#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Correlated Evolution of Nearby Residues in Drosophilid Proteins


Here we investigate the correlations between coding sequence substitutions as a function of their separation along the protein sequence. We consider both substitutions between the reference genomes of several Drosophilids as well as polymorphisms in a population sample of Zimbabwean Drosophila melanogaster. We find that amino acid substitutions are “clustered” along the protein sequence, that is, the frequency of additional substitutions is strongly enhanced within ≈10 residues of a first such substitution. No such clustering is observed for synonymous substitutions, supporting a “correlation length” associated with selection on proteins as the causative mechanism. Clustering is stronger between substitutions that arose in the same lineage than it is between substitutions that arose in different lineages. We consider several possible origins of clustering, concluding that epistasis (interactions between amino acids within a protein that affect function) and positional heterogeneity in the strength of purifying selection are primarily responsible. The role of epistasis is directly supported by the tendency of nearby substitutions that arose on the same lineage to preserve the total charge of the residues within the correlation length and by the preferential cosegregation of neighboring derived alleles in our population sample. We interpret the observed length scale of clustering as a statistical reflection of the functional locality (or modularity) of proteins: amino acids that are near each other on the protein backbone are more likely to contribute to, and collaborate toward, a common subfunction.


Vyšlo v časopise: Correlated Evolution of Nearby Residues in Drosophilid Proteins. PLoS Genet 7(2): e32767. doi:10.1371/journal.pgen.1001315
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001315

Souhrn

Here we investigate the correlations between coding sequence substitutions as a function of their separation along the protein sequence. We consider both substitutions between the reference genomes of several Drosophilids as well as polymorphisms in a population sample of Zimbabwean Drosophila melanogaster. We find that amino acid substitutions are “clustered” along the protein sequence, that is, the frequency of additional substitutions is strongly enhanced within ≈10 residues of a first such substitution. No such clustering is observed for synonymous substitutions, supporting a “correlation length” associated with selection on proteins as the causative mechanism. Clustering is stronger between substitutions that arose in the same lineage than it is between substitutions that arose in different lineages. We consider several possible origins of clustering, concluding that epistasis (interactions between amino acids within a protein that affect function) and positional heterogeneity in the strength of purifying selection are primarily responsible. The role of epistasis is directly supported by the tendency of nearby substitutions that arose on the same lineage to preserve the total charge of the residues within the correlation length and by the preferential cosegregation of neighboring derived alleles in our population sample. We interpret the observed length scale of clustering as a statistical reflection of the functional locality (or modularity) of proteins: amino acids that are near each other on the protein backbone are more likely to contribute to, and collaborate toward, a common subfunction.


Zdroje

1. KimuraM

1983 The neutral theory of molecular evolution. Cambridge Cambridge University Press

2. GillespieJH

1991 The Causes of Molecular Evolution. Oxford Oxford University Press

3. HeyJ

1999 The neutralist, the y and the selectionist. Trends in Ecology & Evolution 14 35 38

4. NeiM

2005 Selectionism and neutralism in molecular evolution. Molecular Biology and Evolution 22 2318 2342

5. SellaG

PetrovDA

PrzeworskiM

AndolfattoP

2009 Pervasive natural selection in the drosophila genome? PLoS Genet 5 e1000495 doi:10.1371/journal.pgen.1000495

6. SmithNGC

Eyre-WalkerA

2002 Adaptive protein evolution in drosophila. Nature 415 1022 4

7. FayJC

WyckoffGJ

WuCI

2002 Testing the neutral theory of molecular evolution with genomic data from drosophila. Nature 415 1024 1026

8. McDonaldJH

KreitmanM

1991 Adaptive protein evolution at the adh locus in drosophila. Nature 351 652 4

9. Eyre-WalkerA

2006 The genomic rate of adaptive evolution. Trends in Ecology & Evolution 21 569 575

10. OhtaT

1992 The nearly neutral theory of molecular evolution. Annual Review of Ecology and Systematics 23 263 286

11. HughesAL

2007 Looking for darwin in all the wrong places: the misguided quest for positive selection at the nucleotide sequence level. Heredity 99 364 373

12. BrandenC

ToozeJ

1999 Introduction to protein structure. New York Garland Science

13. ChothiaC

LeskAM

1986 The relation between the divergence of sequence and structure in proteins. EMBO Journal 5 823 26

14. Olivier LichtargeHRB

CohenFE

1996 An evolutionary trace method defines binding surfaces common to protein families. J Mol Biol 342 358

15. FitchW

MarkowitzE

1970 An improved method for determining codon variability in a gene and its application to the rate of fixation of mutations in evolution. Biochem Genet 4 579 593

16. ZvelebilM

BartonG

TaylorW

SternbergM

1987 Prediction of protein secondary structure and active sites using the alignment of homologous sequences. J Mol Biol 195 957 961

17. RidoutK

DixonC

FilatovD

2010 Positive selection differs between protein secondary structure elements in drosophila. Genome Biology and Evolution 2010 166 179

18. KirbyDA

MuseSV

StephanW

1995 Maintenance of pre-mrna secondary structure by epistatic selection. PNAS 92 9047 9051

19. StephanW

1996 The rate of compensatory evolution. Genetics 144 419 26

20. MeerMV

KondrashovAS

Artzy-RandrupY

KondrashovFA

2010 Compensatory evolution in mitochondrial trnas navigates valleys of low fitness. Nature 464 279 282

21. WhisstockJC

LeskAM

2004 Prediction of protein function from protein sequence and structure. Quarterly Reviews of Biophysics 36 307 340

22. NeherE

1994 How frequent are correlated changes in families of protein sequences? PNAS 91 98 102

23. LocklessSW

RanganathanR

1999 Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286 295 9

24. YeangCH

HausslerD

2007 Detecting coevolution in and among protein domains. PLoS Comput Biol 3 e211 doi:10.1371/journal.pcbi.0030211

25. BurgerL

van NimwegenE

2010 Disentangling direct from indirect co-evolution of residues in protein alignments. PLoS Comput Biol 6 e1000633 doi:10.1371/journal.pcbi.1000633

26. WangQ

LeeC

2007 Distinguishing functional amino acid covariation from background linkage disequilibrium in HIV protease and reverse transcriptase. PLoS ONE 2 e814 doi:10.1371/journal.pone.0000814

27. PoonAFY

SwensonLC

DongWWY

DengW

PondSLK

2010 Phylogenetic analysis of population-based and deep sequencing data to identify coevolving sites in the nef gene of hiv-1. MBE 27 819 832

28. SocolichM

LocklessSW

RussWP

LeeH

GardnerKH

2005 Evolutionary information for specifying a protein fold. Nature 437 512 8

29. ConsortiumDG

2007 Evolution of genes and genomes on the drosophila phylogeny. Nature 450 203 18

30. SchwartzS

KentWJ

SmitA

ZhangZ

BaertschR

2003 Human-mouse alignments with blastz. Genome Res 13 103 7

31. KarolchikD

BaertschR

DiekhansM

FureyTS

HinrichsA

2003 The ucsc genome browser database. Nucleic Acids Res 31 51 4

32. ColginLM

HackmannAFM

EmondMJ

MonnatRJ

2002 The unexpected landscape of in vivo somatic mutation in a human epithelial cell lineage. PNAS 99 1437 42

33. WangJ

GonzalezKD

ScaringeWA

TsaiK

LiuN

2007 Evidence for mutation showers. PNAS 104 8403 8

34. Fukami-KobayashiK

SchreiberD

BennerS

2002 Detecting compensatory covariation signals in protein evolution using reconstructed ancestral sequences. Journal of Molecular Biology 319 729 743

35. SlatkinM

2008 Linkage disequilibrium - understanding the evolutionary past and mapping the medical future. Nat Rev Genet 9 477 485

36. TakahasiKR

InnanH

2008 The direction of linkage disequilibrium: A new measure based on the ancestral-derived status of segregating alleles. Genetics 179 1705 1712

37. DavisBH

PoonAFY

WhitlockMC

2009 Compensatory mutations are repeatable and clustered within proteins. Proc Biol Sci 276 1823 7

38. BazykinGA

KondrashovFA

OgurtsovAY

SunyaevS

KondrashovAS

2004 Positive selection at sites of multiple amino acid replacements since rat-mouse divergence. Nature 429 558 62

39. BazykinGA

DushoffJ

LevinSA

KondrashovAS

2006 Bursts of nonsynonymous substitutions in HIV-1 evolution reveal instances of positive selection at conservative protein sites. PNAS 103 19396 401

40. OrrHA

2003 A minimum on the mean number of steps taken in adaptive walks. Journal of Theoretical Biology 220 241 247

41. KulathinalR

BettencourtB

HartlD

2004 Compensated deleterious mutations in insect genomes. Science 306 1553 4

42. WeinreichDM

DelaneyNF

DepristoMA

HartlDL

2006 Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312 111 4

43. SmithJM

HaighJ

1974 The hitch-hiking effect of a favourable gene. Genetical Research 23 23 35

44. RiceWR

1987 Genetic hitchhiking and the evolution of reduced genetic activity of the y sex chromosome. Genetics 116 161 167

45. BirkyCW

WalshJB

1988 Effects of linkage on rates of molecular evolution. PNAS 85 6414 6418

46. BartonNH

1995 Linkage and the limits to natural selection. Genetics 140 821 841

47. AndolfattoP

2005 Adaptive evolution of non-coding DNA in drosophila. Nature 437 1149 52

48. BegunDJ

HollowayAK

StevensK

HillierLW

PohYP

2007 Population genomics: Whole-genome analysis of polymorphism and divergence in drosophila simulans. PLoS Biol 5 e310 doi:10.1371/journal.pbio.0050310

49. ShapiroJA

HuangW

ZhangC

HubiszMJ

LuJ

2007 Adaptive genic evolution in the drosophila genomes. PNAS 104 2271 2276

50. HillWG

RoberstonA

1966 The effect of linkage on limits to artificial selection. Genetical Research 8 269 294

51. OrtlundEA

BridghamJT

RedinboMR

ThorntonJW

2007 Crystal structure of an ancient protein: evolution by conformational epistasis. Science 317 1544 8

52. YangZ

2007 Paml 4: Phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24 1586 1591

53. TanayA

SiggiaED

2008 Sequence context affects the rate of short insertions and deletions in ies and primates. Genome Biol 9 R37

54. AndolfattoP

2007 Hitchhiking effects of recurrent beneficial amino acid substitutions in the drosophila melanogaster genome. Genome Research 17 1755 1762

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 2
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

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#