Association Mapping and the Genomic Consequences of Selection in Sunflower

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The combination of large-scale population genomic analyses and trait-based mapping approaches has the potential to provide novel insights into the evolutionary history and genome organization of crop plants. Here, we describe the detailed genotypic and phenotypic analysis of a sunflower (Helianthus annuus L.) association mapping population that captures nearly 90% of the allelic diversity present within the cultivated sunflower germplasm collection. We used these data to characterize overall patterns of genomic diversity and to perform association analyses on plant architecture (i.e., branching) and flowering time, successfully identifying numerous associations underlying these agronomically and evolutionarily important traits. Overall, we found variable levels of linkage disequilibrium (LD) across the genome. In general, islands of elevated LD correspond to genomic regions underlying traits that are known to have been targeted by selection during the evolution of cultivated sunflower. In many cases, these regions also showed significantly elevated levels of differentiation between the two major sunflower breeding groups, consistent with the occurrence of divergence due to strong selection. One of these regions, which harbors a major branching locus, spans a surprisingly long genetic interval (ca. 25 cM), indicating the occurrence of an extended selective sweep in an otherwise recombinogenic interval.

Vyšlo v časopise: Association Mapping and the Genomic Consequences of Selection in Sunflower. PLoS Genet 9(3): e32767. doi:10.1371/journal.pgen.1003378
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003378

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Zdroje

1. ClarkRM, LintonE, MessingJ, DoebleyJF (2004) Pattern of diversity in the genomic region near the maize domestication gene tb1. Proc Natl Acad Sci U S A 101: 700–707.

2. OlsenKM, CaicedoAL, PolatoN, McClungA, McCouchS, et al. (2006) Selection Under Domestication: Evidence for a Sweep in the Rice Waxy Genomic Region. Genetics 173: 975–983.

3. WangE, WangJ, ZhuX, HaoW, WangL, et al. (2008) Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat Genet 40: 1370–1374 doi:10.1038/ng.220.

4. VigourouxY, McMullenM, HittingerCT, HouchinsK, SchulzL, et al. (2002) Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc Natl Acad Sci U S A 99: 9650–9655.

5. CasaAM, MitchellSE, HamblinMT, SunH, BowersJE, et al. (2005) Diversity and selection in sorghum: simultaneous analyses using simple sequence repeats. Theor Appl Genet 111: 23–30.

6. NielsenR (2005) Molecular signatures of natural selection. Ann Rev Genet 39: 197–218 doi:10.1146/annurev.genet.39.073003.112420.

7. DoebleyJ, StecA, WendelJ, EdwardsM (1990) Genetic and morphological analysis of a maize-teosinte F2 population: implications for the origin of maize. Proc Natl Acad Sci U S A 87: 9888–9892.

8. XiongLZ, LiuKD, DaiXK, XuCG, ZhangQ (1999) Identification of genetic factors controlling domestication-related traits of rice using an F 2 population of a cross between Oryza sativa and O. rufipogon. Theor Appl Genet 98: 243–251 doi:10.1007/s001220051064.

9. BurkeJM, TangS, KnappSJ, RiesebergLH (2002) Genetic analysis of sunflower domestication. Genetics 161: 1257–1267.

10. YuJ, BucklerES (2006) Genetic association mapping and genome organization of maize. Curr Opin Biotech 17: 155–160 doi:10.1016/j.copbio.2006.02.003.

11. PritchardJK, StephensM, RosenbergNA, DonnellyP (2000) Association mapping in structured populations. Am J Hum Genet 67: 170–181 doi:10.1086/302959.

12. BucklerES, ThornsberryJM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5: 107–111.

13. AranzanaMJ, KimS, ZhaoK, BakkerE, HortonM, et al. (2005) Genome-wide association mapping in Arabidopsis identifies previously known flowering time and pathogen resistance genes. PLoS Genet 1: e60 doi:10.1371/journal.pgen.0010060.

14. PriceAL, PattersonNJ, PlengeRM, WeinblattME, ShadickNA, et al. (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38: 904–909 doi:10.1038/ng1847.

15. YuJ, PressoirG, BriggsWH, Vroh BiI, YamasakiM, et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38: 203–208 doi:10.1038/ng1702.

16. CollardBCY, MackillDJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc Lond B Biol Sci 363: 557–572 doi:10.1098/rstb.2007.2170.

17. HeiserCB, Smith DMCS (1969) MW (1969) The North American sunflower (Helianthus). Mem Torrey Bot Club 22: 1–218.

18. SmithBD (1989) Origins of agriculture in eastern North America. Science (New York, NY) 246: 1566–1571 doi:10.1126/science.246.4937.1566.

19. SoleriD (1993) DAC (1993) Hopi crop diversity and change. J Ethnobiol 13: 203–231.

20. BachlavaE, TaylorCA, TangS, BowersJE, MandelJR, et al. (2012) SNP discovery and development of a high-density genotyping array for sunflower. PLoS ONE 7: e29814 doi:10.1371/journal.pone.0029814.

21. BowersJE, BachlavaE, BrunickRK, RiesebergLH, KnappSJ, et al. (2012) Development of a 10,000 locus genetic map of the sunflower genome based on multiple crosses. G3 2: 721–729.

22. MandelJR, DechaineJM, MarekLF, BurkeJM (2011) Genetic diversity and population structure in cultivated sunflower and a comparison to its wild progenitor, Helianthus annuus L. Theor Appl Genet 123: 693–704 doi:10.1007/s00122-011-1619-3.

23. BeardB (1982) Registration of Helianthus germplasm pools III and IV. Crop Science 22: 1276–1277.

24. KorellM, Mösges GFW (1992) Construction of a sunflower pedigree map. Helia 15: 7–16.

25. DoyleJLDJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11–15.

26. NeiM (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583–590.

27. PeakallR, SmousePE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6: 288–295 doi:10.1111/j.1471-8286.2005.01155.x.

28. PritchardJK, StephensM, DonnellyP (2000) Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

29. EvannoG, RegnautS, GoudetJ (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14: 2611–2620 doi:10.1111/j.1365-294X.2005.02553.x.

30. HardyOJ, VekemansX (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2: 618–620 doi:10.1046/j.1471-8278.

31. MacdonaldSJ, PastinenT, LongAD (2005) The effect of polymorphisms in the enhancer of split gene complex on bristle number variation in a large wild-caught cohort of Drosophila melanogaster. Genetics 171: 1741–1756.

32. FollM, GaggiottiO (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180: 977–993.

33. BradburyPJ, ZhangZ, KroonDE, CasstevensTM, RamdossY, et al. (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics (Oxford, England) 23: 2633–2635 doi:10.1093/bioinformatics/btm308.

34. De Silva HN, Ball RD (2007) Linkage disequilibrium mapping concepts. In: Oraguzie NC, Rikkerink EHA, Gardiner SE, Silva HN, editors. Association mapping in plants. New York: Springer. pp. 103–132.

35. GaoX, StarmerJ, MartinER (2008) A multiple testing correction method for genetic association studies using correlated single nucleotide polymorphisms. Genet Epidemiol 32: 361–369 doi:10.1002/gepi.20310.

36. TangS, YuJK, SlabaughB, ShintaniK, KnappJ (2002) Simple sequence repeat map of the sunflower genome. Theor Appl Genet 105: 1124–1136 doi:10.1007/s00122-002-0989-y.

37. WangM, JiangN, JiaT, LeachL, CockramJ, et al. (2012) Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theor Appl Genet 124: 233–246 doi:10.1007/s00122-011-1697-2.

38. ChingA, CaldwellKS, JungM, DolanM, SmithOS, et al. (2002) SNP frequency, haplotype structure and linkage disequilibrium in elite maize inbred lines. BMC Genet 3: 19.

39. JonesE, ChuW-C, AyeleM, HoJ, BruggemanE, et al. (2009) Development of single nucleotide polymorphism (SNP) markers for use in commercial maize (Zea mays L.) germplasm. Mol Breed 24: 165–176 doi:10.1007/s11032-009-9281-z.

40. YanJ, ShahT, WarburtonML, BucklerES, McMullenMD, et al. (2009) Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS ONE 4: e8451 doi:10.1371/journal.pone.0008451.

41. HamblinMT, CloseTJ, BhatPR, ChaoS, KlingJG, et al. (2010) Population structure and linkage disequilibrium in U.S. barley germplasm: implications for association mapping. Crop Science 50: 556 doi:10.2135/cropsci2009.04.0198.

42. ChenH, HeH, ZouY, ChenW, YuR, et al. (2011) Development and application of a set of breeder-friendly SNP markers for genetic analyses and molecular breeding of rice (Oryza sativa L.). Theor Appl Genet 123: 869–879 doi:10.1007/s00122-011-1633-5.

43. MorinPA, LuikartG, WayneRK (2004) SNPs in ecology, evolution and conservation. Trends Ecol Evol 19: 208–216 doi:10.1016/j.tree.2004.01.009.

44. Ferh WR (1987) Principles of cultivar development: theory and technique. Vol 1. New York: Macmillan.

45. Fick GN MJ (1997) Sunflower breeding. In: AA S, editor. Sunflower production and technology. Madison: American Society of Agronomy. pp. 395–440.

46. SackstonWE (1992) On a treadmill: breeding sunflowers for resistance to disease. Ann Rev Phytopathol 30: 529–551.

47. MouzeyarS, Roeckel-DrevetP, GentzbittelL, PhilipponJ, Tourvieille De LabrouheD, et al. (1995) RFLP and RAPD mapping of the sunflower Pl1 locus for resistance to Plasmopara halstedii race 1. Theor Appl Genet 91: 733–737 doi:10.1007/BF00220951.

48. Roeckel-DrevetP, TourvieilleJ, GulyaTJ, CharmetG, NicolasP, et al. (2003) Molecular variability of sunflower downy mildew, Plasmopara halstedii, from different continents. Can J Microbiol 49: 492–502.

49. VearF, GarreynM, LabrouheDT (1997) Inheritance of resistance to phomopsis (Diaporthe helianthi) in sunflower. Plant Breed 116: 277–281 doi:10.1111/j.1439-0523.1997.tb00996.x.

50. BertPF, Tourvieille De LabrouheD, PhilipponJ, MouzeyarS, JouanI, et al. (2001) Identification of a second linkage group carrying genes controlling resistance to downy mildew (Plasmopara halstedii) in sunflower (Helianthus annuus L.). Theor Appl Genet 103: 992–997 doi:10.1007/s001220100660.

51. BrahmL, RocherT, FriedtW (2000) PCR-based markers facilitating marker assisted selection in sunflower for resistance to downy mildew. Crop Science 40: 676–682.

52. BachlavaE, RadwanOE, AbrattiG, TangS, GaoW, et al. (2011) Downy mildew (Pl (8) and Pl (14)) and rust (R (Adv)) resistance genes reside in close proximity to tandemly duplicated clusters of non-TIR-like NBS-LRR-encoding genes on sunflower chromosomes 1 and 13. Theor Appl Genet 122: 1211–1221 doi:10.1007/s00122-010-1525-0.

53. Al-ChaaraniGR, RoustaeeA, GentzbittelL, MokraniL, BarraultG, et al. (2002) A QTL analysis of sunflower partial resistance to downy mildew (Plasmopara halstedii) and black stem (Phoma macdonaldii) by the use of recombinant inbred lines (RILs). Theor Appl Genet 104: 490–496 doi:10.1007/s001220100742.

54. YuJK, TangS, SlabaughMB, HeesackerA, ColeG, et al. (2003) Towards a saturated molecular genetic linkage map for cultivated sunflower. Crop Science 43: 367–387.

55. HeiserCB (1945) The Hopi sunflower. Mo Bot Gard Bull 3: 163–166.

56. HeiserCB (1951) The sunflower among the North American Indians. Proc Am Philos Soc 95: 432–448.

57. Rogers CE, Thompson TE SG (1982) Sunflower species of the United States. Bismark, ND: National Sunflower Association.

58. BachlavaE, TangS, PizarroG, SchuppertGF, BrunickRK, et al. (2010) Pleiotropy of the branching locus (B) masks linked and unlinked quantitative trait loci affecting seed traits in sunflower. Theor Appl Genet 120: 829–842 doi:10.1007/s00122-009-1212-1.

59. WillsDM, BurkeJM (2007) Quantitative trait locus analysis of the early domestication of sunflower. Genetics 176: 2589–2599 doi:10.1534/genetics.107.075333.

60. WillsDM, Abdel-HaleemH, KnappSJ, BurkeJM (2010) Genetic architecture of novel traits in the Hopi sunflower. J Hered 101: 727–736.

61. DechaineJM, BurgerJC, ChapmanMA, SeilerGJ, BrunickR, et al. (2009) Fitness effects and genetic architecture of plant-herbivore interactions in sunflower crop-wild hybrids. New Phyt 184: 828–841.

62. BlackmanBK, RasmussenDA, StrasburgJL, RaduskiAR, BurkeJM, et al. (2011) Contributions of flowering time genes to sunflower domestication and improvement. Genetics 187: 271–287 doi:10.1534/genetics.110.121327.

63. ElshireRJ, GlaubitzJC, SunQ, PolandJA, KawamotoK, et al. (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE 6: e19379.