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Evidence for the Robustness of Protein Complexes to Inter-Species Hybridization
Despite the tremendous efforts devoted to the identification of genetic incompatibilities underlying hybrid sterility and inviability, little is known about the effect of inter-species hybridization at the protein interactome level. Here, we develop a screening platform for the comparison of protein–protein interactions (PPIs) among closely related species and their hybrids. We examine in vivo the architecture of protein complexes in two yeast species (Saccharomyces cerevisiae and Saccharomyces kudriavzevii) that diverged 5–20 million years ago and in their F1 hybrids. We focus on 24 proteins of two large complexes: the RNA polymerase II and the nuclear pore complex (NPC), which show contrasting patterns of molecular evolution. We found that, with the exception of one PPI in the NPC sub-complex, PPIs were highly conserved between species, regardless of protein divergence. Unexpectedly, we found that the architecture of the complexes in F1 hybrids could not be distinguished from that of the parental species. Our results suggest that the conservation of PPIs in hybrids likely results from the slow evolution taking place on the very few protein residues involved in the interaction or that protein complexes are inherently robust and may accommodate protein divergence up to the level that is observed among closely related species.
Vyšlo v časopise: Evidence for the Robustness of Protein Complexes to Inter-Species Hybridization. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003161
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003161Souhrn
Despite the tremendous efforts devoted to the identification of genetic incompatibilities underlying hybrid sterility and inviability, little is known about the effect of inter-species hybridization at the protein interactome level. Here, we develop a screening platform for the comparison of protein–protein interactions (PPIs) among closely related species and their hybrids. We examine in vivo the architecture of protein complexes in two yeast species (Saccharomyces cerevisiae and Saccharomyces kudriavzevii) that diverged 5–20 million years ago and in their F1 hybrids. We focus on 24 proteins of two large complexes: the RNA polymerase II and the nuclear pore complex (NPC), which show contrasting patterns of molecular evolution. We found that, with the exception of one PPI in the NPC sub-complex, PPIs were highly conserved between species, regardless of protein divergence. Unexpectedly, we found that the architecture of the complexes in F1 hybrids could not be distinguished from that of the parental species. Our results suggest that the conservation of PPIs in hybrids likely results from the slow evolution taking place on the very few protein residues involved in the interaction or that protein complexes are inherently robust and may accommodate protein divergence up to the level that is observed among closely related species.
Zdroje
1. Darwin C (1859) On the origin of species by means of natural selection. London: J. Murray. ix: , 1, 502 p.
2. MullerHJ, PontecorvoG (1940) Recombinants between Drosophila species the F-1 hybrids of which are sterile. Nature 146 : 199–200.
3. Bateson (1909) Discussion on the Influence of Heredity on Disease, with special Reference to Tuberculosis, Cancer, and Diseases of the Nervous System: Introductory Address. Proc R Soc Med 2 : 22–30.
4. DobzhanskyT (1940) Speciation as a stage in evolutionary divergence. American Naturalist 74 : 312–321.
5. GourbiereS, MalletJ (2010) Are species real? The shape of the species boundary with exponential failure, reinforcement, and the “missing snowball”. Evolution 64 : 1–24.
6. OrrHA, TurelliM (2001) The evolution of postzygotic isolation: Accumulating Dobzhansky-Muller incompatibilities. Evolution 55 : 1085–1094.
7. AraripeLO, MontenegroH, LemosB, HartlDL (2010) Fine-scale genetic mapping of a hybrid sterility factor between Drosophila simulans and D. mauritiana: the varied and elusive functions of “speciation genes”. BMC Evol Biol 10 : 385.
8. BarbashDA (2007) Nup96-dependent hybrid lethality occurs in a subset of species from the simulans clade of Drosophila. Genetics 176 : 543–552.
9. BrideauNJ, FloresHA, WangJ, MaheshwariS, WangX, et al. (2006) Two Dobzhansky-Muller genes interact to cause hybrid lethality in Drosophila. Science 314 : 1292–1295.
10. LeeHY, ChouJY, CheongL, ChangNH, YangSY, et al. (2008) Incompatibility of nuclear and mitochondrial genomes causes hybrid sterility between two yeast species. Cell 135 : 1065–1073.
11. Arabidopsis-Interactome-Mapping-Consortium (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333 : 601–607.
12. GuruharshaKG, RualJF, ZhaiB, MintserisJ, VaidyaP, et al. (2011) A protein complex network of Drosophila melanogaster. Cell 147 : 690–703.
13. TarassovK, MessierV, LandryCR, RadinovicS, Serna MolinaMM, et al. (2008) An in vivo map of the yeast protein interactome. Science 320 : 1465–1470.
14. ChoudharyC, KumarC, GnadF, NielsenML, RehmanM, et al. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325 : 834–840.
15. CollinsSR, MillerKM, MaasNL, RoguevA, FillinghamJ, et al. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446 : 806–810.
16. GuoW, SacherM, BarrowmanJ, Ferro-NovickS, NovickP (2000) Protein complexes in transport vesicle targeting. Trends Cell Biol 10 : 251–255.
17. LemmonMA, SchlessingerJ (2010) Cell signaling by receptor tyrosine kinases. Cell 141 : 1117–1134.
18. LovellSC, RobertsonDL (2010) An integrated view of molecular coevolution in protein-protein interactions. Mol Biol Evol 27 : 2567–2575.
19. PazosF, ValenciaA (2008) Protein co-evolution, co-adaptation and interactions. Embo J 27 : 2648–2655.
20. RamaniAK, MarcotteEM (2003) Exploiting the co-evolution of interacting proteins to discover interaction specificity. J Mol Biol 327 : 273–284.
21. HarrisonJS, BurtonRS (2006) Tracing hybrid incompatibilities to single amino acid substitutions. Mol Biol Evol 23 : 559–564.
22. DujonB (2006) Yeasts illustrate the molecular mechanisms of eukaryotic genome evolution. Trends Genet 22 : 375–387.
23. ScannellDR, ZillOA, RokasA, PayenC, DunhamMJ, et al. (2011) The Awesome Power of Yeast Evolutionary Genetics: New Genome Sequences and Strain Resources for the Saccharomyces sensu stricto Genus. Genes Genomes Genetics 1 : 11–25.
24. StarkC, BreitkreutzBJ, Chatr-AryamontriA, BoucherL, OughtredR, et al. (2011) The BioGRID Interaction Database: 2011 update. Nucleic Acids Res 39: D698–704.
25. GonzalezSS, GalloL, ClimentMA, BarrioE, QuerolA (2007) Enological characterization of natural hybrids from Saccharomyces cerevisiae and S. kudriavzevii. Int J Food Microbiol 116 : 11–18.
26. SniegowskiPD, DombrowskiPG, FingermanE (2002) Saccharomyces cerevisiae and Saccharomyces paradoxus coexist in a natural woodland site in North America and display different levels of reproductive isolation from European conspecifics. FEMS Yeast Res 1 : 299–306.
27. GreigD, BortsRH, LouisEJ, TravisanoM (2002) Epistasis and hybrid sterility in Saccharomyces. P R Soc B 269 : 1167–1171.
28. XuM, HeX (2011) Genetic incompatibility dampens hybrid fertility more than hybrid viability: yeast as a case study. PLoS ONE 6: e18341 doi:10.1371/journal.pone.0018341.
29. MichnickSW, EarPH, LandryC, MalleshaiahMK, MessierV (2010) A toolkit of protein-fragment complementation assays for studying and dissecting large-scale and dynamic protein-protein interactions in living cells. Methods in Enzymology 470 : 335–368.
30. FreschiL, Torres-QuirozF, DubéAK, LandryCR (2012) qPCA: a scalable assay to measure the perturbation of protein-protein interactions in living cells. Molecular BioSystems DOI: 10.1039/C2MB25265A.
31. NeumannN, LundinD, PooleAM (2010) Comparative genomic evidence for a complete nuclear pore complex in the last eukaryotic common ancestor. PLoS ONE 5: e13241 doi:10.1371/journal.pone.0013241.
32. BaptesteE, CharleboisRL, MacLeodD, BrochierC (2005) The two tempos of nuclear pore complex evolution: highly adapting proteins in an ancient frozen structure. Genome Biol 6: R85.
33. WoychikNA (1998) Fractions to functions: RNA polymerase II thirty years later. Cold Spring Harb Symp Quant Biol 63 : 311–317.
34. AlberF, DokudovskayaS, VeenhoffLM, ZhangW, KipperJ, et al. (2007) The molecular architecture of the nuclear pore complex. Nature 450 : 695–701.
35. CramerP, BushnellDA, FuJ, GnattAL, Maier-DavisB, et al. (2000) Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288 : 640–649.
36. FraserHB, HirshAE, SteinmetzLM, ScharfeC, FeldmanMW (2002) Evolutionary rate in the protein interaction network. Science 296 : 750–752.
37. WinzelerEA, ShoemakerDD, AstromoffA, LiangH, AndersonK, et al. (1999) Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285 : 901–906.
38. KellisM, BirrenBW, LanderES (2004) Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428 : 617–624.
39. EarPH, MichnickSW (2009) A general life-death selection strategy for dissecting protein functions. Nat Methods 6 : 813–816.
40. HittingerCT, GoncalvesP, SampaioJP, DoverJ, JohnstonM, et al. (2010) Remarkably ancient balanced polymorphisms in a multi-locus gene network. Nature 464 : 54–58.
41. HoelzA, DeblerEW, BlobelG (2011) The structure of the nuclear pore complex. Annu Rev Biochem 80 : 613–643.
42. ZamirL, ZaretskyM, FridmanY, Ner-GaonH, RubinE, et al. (2012) Tight coevolution of proliferating cell nuclear antigen (PCNA)-partner interaction networks in fungi leads to interspecies network incompatibility. Proc Natl Acad Sci U S A 109: E406–414.
43. Fernandez-MartinezJ, PhillipsJ, SekedatMD, Diaz-AvalosR, Velazquez-MurielJ, et al. (2012) Structure-function mapping of a heptameric module in the nuclear pore complex. J Cell Biol 196 : 419–434.
44. EmtageJL, BucciM, WatkinsJL, WenteSR (1997) Defining the essential functional regions of the nucleoporin Nup145p. J Cell Sci 110 (Pt 7) 911–925.
45. TeixeiraMT, FabreE, DujonB (1999) Self-catalyzed cleavage of the yeast nucleoporin Nup145p precursor. J Biol Chem 274 : 32439–32444.
46. FicarroSB, McClelandML, StukenbergPT, BurkeDJ, RossMM, et al. (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nat Biotechnol 20 : 301–305.
47. SmolkaMB, AlbuquerqueCP, ChenSH, ZhouH (2007) Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc Natl Acad Sci U S A 104 : 10364–10369.
48. MalmstromL, RiffleM, StraussCE, ChivianD, DavisTN, et al. (2007) Superfamily assignments for the yeast proteome through integration of structure prediction with the gene ontology. PLoS Biol 5: e76 doi:10.1371/journal.pbio.0050076.
49. RoutMP, AitchisonJD, SupraptoA, HjertaasK, ZhaoY, et al. (2000) The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 148 : 635–651.
50. LevyED (2010) A simple definition of structural regions in proteins and its use in analyzing interface evolution. J Mol Biol 403 : 660–670.
51. MelcakI, HoelzA, BlobelG (2007) Structure of Nup58/45 suggests flexible nuclear pore diameter by intermolecular sliding. Science 315 : 1729–1732.
52. BoehmerT, JeudyS, BerkeIC, SchwartzTU (2008) Structural and functional studies of Nup107/Nup133 interaction and its implications for the architecture of the nuclear pore complex. Mol Cell 30 : 721–731.
53. YoshidaK, SeoHS, DeblerEW, BlobelG, HoelzA (2011) Structural and functional analysis of an essential nucleoporin heterotrimer on the cytoplasmic face of the nuclear pore complex. Proc Natl Acad Sci U S A 108 : 16571–16576.
54. QianW, HeX, ChanE, XuH, ZhangJ (2011) Measuring the evolutionary rate of protein-protein interaction. Proc Natl Acad Sci U S A 108 : 8725–8730.
55. PresgravesDC, BalagopalanL, AbmayrSM, OrrHA (2003) Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. Nature 423 : 715–719.
56. PresgravesDC, StephanW (2007) Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96. Mol Biol Evol 24 : 306–314.
57. GreigD (2007) A screen for recessive speciation genes expressed in the gametes of F1 hybrid yeast. PLoS Genet 3: e21 doi:10.1371/journal.pgen.0030021.
58. KaoKC, SchwartzK, SherlockG (2010) A genome-wide analysis reveals no nuclear dobzhansky-muller pairs of determinants of speciation between S. cerevisiae and S. paradoxus, but suggests more complex incompatibilities. PLoS Genet 6: e1001038 doi:10.1371/journal.pgen.1001038.
59. HeckJA, ArguesoJL, GemiciZ, ReevesRG, BernardA, et al. (2006) Negative epistasis between natural variants of the Saccharomyces cerevisiae MLH1 and PMS1 genes results in a defect in mismatch repair. Proc Natl Acad Sci U S A 103 : 3256–3261.
60. LitiG, HaricharanS, CubillosFA, TierneyAL, SharpS, et al. (2009) Segregating YKU80 and TLC1 alleles underlying natural variation in telomere properties in wild yeast. PLoS Genet 5: e1000659 doi:10.1371/journal.pgen.1000659.
61. Arroyo-LopezFN, OrlicS, QuerolA, BarrioE (2009) Effects of temperature, pH and sugar concentration on the growth parameters of Saccharomyces cerevisiae, S. kudriavzevii and their interspecific hybrid. Int J Food Microbiol 131 : 120–127.
62. HittingerCT, RokasA, CarrollSB (2004) Parallel inactivation of multiple GAL pathway genes and ecological diversification in yeasts. Proc Natl Acad Sci U S A 101 : 14144–14149.
63. WardJJ, SodhiJS, McGuffinLJ, BuxtonBF, JonesDT (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337 : 635–645.
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