#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Chimeric Protein Complexes in Hybrid Species Generate Novel Phenotypes


Hybridization between species is an important mechanism for the origin of novel lineages and adaptation to new environments. Increased allelic variation and modification of the transcriptional network are the two recognized forces currently deemed to be responsible for the phenotypic properties seen in hybrids. However, since the majority of the biological functions in a cell are carried out by protein complexes, inter-specific protein assemblies therefore represent another important source of natural variation upon which evolutionary forces can act. Here we studied the composition of six protein complexes in two different Saccharomyces “sensu stricto” hybrids, to understand whether chimeric interactions can be freely formed in the cell in spite of species-specific co-evolutionary forces, and whether the different types of complexes cause a change in hybrid fitness. The protein assemblies were isolated from the hybrids via affinity chromatography and identified via mass spectrometry. We found evidence of spontaneous chimericity for four of the six protein assemblies tested and we showed that different types of complexes can cause a variety of phenotypes in selected environments. In the case of TRP2/TRP3 complex, the effect of such chimeric formation resulted in the fitness advantage of the hybrid in an environment lacking tryptophan, while only one type of parental combination of the MBF complex allowed the hybrid to grow under respiratory conditions. These phenotypes were dependent on both genetic and environmental backgrounds. This study provides empirical evidence that chimeric protein complexes can freely assemble in cells and reveals a new mechanism to generate phenotypic novelty and plasticity in hybrids to complement the genomic innovation resulting from gene duplication. The ability to exchange orthologous members has also important implications for the adaptation and subsequent genome evolution of the hybrids in terms of pattern of gene loss.


Vyšlo v časopise: Chimeric Protein Complexes in Hybrid Species Generate Novel Phenotypes. PLoS Genet 9(10): e32767. doi:10.1371/journal.pgen.1003836
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003836

Souhrn

Hybridization between species is an important mechanism for the origin of novel lineages and adaptation to new environments. Increased allelic variation and modification of the transcriptional network are the two recognized forces currently deemed to be responsible for the phenotypic properties seen in hybrids. However, since the majority of the biological functions in a cell are carried out by protein complexes, inter-specific protein assemblies therefore represent another important source of natural variation upon which evolutionary forces can act. Here we studied the composition of six protein complexes in two different Saccharomyces “sensu stricto” hybrids, to understand whether chimeric interactions can be freely formed in the cell in spite of species-specific co-evolutionary forces, and whether the different types of complexes cause a change in hybrid fitness. The protein assemblies were isolated from the hybrids via affinity chromatography and identified via mass spectrometry. We found evidence of spontaneous chimericity for four of the six protein assemblies tested and we showed that different types of complexes can cause a variety of phenotypes in selected environments. In the case of TRP2/TRP3 complex, the effect of such chimeric formation resulted in the fitness advantage of the hybrid in an environment lacking tryptophan, while only one type of parental combination of the MBF complex allowed the hybrid to grow under respiratory conditions. These phenotypes were dependent on both genetic and environmental backgrounds. This study provides empirical evidence that chimeric protein complexes can freely assemble in cells and reveals a new mechanism to generate phenotypic novelty and plasticity in hybrids to complement the genomic innovation resulting from gene duplication. The ability to exchange orthologous members has also important implications for the adaptation and subsequent genome evolution of the hybrids in terms of pattern of gene loss.


Zdroje

1. MasneufI, HansenJ, GrothC, PiskurJ, DubourdieuD (1998) New hybrids between Saccharomyces sensu stricto yeast species found among wine and cider production strains. Appl Environ Microbiol 64: 3887–3892.

2. GanglH, BatusicM, TscheikG, TiefenbrunnerW, HackC, et al. (2009) Exceptional fermentation characteristics of natural hybrids from Saccharomyces cerevisiae and S. kudriavzevii. Nat Biotechnol 25: 244–251.

3. LitiG, CarterDM, MosesAM, WarringerJ, PartsL, et al. (2009) Population genomics of domestic and wild yeasts. Nature 458: 337–341.

4. GreigD, BortsRH, LouisEJ, TravisanoM (2002) Epistasis and hybrid sterility in Saccharomyces. Proc Biol Sci 269: 1167–1171.

5. 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.

6. BlieckL, ToyeG, DumortierF, VerstrepenKJ, DelvauxFR, et al. (2007) Isolation and characterization of brewer's yeast variants with improved fermentation performance under high-gravity conditions. Appl Environ Microbiol 73: 815–824.

7. GonzálezSS, GalloL, ClimentMA, BarrioE, QuerolA, et al. (2007) Enological characterization of natural hybrids from Saccharomyces cerevisiae and S. kudriavzevii. Int J Food Microbiol 116: 11–17.

8. TiroshI, ReikhavS, LevyAA, BarkaiN (2009) A yeast hybrid provides insight into the evolution of gene expression regulation. Science 324: 659–662.

9. BornemanAR, GianoulisTA, ZhangZD, YuH, RozowskyJ, et al. (2007) Divergence of transcription factor binding sites across related yeast species. Science 317: 815–819.

10. PuS, WongJ, TurnerB, ChoE, WodakSJ (2009) Up-to-date catalogues of yeast protein complexes. Nucleic Acids Res 37: 825–831.

11. GavinAC, BöscheM, KrauseR, GrandiP, MarziochM, et al. (2002) Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141–147.

12. TarassovK, MessierV, LandryCR, RadinovicS, Serna MolinaMM, et al. (2008) An in vivo map of the yeast protein interactome. Science 320: 1465–1470.

13. SteelGJ, BrownswordJ, StirlingCJ (2002) Tail-anchored protein insertion into yeast ER requires a novel posttranslational mechanism which is independent of the SEC machinery. Biochemistry 41: 11914–11920.

14. PrasadR, NiederbergerP, HütterR (1987) Tryptophan accumulation in Saccharomyces cerevisiae under the influence of an artificial yeast TRP gene cluster. Yeast 3: 95–105.

15. ChoEJ, KoborMS, KimM, GreenblattJ, BuratowskiS (2001) Opposing effects of Ctk1 kinase and Fep1 phosphatase at Ser 2 of the RNA polymerase II C- terminal domain. Genes Dev 15: 3319–3329.

16. BeanJM, SiggiaED, CrossFR (2005) High functional overlap between Mlu I cell- cycle box binding factor in the G1/S transcriptional program in Saccharomyces cerevisiae. Genetics 171: 49–61.

17. HeB, ChenP, ChenSY, VancuraKL, MichaelisS, et al. (1991) RAM2, an essential gene of yeast, and RAM1 encode the two polypeptide components of the farnesyltransferase that prenylates a-factor and Ras proteins. Proc Natl Acad Sci U S A 88: 11373–11377.

18. TamATY, PikeBL, HammetA, HeierhorstJ (2007) Telomere-related function of yeast KU in the repair of bleomycin-induced DNA damage. Biochem Biophys Res Commun 357: 800–803.

19. 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.

20. SteinmetzLM, ScharfeC, DeutschbauerAM, MokranjacD, HermanZS, et al. (2002) Systematic screen for human disease genes in yeast. Nat Genet 31: 400–404.

21. LangGI, MurrayAW, BotsteinD (2009) The cost of gene expression underlies a fitness trade-off in yeast. Proc Natl Acad Sci U S A 106: 5755–5760.

22. ChouJY, HungYS, LinKH, LeeHY, LeuJY (2010) Multiple molecular mechanisms cause reproductive isolation between three yeast species. PLoS Biol 8: e1000432.

23. DowellRD, RyanO, JansenA, CheungD, AgarwalaS, et al. (2010) Genotype to phenotype: a complex problem. Science 328: 469.

24. LeducqJB, CharronG, DissG, Gagnon-ArsenaultI, DubéAK, et al. (2012) Evidence for the robustness of protein complexes to inter-species hybridization. PLoS Genetics 8 (12) e1003161.

25. Ohno S. (1970) Evolution by gene duplication. New York Springer-Verlag.

26. PappB, PálC, HurstLD (2003) Dosage sensitivity and the evolution of gene families in yeast. Nature 424: 194–197.

27. IsalanM, LemerleC, MichalodimitrakisK, HornC, BeltraoP, et al. (2008) Evolvability and hierarchy in rewired bacterial gene networks. Nature 452: 840–845.

28. DelneriD, ColsonI, GrammenoudiS, RobertsIN, LouisEJ, et al. (2003) Engineering evolution to study speciation in yeasts. Nature 422: 68–72.

29. RigautG, ShevchenkoA, RutzB, WilmM, MannM, et al. (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17: 1030–1032.

30. ShevchenkoA, TomasH, HavlisJ, OlsenJV, MannM (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856–2860.

31. NesvizhskiiAI, KellerA, KolkerE, AebersoldRA (2003) Statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646–4658.

32. CarterZ, DelneriD (2010) New generation of loxP-mutated deletion cassettes for the genetic manipulation of yeast natural isolates. Yeast 27: 765–775.

33. DelneriD (2011) Competition experiments coupled with high-throughput analyses for functional genomics studies in yeast. Methods Mol Biol 759: 271–282.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#