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Long- and Short-Term Selective Forces on Malaria Parasite Genomes


Plasmodium parasites, the causal agents of malaria, result in more than 1 million deaths annually. Plasmodium are unicellular eukaryotes with small ∼23 Mb genomes encoding ∼5200 protein-coding genes. The protein-coding genes comprise about half of these genomes. Although evolutionary processes have a significant impact on malaria control, the selective pressures within Plasmodium genomes are poorly understood, particularly in the non-protein-coding portion of the genome. We use evolutionary methods to describe selective processes in both the coding and non-coding regions of these genomes. Based on genome alignments of seven Plasmodium species, we show that protein-coding, intergenic and intronic regions are all subject to purifying selection and we identify 670 conserved non-genic elements. We then use genome-wide polymorphism data from P. falciparum to describe short-term selective processes in this species and identify some candidate genes for balancing (diversifying) selection. Our analyses suggest that there are many functional elements in the non-genic regions of these genomes and that adaptive evolution has occurred more frequently in the protein-coding regions of the genome.


Vyšlo v časopise: Long- and Short-Term Selective Forces on Malaria Parasite Genomes. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001099
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001099

Souhrn

Plasmodium parasites, the causal agents of malaria, result in more than 1 million deaths annually. Plasmodium are unicellular eukaryotes with small ∼23 Mb genomes encoding ∼5200 protein-coding genes. The protein-coding genes comprise about half of these genomes. Although evolutionary processes have a significant impact on malaria control, the selective pressures within Plasmodium genomes are poorly understood, particularly in the non-protein-coding portion of the genome. We use evolutionary methods to describe selective processes in both the coding and non-coding regions of these genomes. Based on genome alignments of seven Plasmodium species, we show that protein-coding, intergenic and intronic regions are all subject to purifying selection and we identify 670 conserved non-genic elements. We then use genome-wide polymorphism data from P. falciparum to describe short-term selective processes in this species and identify some candidate genes for balancing (diversifying) selection. Our analyses suggest that there are many functional elements in the non-genic regions of these genomes and that adaptive evolution has occurred more frequently in the protein-coding regions of the genome.


Zdroje

1. AregawiM

CibulskisR

OttenM

WilliamsR

DyeC

2008 World malaria report 2008 World Health Organization

2. WoottonJC

FengX

FerdigMT

CooperRA

MuJ

2002 Genetic diversity and chloroquine selective sweeps in Plasmodium falciparum. Nature 418 320 323

3. NairS

WilliamsJT

BrockmanA

PaiphunL

MayxayM

2003 A selective sweep driven by pyrimethamine treatment in southeast asian malaria parasites. Mol Biol Evol 20 1526 1536

4. RoperC

PearceR

NairS

SharpB

NostenF

2004 Intercontinental spread of pyrimethamine-resistant malaria. Science 305 1124

5. AndersonTJ

RoperC

2005 The origins and spread of antimalarial drug resistance: lessons for policy makers. Acta Trop 94 269 280

6. DzikowskiR

TempletonTJ

DeitschK

2006 Variant antigen gene expression in malaria. Cell Microbiol 8 1371 1381

7. PierceSK

MillerLH

2009 World Malaria Day 2009: what malaria knows about the immune system that immunologists still do not. J Immunol 182 5171 5177

8. NeafseyDE

HartlDL

BerrimanM

2005 Evolution of noncoding and silent coding sites in the Plasmodium falciparum and Plasmodium reichenowi genomes. Mol Biol Evol 22 1621 1626

9. JeffaresDC

PainA

BerryA

CoxAV

StalkerJ

2007 Genome variation and evolution of the malaria parasite Plasmodium falciparum. Nat Genet 39 120 125

10. HalliganDL

Eyre-WalkerA

AndolfattoP

2004 Patterns of evolutionary constraints in intronic and intergenic DNA of Drosophila. Genome Research

11. HalliganDL

KeightleyPD

2006 Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison. Genome Res 16 875 884

12. GaffneyDJ

KeightleyPD

2006 Genomic selective constraints in murid noncoding DNA. PLoS Genet 2 e204

13. HasegawaM

KishinoH

YanoT

1985 Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22 160 174

14. ScherfA

Lopez-RubioJJ

RiviereL

2008 Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62 445 470

15. PetterM

BonowI

KlinkertMQ

2008 Diverse expression patterns of subgroups of the rif multigene family during Plasmodium falciparum gametocytogenesis. PLoS ONE 3 e3779

16. BlytheJE

YamXY

KussC

BozdechZ

HolderAA

2008 Plasmodium falciparum STEVOR proteins are highly expressed in patient isolates and located in the surface membranes of infected red blood cells and the apical tips of merozoites. Infect Immun 76 3329 3336

17. CooperGM

StoneEA

AsimenosG

GreenED

BatzoglouS

2005 Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 15 901 913

18. OttoTD

WilinskiD

AssefaS

KeaneTM

SarryLR

2010 New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol 76 12 24

19. MourierT

CarretC

KyesS

ChristodoulouZ

GardnerPP

2008 Genome-wide discovery and verification of novel structured RNAs in Plasmodium falciparum. Genome Res 18 281 292

20. RaabeCA

SanchezCP

RandauG

RobeckT

SkryabinBV

2009 A global view of the nonprotein-coding transcriptome in Plasmodium falciparum. Nucleic Acids Res

21. WashietlS

HofackerIL

StadlerPF

2005 Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci U S A 102 2454 2459

22. GesellT

WashietlS

2008 Dinucleotide controlled null models for comparative RNA gene prediction. BMC Bioinformatics 9 248

23. NielsenR

2005 Molecular signatures of natural selection. Annual Review of Genetics 39 197 218

24. CharlesworthD

2006 Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2 e64

25. VerraF

HughesAL

1999 Natural selection on apical membrane antigen-1 of Plasmodium falciparum. Parassitologia 41 93 95

26. VolkmanSK

HartlDL

WirthDF

NielsenKM

ChoiM

2002 Excess polymorphisms in genes for membrane proteins in Plasmodium falciparum. Science 298 216 218

27. KarP

DashAP

SupakarPC

2007 Polymorphism study of rhoptry associated membrane antigen (RAMA) gene of Plasmodium falciparum–a putative vaccine candidate. Mol Biochem Parasitol 155 156 160

28. PolleySD

TettehKK

LloydJM

AkpoghenetaOJ

GreenwoodBM

2007 Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis 195 279 287

29. MuJ

AwadallaP

DuanJ

McGeeKM

KeeblerJ

2007 Genome-wide variation and identification of vaccine targets in the Plasmodium falciparum genome. Nat Genet 39 126 130

30. AyalaFJ

AnaniasA

L.AA

RichSM

1998 Evolutionary relationships of human malaria parasites.

ShermanIW

Malaria: Biology, pathogenesis and protection Washington (D.C.) ASM Press

31. McDonaldJH

KreitmanM

1991 Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 652 654

32. SmithNG

Eyre-WalkerA

2002 Adaptive protein evolution in Drosophila. Nature 415 1022 1024

33. AndolfattoP

2005 Adaptive evolution of non-coding DNA in Drosophila. Nature 437 1149 1152

34. ConwayDJ

1997 Natural selection on polymorphic malaria antigens and the search for a vaccine. Parasitol Today 13 26 29

35. TajimaF

1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123 585 595

36. PolleySD

ConwayDJ

2001 Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158 1505 1512

37. TheraMA

DoumboOK

CoulibalyD

DialloDA

KoneAK

2008 Safety and immunogenicity of an AMA-1 malaria vaccine in Malian adults: results of a phase 1 randomized controlled trial. PLoS ONE 3 e1465

38. KennedyMC

WangJ

ZhangY

MilesAP

ChitsazF

2002 In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect Immun 70 6948 6960

39. PinzonCG

CurtidorH

ReyesC

MendezD

PatarroyoME

2008 Identification of Plasmodium falciparum RhopH3 protein peptides that specifically bind to erythrocytes and inhibit merozoite invasion. Protein Sci 17 1719 1730

40. BirneyE

StamatoyannopoulosJA

DuttaA

GuigoR

GingerasTR

2007 Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447 799 816

41. WaterstonRH

Lindblad-TohK

BirneyE

RogersJ

AbrilJF

2002 Initial sequencing and comparative analysis of the mouse genome. Nature 420 520 562

42. ShabalinaSA

OgurtsovAY

KondrashovVA

2001 Selective constraint in intergenic regions of human and mouse genomes. Trends in Genetics

43. ShabalinaSA

KondrashovAS

1999 Pattern of selective constraint in C. elegans and C. briggsae genomes. Genet Res 74 23 30

44. BensassonD

ZarowieckiM

BurtA

KoufopanouV

2008 Rapid evolution of yeast centromeres in the absence of drive. Genetics 178 2161 2167

45. GunasekeraAM

MyrickA

MilitelloKT

SimsJS

DongCK

2007 Regulatory motifs uncovered among gene expression clusters in Plasmodium falciparum. Mol Biochem Parasitol 153 19 30

46. JurgelenaiteR

DijkstraTM

KockenCH

HeskesT

2009 Gene regulation in the intraerythrocytic cycle of Plasmodium falciparum. Bioinformatics 25 1484 1491

47. ImamuraH

PersampieriJH

ChuangJH

2007 Sequences conserved by selection across mouse and human malaria species. BMC Genomics 8 372

48. WuJ

SieglaffDH

GervinJ

XieXS

2008 Discovering regulatory motifs in the Plasmodium genome using comparative genomics. Bioinformatics 24 1843 1849

49. YoungJA

JohnsonJR

BennerC

YanSF

ChenK

2008 In silico discovery of transcription regulatory elements in Plasmodium falciparum. BMC Genomics 9 70

50. ElementoO

SlonimN

TavazoieS

2007 A universal framework for regulatory element discovery across all genomes and data types. Mol Cell 28 337 350

51. IengarP

JoshiNV

2009 Identification of putative regulatory motifs in the upstream regions of co-expressed functional groups of genes in Plasmodium falciparum. BMC Genomics 10 18

52. De SilvaEK

GehrkeAR

OlszewskiK

LeonI

ChahalJS

2008 Specific DNA-binding by apicomplexan AP2 transcription factors. Proc Natl Acad Sci U S A 105 8393 8398

53. NeafseyDE

SchaffnerSF

VolkmanSK

ParkD

MontgomeryP

2008 Genome-wide SNP genotyping highlights the role of natural selection in Plasmodium falciparum population divergence. Genome Biol 9 R171

54. International Hapmap Consortium 2007 A second generation human haplotype map of over 3.1 million SNPs. Nature 449 851 861

55. BierneN

Eyre-WalkerA

2006 Variation in synonymous codon use and DNA polymorphism within the Drosophila genome. J Evol Biol 19 1 11

56. Eyre-WalkerA

2002 Changing effective population size and the McDonald-Kreitman test. Genetics 162 2017 2024

57. MustoH

RomeroH

ZavalaA

JabbariK

BernardiG

1999 Synonymous codon choices in the extremely GC-poor genome of Plasmodium falciparum: compositional constraints and translational selection. Journal of molecular evolution 49 27 35

58. ConwayDJ

FanelloC

LloydJM

Al-JouboriBM

BalochAH

2000 Origin of Plasmodium falciparum malaria is traced by mitochondrial DNA. Mol Biochem Parasitol 111 163 171

59. JoyDA

FengX

MuJ

FuruyaT

ChotivanichK

2003 Early origin and recent expansion of Plasmodium falciparum. Science 300 318 321

60. CarltonJM

AdamsJH

SilvaJC

BidwellSL

LorenziH

2008 Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455 757 763

61. DeweyCN

2007 Aligning multiple whole genomes with Mercator and MAVID. Methods Mol Biol 395 221 236

62. KentWJ

2002 BLAT–the BLAST-like alignment tool. Genome Res 12 656 664

63. HirshAE

FraserHB

2001 Protein dispensability and rate of evolution. Nature 411 1046 1049

64. BrayN

PachterL

2004 MAVID: constrained ancestral alignment of multiple sequences. Genome Res 14 693 699

65. YangZ

2007 PAML 4: phylogenetic analysis by maximum likelihood. Mol Biol Evol 24 1586 1591

66. PondSL

FrostSD

MuseSV

2005 HyPhy: hypothesis testing using phylogenies. Bioinformatics 21 676 679

67. VilellaAJ

Blanco-GarciaA

HutterS

RozasJ

2005 VariScan: Analysis of evolutionary patterns from large-scale DNA sequence polymorphism data. Bioinformatics 21 2791 2793

68. R Development Core Team 2007 R: A Language and Environment for Statistical Computing Vienna, Austria

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PLOS Genetics


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