc Natl Acad Sci U S A
14. Li
Tucker
Sung
Thomask
Lynch
2009 Extensive, Recent Intron Gains in Daphnia Population. Science 326 1260 1262
15. CataniaF
GaoX
ScofieldDG
2009 Endogenous mechanisms for the origins of spliceosomal introns. J Hered 100 591 596
16. SayaniS
JanisM
LeeCY
ToescaI
ChanfreauGF
2008 Widespread impact of nonsense-mediated mRNA decay on the yeast intronome. Mol Cell 31 360 370
17. HansenKD
LareauLF
BlanchetteM
GreenRE
MengQ
2009 Genome-wide identification of alternative splice forms down-regulated by nonsense-mediated mRNA decay in Drosophila. PLoS Genet 5 e1000525 doi:10.1371/journal.pgen.1000525
18. NielsenC
FriedmanB
BirrenB
BurgeC
GalaganJ
2004 Patterns of Intron Gain and Loss in Fungi. Plos Biol 2 e422 doi:10.1371/journal.pbio.0020422
19. 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
20. PalmerJD
LogsdonJMJr
1991 The recent origins of introns. Curr Opin Genet Dev 1 470 477
21. CrickF
1979 Split genes and RNA splicing. Science 204 264 271
22. RogersJH
1989 How were introns inserted into nuclear genes? Trends Genet 5 213 216
23. VenkateshB
NingY
BrennerS
1999 Late changes in spliceosomal introns define clades in vertebrate evolution. Proc Natl Acad Sci U S A 96 10267 10271
24. KnowlesDG
McLysaghtA
2006 High rate of recent intron gain and loss in simultaneously duplicated Arabidopsis genes. Mol Biol Evol 23 1548 1557
25. SharptonT
NeafseyD
GalaganJ
TaylorJ
2008 Mechanisms of intron gain and loss in Cryptococcus. Genome Biol 9 R24
26. FedorovA
RoyS
FedorovaL
GilbertW
2003 Mystery of intron gain. Genome Res 13 2236 2241
27. Hazkani-CovoE
CovoS
2008 Numt-mediated double-strand break repair mitigates deletions during primate genome evolution. PLoS Genet 4 e1000237 doi:10.1371/journal.pgen.1000237
28. TanayA
SiggiaED
2008 Sequence context affects the rate of short insertions and deletions in flies and primates. Genome Biol 9 R37
29. RocaX
SachidanandamR
KrainerAR
2005 Determinants of the inherent strength of human 5′ splice sites. Rna 11 683 698
30. FreundM
HicksMJ
KonermannC
OtteM
HertelKJ
2005 Extended base pair complementarity between U1 snRNA and the 5′ splice site does not inhibit splicing in higher eukaryotes, but rather increases 5′ splice site recognition. Nucleic Acids Res 33 5112 5119
31. DingW
LinL
RenF
ZouH
DuanZ
2009 Effects of splice sites on the intron retention in histamine H3 receptors from rats and mice. J Genet Genomics 36 475 482
32. JaillonO
BouhoucheK
GoutJ
AuryJ
NoelB
2008 Translational control of intron splicing in eukaryotes. Nature 451 359 362
33. BrognaS
WenJ
2009 Nonsense-mediated mRNA decay (NMD) mechanisms. Nat Struct Mol Biol 16 107 113
34. StalderL
MuhlemannO
2008 The meaning of nonsense. Trends Cell Biol 18 315 321
35. JeffaresD
MourierT
PennyD
2006 The biology of intron gain and loss. Trends in Genetics 22 16 22
36. LinH
ZhuW
SilvaJ
GuX
BuellC
2006 Intron gain and loss in segmentally duplicated genes in rice. Genome Biol 7 R41
37. ChenJQ
WuY
YangH
BergelsonJ
KreitmanM
2009 Variation in the ratio of nucleotide substitution and indel rates across genomes in mammals and bacteria. Mol Biol Evol 26 1523 1531
38. HahnM
HanM
HanS
2007 Gene Family Evolution across 12 Drosophila Genomes. PLoS Genet 3 e197 doi:10.1371/journal.pgen.0030197
39. BirneyE
ClampM
DurbinR
2004 GeneWise and Genomewise. Genome Res 14 988 995
40. CsurosM
HoleyJ
RogozinI
2007 In search of lost introns. Bioinformatics 23 i87 i96
41. RoySW
GilbertW
2005 Rates of intron loss and gain: implications for early eukaryotic evolution. Proc Natl Acad Sci U S A 102 5773 5778
42. StajichJE
DietrichFS
RoySW
2007 Comparative genomic analysis of fungal genomes reveals intron-rich ancestors. Genome Biol 8 R223
43. StephensRM
SchneiderTD
1992 Features of spliceosome evolution and function inferred from an analysis of the information at human splice sites. J Mol Biol 228 1124 1136
44. IrimiaM
RoySW
2008 Evolutionary convergence on highly-conserved 3′ intron structures in intron-poor eukaryotes and insights into the ancestral eukaryotic genome. PLoS Genet 4 e1000148 doi:10.1371/journal.pgen.1000148
45. HillerM
PlatzerM
2008 Widespread and subtle: alternative splicing at short-distance tandem sites. Trends in Genetics 24 246 255
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 1
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- A Major Role of the RecFOR Pathway in DNA Double-Strand-Break Repair through ESDSA in
- Kidney Development in the Absence of and Requires
- The Werner Syndrome Protein Functions Upstream of ATR and ATM in Response to DNA Replication Inhibition and Double-Strand DNA Breaks
- Alternative Epigenetic Chromatin States of Polycomb Target Genes