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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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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