Alternative splicing is commonly used by the Metazoa to generate more than one protein from a gene. However, such diversification of the proteome by alternative splicing is much rarer in fungi. We describe here an ancient fungal alternative splicing event in which these two proteins are generated from a single alternatively spliced ancestral SKI7/HBS1 gene retained in many species in both the Ascomycota and Basidiomycota. While the ability to express two proteins from a single SKI7/HBS1 gene is conserved in many fungi, the exact mechanism by which they achieve this varies. The alternative splicing was lost in Saccharomyces cerevisiae following the whole-genome duplication event as these two genes subfunctionalized into the present functionally distinct HBS1 and SKI7 genes. When expressed in yeast, the single gene from Lachancea kluyveri generates two functionally distinct proteins. Expression of one of these proteins complements hbs1, but not ski7 mutations, while the other protein complements ski7, but not hbs1. This is the first known case of subfunctionalization by loss of alternative splicing in yeast. By coincidence, the ancestral alternatively spliced gene was also duplicated in Schizosaccharomyces pombe with subsequent subfunctionalization and loss of splicing. Similar subfunctionalization by loss of alternative splicing in fungi also explains the presence of two PTC7 genes in the budding yeast Tetrapisispora blattae, suggesting that this is a common mechanism to preserve duplicate alternatively spliced genes.
Vyšlo v časopise: Alternative Splicing and Subfunctionalization Generates Functional Diversity in Fungal Proteomes. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003376 Kategorie: Research Article prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003376
1. Ohno S (1970) Evolution by gene duplication: Springer-Verlag.
2. HughesAL (1994) The evolution of functionally novel proteins after gene duplication. Proc R Soc Lond B Biol Sci 256 : 119–124.
3. ForceA, LynchM, PickettFB, AmoresA, YanYL, et al. (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151 : 1531–1545.
4. GordonJL, ByrneKP, WolfeKH (2009) Additions, losses, and rearrangements on the evolutionary route from a reconstructed ancestor to the modern Saccharomyces cerevisiae genome. PLoS Genet 5: e1000485 doi:10.1371/journal.pgen.1000485
5. OhEigeartaighSS, ArmisenD, ByrneKP, WolfeKH (2011) Systematic discovery of unannotated genes in 11 yeast species using a database of orthologous genomic segments. BMC genomics 12 : 377.
6. KellisM, BirrenBW, LanderES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428 : 617–624.
7. ByrneKP, WolfeKH (2005) The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome research 15 : 1456–1461.
8. Proux-WeraE, ArmisenD, ByrneKP, WolfeKH (2012) A pipeline for automated annotation of yeast genome sequences by a conserved-synteny approach. BMC bioinformatics 13 : 237.
9. ScannellDR, FrankAC, ConantGC, ByrneKP, WoolfitM, et al. (2007) Independent sorting-out of thousands of duplicated gene pairs in two yeast species descended from a whole-genome duplication. Proceedings of the National Academy of Sciences of the United States of America 104 : 8397–8402.
10. FroydCA, RuscheLN (2011) The duplicated deacetylases Sir2 and Hst1 subfunctionalized by acquiring complementary inactivating mutations. Molecular and cellular biology 31 : 3351–3365.
11. van HoofA (2005) Conserved functions of yeast genes support the duplication, degeneration and complementation model for gene duplication. Genetics 171 : 1455–1461.
12. FinniganGC, Hanson-SmithV, StevensTH, ThorntonJW (2012) Evolution of increased complexity in a molecular machine. Nature 481 : 360–364.
13. van HoofA, FrischmeyerPA, DietzHC, ParkerR (2002) Exosome-mediated recognition and degradation of mRNAs lacking a termination codon. Science 295 : 2262–2264.
14. DomaMK, ParkerR (2006) Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 440 : 561–564.
15. SchaefferD, van HoofA (2011) Different nuclease requirements for exosome-mediated degradation of normal and nonstop mRNAs. Proc Natl Acad Sci U S A 108 : 2366–2371.
16. WangB, GuoG, WangC, LinY, WangX, et al. (2010) Survey of the transcriptome of Aspergillus oryzae via massively parallel mRNA sequencing. Nucleic acids research 38 : 5075–5087.
17. HeF, PeltzSW, DonahueJL, RosbashM, JacobsonA (1993) Stabilization and ribosome association of unspliced pre-mRNAs in a yeast upf1 - mutant. Proc Natl Acad Sci U S A 90 : 7034–7038.
18. GrundSE, FischerT, CabalGG, AntunezO, Perez-OrtinJE, et al. (2008) The inner nuclear membrane protein Src1 associates with subtelomeric genes and alters their regulated gene expression. The Journal of cell biology 182 : 897–910.
19. Rodriguez-NavarroS, IgualJC, Perez-OrtinJE (2002) SRC1: an intron-containing yeast gene involved in sister chromatid segregation. Yeast 19 : 43–54.
20. JuneauK, NislowC, DavisRW (2009) Alternative splicing of PTC7 in Saccharomyces cerevisiae determines protein localization. Genetics 183 : 185–194.
21. StrijbisK, van den BurgJ, VisserWF, van den BergM, DistelB (2012) Alternative splicing directs dual localization of Candida albicans 6-phosphogluconate dehydrogenase to cytosol and peroxisomes. FEMS yeast research 12 : 61–68.
22. KabranP, RossignolT, GaillardinC, NicaudJM, NeuvegliseC (2012) Alternative splicing regulates targeting of malate dehydrogenase in Yarrowia lipolytica. DNA research : an international journal for rapid publication of reports on genes and genomes 19 : 231–244.
23. FreitagJ, AstJ, BolkerM (2012) Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature 485 : 522–525.
24. AltschmiedJ, DelfgaauwJ, WildeB, DuschlJ, BouneauL, et al. (2002) Subfunctionalization of duplicate mitf genes associated with differential degeneration of alternative exons in fish. Genetics 161 : 259–267.
25. CusackBP, WolfeKH (2007) When gene marriages don't work out: divorce by subfunctionalization. Trends in genetics : TIG 23 : 270–272.
26. van HoofA, StaplesRR, BakerRE, ParkerR (2000) Function of the ski4p (Csl4p) and Ski7p proteins in 3′-to-5′ degradation of mRNA. Mol Cell Biol 20 : 8230–8243.
27. Carr-SchmidA, PfundC, CraigEA, KinzyTG (2002) Novel G-protein complex whose requirement is linked to the translational status of the cell. Mol Cell Biol 22 : 2564–2574.
28. BeckerT, ArmacheJP, JaraschA, AngerAM, VillaE, et al. (2011) Structure of the no-go mRNA decay complex Dom34-Hbs1 bound to a stalled 80S ribosome. Nature structural & molecular biology 18 : 715–720.
29. ChenL, MuhlradD, HauryliukV, ChengZ, LimMK, et al. (2010) Structure of the Dom34-Hbs1 complex and implications for no-go decay. Nature structural & molecular biology 17 : 1233–1240.
30. van den ElzenAM, HenriJ, LazarN, GasME, DurandD, et al. (2010) Dissection of Dom34-Hbs1 reveals independent functions in two RNA quality control pathways. Nature structural & molecular biology 17 : 1446–1452.
31. ShoemakerCJ, EylerDE, GreenR (2010) Dom34:Hbs1 promotes subunit dissociation and peptidyl-tRNA drop-off to initiate no-go decay. Science 330 : 369–372.
32. PisarevaVP, SkabkinMA, HellenCU, PestovaTV, PisarevAV (2011) Dissociation by Pelota, Hbs1 and ABCE1 of mammalian vacant 80S ribosomes and stalled elongation complexes. The EMBO journal 30 : 1804–1817.
33. ShoemakerCJ, GreenR (2011) Kinetic analysis reveals the ordered coupling of translation termination and ribosome recycling in yeast. Proceedings of the National Academy of Sciences of the United States of America 108: E1392–1398.
34. ArakiY, TakahashiS, KobayashiT, KajihoH, HoshinoS, et al. (2001) Ski7p G protein interacts with the exosome and the Ski complex for 3′ - to-5′ mRNA decay in yeast. EMBO J 20 : 4684–4693.
35. AtkinsonGC, BaldaufSL, HauryliukV (2008) Evolution of nonstop, no-go and nonsense-mediated mRNA decay and their termination factor-derived components. BMC evolutionary biology 8 : 290.
36. FinkGR (1987) Pseudogenes in yeast? Cell 49 : 5–6.
37. HughesAL, FriedmanR (2003) Parallel evolution by gene duplication in the genomes of two unicellular fungi. Genome research 13 : 794–799.
38. FonziWA, IrwinMY (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134 : 717–728.
39. NishidaH, HamamotoM, SugiyamaJ (2011) Draft genome sequencing of the enigmatic yeast Saitoella complicata. The Journal of general and applied microbiology 57 : 243–246.
40. RamirezMA, LorenzMC (2009) The transcription factor homolog CTF1 regulates {beta}-oxidation in Candida albicans. Eukaryotic cell 8 : 1604–1614.
41. GietzRD, WoodsRA (2002) Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350 : 87–96.
42. LiuY, LeighJW, BrinkmannH, CushionMT, Rodriguez-EzpeletaN, et al. (2009) Phylogenomic analyses support the monophyly of Taphrinomycotina, including Schizosaccharomyces fission yeasts. Molecular biology and evolution 26 : 27–34.
43. ButlerG, RasmussenMD, LinMF, SantosMA, SakthikumarS, et al. (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459 : 657–662.
44. RhindN, ChenZ, YassourM, ThompsonDA, HaasBJ, et al. (2011) Comparative functional genomics of the fission yeasts. Science 332 : 930–936.
Zvýšte si kvalifikáciu online z pohodlia domova
Nemáte účet? Registrujte sa
Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
