A Genome-Wide, Fine-Scale Map of Natural Pigmentation Variation in
Various approaches can be applied to uncover the genetic basis of natural phenotypic variation, each with their specific strengths and limitations. Here, we use a replicated genome-wide association approach (Pool-GWAS) to fine-scale map genomic regions contributing to natural variation in female abdominal pigmentation in Drosophila melanogaster, a trait that is highly variable in natural populations and highly heritable in the laboratory. We examined abdominal pigmentation phenotypes in approximately 8000 female European D. melanogaster, isolating 1000 individuals with extreme phenotypes. We then used whole-genome Illumina sequencing to identify single nucleotide polymorphisms (SNPs) segregating in our sample, and tested these for associations with pigmentation by contrasting allele frequencies between replicate pools of light and dark individuals. We identify two small regions near the pigmentation genes tan and bric-à-brac 1, both corresponding to known cis-regulatory regions, which contain SNPs showing significant associations with pigmentation variation. While the Pool-GWAS approach suffers some limitations, its cost advantage facilitates replication and it can be applied to any non-model system with an available reference genome.
Vyšlo v časopise:
A Genome-Wide, Fine-Scale Map of Natural Pigmentation Variation in. PLoS Genet 9(6): e32767. doi:10.1371/journal.pgen.1003534
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003534
Souhrn
Various approaches can be applied to uncover the genetic basis of natural phenotypic variation, each with their specific strengths and limitations. Here, we use a replicated genome-wide association approach (Pool-GWAS) to fine-scale map genomic regions contributing to natural variation in female abdominal pigmentation in Drosophila melanogaster, a trait that is highly variable in natural populations and highly heritable in the laboratory. We examined abdominal pigmentation phenotypes in approximately 8000 female European D. melanogaster, isolating 1000 individuals with extreme phenotypes. We then used whole-genome Illumina sequencing to identify single nucleotide polymorphisms (SNPs) segregating in our sample, and tested these for associations with pigmentation by contrasting allele frequencies between replicate pools of light and dark individuals. We identify two small regions near the pigmentation genes tan and bric-à-brac 1, both corresponding to known cis-regulatory regions, which contain SNPs showing significant associations with pigmentation variation. While the Pool-GWAS approach suffers some limitations, its cost advantage facilitates replication and it can be applied to any non-model system with an available reference genome.
Zdroje
1. YiX, LiangY, Huerta-SanchezE, JinX, CuoZX, et al. (2010) Sequencing of 50 human exomes reveals adaptation to high altitude. Science 329: 75–78.
2. HancockAM, BrachiB, FaureN, HortonMW, JarymowyczLB, et al. (2011) Adaptation to climate across the Arabidopsis thaliana genome. Science 334: 83–86.
3. HuangX, WeiX, SangT, ZhaoQ, FengQ, et al. (2010) Genome-wide association studies of 14 agronomic traits in rice landraces. Nat Genet 42: 961–967.
4. KarlssonEK, BaranowskaI, WadeCM, Salmon HillbertzNHC, ZodyMC, et al. (2007) Efficient mapping of mendelian traits in dogs through genome-wide association. Nat Genet 39: 1321–1328.
5. Makvandi-NejadS, HoffmanGE, AllenJJ, ChuE, GuE, et al. (2012) Four loci explain 83% of size variation in the horse. PLoS One 7: e39929.
6. Morgan TH, Sturtevant AH, Muller HJ, Bridges CB (1915) The mechanism of Mendelian heredity. New York: Henry Holt and Company.
7. TrueJR (2003) Insect melanism: the molecules matter. Trends in Ecology & Evolution 18: 640–647.
8. WittkoppPJ, CarrollSB, KoppA (2003) Evolution in black and white: genetic control of pigment patterns in Drosophila. Trends Genet 19: 495–504.
9. SimpsonP (2007) The stars and stripes of animal bodies: evolution of regulatory elements mediating pigment and bristle patterns in Drosophila. Trends Genet 23: 350–358.
10. WittkoppPJ, BeldadeP (2009) Development and evolution of insect pigmentation: genetic mechanisms and the potential consequences of pleiotropy. Semin Cell Dev Biol 20: 65–71.
11. RobertsonA, BriscoeDA, LouwJH (1977) Variation in abdomen pigmentation in Drosophila melanogaster females. Genetica 47: 73–76.
12. DavidJR, CapyP, GauthierJP (1990) Abdominal pigmentation and growth temperature in Drosophila melanogaster: Similarities and differences in the norms of reaction of successive segments. J Evol Biol 3: 429–445.
13. LachaiseD, HarryM, SolignacM, LemeunierF, BenassiV, et al. (2000) Evolutionary novelties in islands: Drosophila santomea, a new melanogaster sister species from Sao Tome. Proc Biol Sci 267: 1487–1495.
14. GibertJM, PeronnetF, SchlöttererC (2007) Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network. PLoS Genet 3: e30.
15. JeongS, RebeizM, AndolfattoP, WernerT, TrueJ, et al. (2008) The evolution of gene regulation underlies a morphological difference between two Drosophila sister species. Cell 132: 783–793.
16. KoppA, DuncanI, GodtD, CarrollSB (2000) Genetic control and evolution of sexually dimorphic characters in Drosophila. Nature 408: 553–559.
17. WilliamsTM, SelegueJE, WernerT, GompelN, KoppA, et al. (2008) The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila. Cell 134: 610–623.
18. Telonis-ScottM, HoffmannAA, SgroCM (2011) The molecular genetics of clinal variation: a case study of ebony and thoracic trident pigmentation in Drosophila melanogaster from eastern Australia. Mol Ecol 20: 2100–2110.
19. PoolJE, AquadroCF (2007) The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. Mol Ecol 16: 2844–2851.
20. ParkashR, RajpurohitS, RamniwasS (2008) Changes in body melanisation and desiccation resistance in highland vs. lowland populations of D. melanogaster. J Insect Physiol 54: 1050–1056.
21. TrueJR, YehSD, HovemannBT, KemmeT, MeinertzhagenIA, et al. (2005) Drosophila tan encodes a novel hydrolase required in pigmentation and vision. PLoS Genet 1: e63.
22. JeongS, RokasA, CarrollSB (2006) Regulation of body pigmentation by the Abdominal-B Hox protein and its gain and loss in Drosophila evolution. Cell 125: 1387–1399.
23. RebeizM, PoolJE, KassnerVA, AquadroCF, CarrollSB (2009) Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326: 1663–1667.
24. BickelRD, KoppA, NuzhdinSV (2011) Composite effects of polymorphisms near multiple regulatory elements create a major-effect QTL. PLoS Genet 7: e1001275.
25. KoppA, GrazeRM, XuS, CarrollSB, NuzhdinSV (2003) Quantitative trait loci responsible for variation in sexually dimorphic traits in Drosophila melanogaster. Genetics 163: 771–787.
26. ShamP, BaderJS, CraigI, O'DonovanM, OwenM (2002) DNA pooling: A tool for large-scale association studies. Nat Rev Genetics 3: 862–871.
27. FutschikA, SchlöttererC (2010) The next generation of molecular markers from massively parallel sequencing of pooled DNA samples. Genetics 186: 207–218.
28. KimSY, LiYR, GuoYR, LiRQ, HolmkvistJ, et al. (2010) Design of association studies with pooled or un-pooled next-generation sequencing data. Genetic Epidemiology 34: 479–491.
29. MiyashitaN, LangleyCH (1988) Molecular and phenotypic variation of the white locus region in Drosophila melanogaster. Genetics 120: 199–212.
30. MackayTF, RichardsS, StoneEA, BarbadillaA, AyrolesJF, et al. (2012) The Drosophila melanogaster Genetic Reference Panel. Nature 482: 173–178.
31. LangleyCH, StevensK, CardenoC, LeeYC, SchriderDR, et al. (2012) Genomic variation in natural populations of Drosophila melanogaster. Genetics 192: 533–98.
32. CoudercJL, GodtD, ZollmanS, ChenJ, LiM, et al. (2002) The bric à brac locus consists of two paralogous genes encoding BTB/POZ domain proteins and acts as a homeotic and morphogenetic regulator of imaginal development in Drosophila. Development 129: 2419–2433.
33. Orozco-terWengelP, CoranderJ, SchlöttererC (2011) Genealogical lineage sorting leads to significant, but incorrect Bayesian multilocus inference of population structure. Mol Ecol 20: 1108–1121.
34. KoflerR, BetancourtAJ, SchlöttererC (2012) Sequencing of pooled DNA samples (Pool-Seq) uncovers complex dynamics of transposable element insertions in Drosophila melanogaster. PLoS Genet 8: e1002487.
35. CarboneMA, LlopartA, DeAngelisM, CoyneJA, MackayTFC (2005) Quantitative trait loci affecting the difference in pigmentation between Drosophila yakuba and D. santomea. Genetics 171: 211–225.
36. MatuteDR, ButlerIA, CoyneJA (2009) Little effect of the tan locus on pigmentation in female hybrids between Drosophila santomea and D. melanogaster. Cell 139: 1180–1188.
37. GompelN, Prud'hommeB (2009) The causes of repeated genetic evolution. Devel Biol 332: 36–47.
38. BrissonJA, TempletonAR, DuncanI (2004) Population genetics of the developmental gene optomotor-blind (omb) in Drosophila polymorpha: Evidence for a role in abdominal pigmentation variation. Genetics 168: 1999–2010.
39. NgCS, HamiltonAM, FrankA, BarminaO, KoppA (2008) Genetic basis of sex-specific color pattern variation in Drosophila malerkotliana. Genetics 180: 421–429.
40. DavidJR, CapyP, PayantV, TsakasS (1985) Thoracic trident pigmentation in Drosophila melanogaster: differentiation of geographical populations. Genetics Sel Evol 17: 211–223.
41. GibertP, MoreteauB, MoreteauJC, ParkashR, DavidJR (1998) Light body pigmentation in Indian Drosophila melanogaster: a likely adaptation to a hot and arid climate. J of Genetics 77: 13–20.
42. MunjalAK, KaranD, GibertP, MoreteauB, ParkashR, et al. (1997) Thoracic trident pigmentation in Drosophila melanogaster: Latitudinal and altitudinal clines in Indian populations. Genetics Selection Evolution 29: 601–610.
43. Hudson RR (1991) Gene genealogies and the coalescent process. In: Futuyma D, Antonivics J, editors. Oxford surveys in evolutionary biology. Oxford: Oxford University Press. pp. 1–44.
44. GibertP, MoreteauB, DavidJR (2000) Developmental constraints on an adaptive plasticity: reaction norms of pigmentation in adult segments of Drosophila melanogaster. Evol & Devel 2: 249–260.
45. PritchardJK, PrzeworskiM (2001) Linkage disequilibrium in humans: models and data. Am J Hum Genet 69: 1–14.
46. MichelmoreRW, ParanI, KesseliRV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci U S A 88: 9828–9832.
47. EhrenreichIM, TorabiN, JiaY, KentJ, MartisS, et al. (2010) Dissection of genetically complex traits with extremely large pools of yeast segregants. Nature 464: 1039–1042.
48. HuangW, RichardsS, CarboneMA, ZhuD, AnholtRR, et al. (2012) Epistasis dominates the genetic architecture of Drosophila quantitative traits. Proc Natl Acad Sci U S A 109: 15553–15559.
49. BurkeMK, DunhamJP, ShahrestaniP, ThorntonKR, RoseMR, et al. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature 467: 587–590.
50. ZhouD, UdpaN, GerstenM, ViskDW, BashirA, et al. (2011) Experimental selection of hypoxia-tolerant Drosophila melanogaster. Proc Natl Acad Sci U S A 108: 2349–2354.
51. Orozco-terWengelP, KapunM, NolteV, KoflerR, FlattT, et al. (2012) Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected alleles. Mol Ecol 21: 4931–4941.
52. TurnerTL, StewartAD, FieldsAT, RiceWR, TaroneAM (2011) Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster. PLoS Genet 7: e1001336.
53. TurnerTL, MillerPM (2012) Investigating natural variation in Drosophila courtship song by the evolve and resequence approach. Genetics 191: 633–642.
54. GibertP, MoreteauB, ScheinerSM, DavidJR (1998) Phenotypic plasticity of body pigmentation in Drosophila: correlated variations between segments. Genetics Sel Evol 30: 181–194.
55. KoflerR, Orozco-terWengelP, De MaioN, PandeyRV, NolteV, et al. (2011) PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One 6: e15925.
56. LiH, DurbinR (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754–1760.
57. LiH, HandsakerB, WysokerA, FennellT, RuanJ, et al. (2009) The Sequence alignment/map format and SAMtools. Bioinformatics 25: 2078–2079.
58. SturtevantAH (1919) A new species closely resembling Drosphila melanogaster.. Psyche 26: 153–155.
59. WuTD, NacuS (2010) Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26: 873–881.
60. WuTD, WatanabeCK (2005) GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics 21: 1859–1875.
61. KoflerR, PandeyRV, SchlöttererC (2011) PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 27: 3435–3436.
62. CingolaniP, PlattsA, Wang leL, CoonM, NguyenT, et al. (2012) A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin) 6: 80–92.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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