A Genome-Wide Association Study of Resistance to Stripe Rust ( Puccinia striiformis f. sp. tritici ) in a Worldwide Collection of Hexaploid Spring Wheat ( Triticum aestivum L.)

Abstract

New races of Puccinia striiformis f. sp. tritici (Pst), the causal pathogen of wheat stripe rust, show high virulence to previously deployed resistance genes and are responsible for large yield losses worldwide. To identify new sources of resistance we performed a genome-wide association study (GWAS) using a worldwide collection of 1000 spring wheat accessions. Adult plants were evaluated under field conditions in six environments in the western United States, and seedlings were tested with four Pst races. A single-nucleotide polymorphism (SNP) Infinium 9K-assay provided 4585 SNPs suitable for GWAS. High correlations among environments and high heritabilities were observed for stripe rust infection type and severity. Greater levels of Pst resistance were observed in a subpopulation from Southern Asia than in other groups. GWAS identified 97 loci that were significant for at least three environments, including 10 with an experiment-wise adjusted Bonferroni probability < 0.10. These 10 quantitative trait loci (QTL) explained 15% of the phenotypic variation in infection type, a percentage that increased to 45% when all QTL were considered. Three of these 10 QTL were mapped far from previously identified Pst resistance genes and QTL, and likely represent new resistance loci. The other seven QTL mapped close to known resistance genes and allelism tests will be required to test their relationships. In summary, this study provides an integrated view of stripe rust resistance resources in spring wheat and identifies new resistance loci that will be useful to diversify the current set of resistance genes deployed to control this devastating disease.

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References 95

1. 1.

   Adhikari T. B. Jackson E. W. Gurung S. Hansen J. M. Bonman J. M., 2011 Association mapping of quantitative resistance to Phaeosphaeria nodorum in spring wheat landraces from the USDA National Small Grains Collection. Phytopathology 101: 1301–1310.

   Not in our library10.1094/phyto-03-11-0076

2. 2.

   Agenbag G. M. Pretorius Z. A. Boyd L. A. Bender C. M. Prins R., 2012 Identification of adult plant resistance to stripe rust in the wheat cultivar Cappelle-Desprez. Theor. Appl. Genet. 125: 109–120.

   Not in our library10.1007/s00122-012-1819-5

3. 3.
   Origin, Migration Routes and Worldwide Population Genetic Structure of the Wheat Yellow Rust Pathogen Puccinia striiformis f.sp. tritici · 2014

   No notice
4. 4.

   Ardlie K. G. Kruglyak L. Seielstad M., 2002 Patterns of linkage disequilibrium in the human genome. Nat. Rev. Genet. 3: 299–309.

   Not in our library10.1038/nrg777

5. 5.

   Barrett J. C. Fry B. Maller J. Daly M. J., 2005 Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21: 263–265.

   Not in our library10.1093/bioinformatics/bth457

6. 6.
   Linkage and Association Mapping of Arabidopsis thaliana Flowering Time in Nature · 2010

   No notice
7. 7.

   Brachi B. Morris G. P. Borevitz J. O., 2011 Genome-wide association studies in plants: the missing heritability is in the field. Genome Biol. 12: 232.

   Not in our library10.1186/gb-2011-12-10-232

8. 8.

   Breseghello F. Sorrells M. E., 2006 Association mapping of kernel size and milling quality in wheat (Triticum aestivum L.) cultivars. Genetics 172: 1165–1177.

   Not in our library10.1534/genetics.105.044586

9. 9.

   Cavanagh C. R. Chao S. M. Wang S. C. Huang B. E. Stephen S., 2013 Genome-wide comparative diversity uncovers multiple targets of selection for improvement in hexaploid wheat landraces and cultivars. Proc. Natl. Acad. Sci. USA 110: 8057–8062.

   Not in our library10.1073/pnas.1217133110

10. 10.
    Population- and genome-specific patterns of linkage disequilibrium and SNP variation in spring and winter wheat (Triticum aestivum L.) · 2010

    No notice
11. 11.

    Chen W. Wellings C. Chen X. M. Kang Z. Liu T., 2014 Wheat stripe (yellow) rust caused by Puccinia striiformis f. sp. tritici. Mol. Plant Pathol. 15: 433–446.

    Not in our library10.1111/mpp.12116

12. 12.

    Chen X. M., 2005 Epidemiology and control of stripe rust (Puccinia striiformis f. sp tritici) on wheat. Can. J. Plant Pathol. 27: 314–337.

    Not in our library

13. 13.

    Chen X. M., 2013 High-temperature adult-plant resistance, key for sustainable control of stripe rust. Am. J. Plant Sci. 4: 608–627.

    Not in our library

14. 14.

    Chen X. M. Penman L. Wan A. M. Cheng P., 2010 Virulence races of Puccinia striiformis f. sp tritici in 2006 and 2007 and development of wheat stripe rust and distributions, dynamics, and evolutionary relationships of races from 2000 to 2007 in the United States. Can. J. Plant Pathol. 32: 315–333.

    Not in our library

15. 15.

    Chisholm S. T. Coaker G. Day B. Staskawicz B. J., 2006 Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124: 803–814.

    Not in our library10.1016/j.cell.2006.02.008

16. 16.

    Christopher M. D. Liu S. Y. Hall M. D. Marshall D. S. Fountain M. O., 2013 Identification and mapping of adult-plant stripe rust resistance in soft red winter wheat cultivar ’USG 3555’. Plant Breed. 132: 53–60.

    Not in our library

17. 17.

    Corbeil R. R. Searle S. R., 1976 Restricted maximum likelihood (REML) estimation of variance components in mixed model. Technometrics 18: 31–38.

    Not in our library

18. 18.

    Darvasi A. Soller M., 1997 A simple method to calculate resolving power and confidence interval of QTL map location. Behav. Genet. 27: 125–132.

    Not in our library10.1023/a:1025685324830

19. 19.

    Devos K. M. Dubcovsky J. Dvorak J. Chinoy C. N. Gale M. D., 1995 Structural evolution of wheat chromosomes 4A, 5A, and 7B and its impact on recombination. Theor. Appl. Genet. 91: 282–288.

    Not in our library10.1007/bf00220890

20. 20.

    Dimmock J. P. R. E. Gooding M. J., 2002 The influence of foliar diseases, and their control by fungicides, on the protein concentration in wheat grain: a review. J. Agric. Sci. 138: 349–366.

    Not in our library

21. 21.

    Dodig D. Zoric M. Kobiljski B. Savic J. Kandic V., 2012 Genetic and association mapping study of wheat agronomic traits under contrasting water regimes. Int. J. Mol. Sci. 13: 6167–6188.

    Not in our library10.3390/ijms13056167

22. 22.

    Dubcovsky J. Dvorak J., 2007 Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316: 1862–1866.

    Not in our library10.1126/science.1143986

23. 23.

    Earl D. A. Vonholdt B. M., 2012 STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4: 359–361.

    Not in our library

24. 24.

    Evanno G. Regnaut S. Goudet J., 2005 Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14: 2611–2620.

    Not in our library10.1111/j.1365-294x.2005.02553.x

25. 25.
    Arlequin (version 3.0): An integrated software package for population genetics data analysis · 2005

    No notice
26. 26.

    Flint-Garcia S. A. Thornsberry J. M. Buckler E. S., 2003 Structure of linkage disequilibrium in plants. Annu. Rev. Plant Biol. 54: 357–374.

    Not in our library10.1146/annurev.arplant.54.031902.134907

27. 27.

    Forrest K. Pujol V. Bulli P. Pumphrey M. Wellings C., 2014 Development of a SNP marker assay for the Lr67 gene of wheat using a genotyping by sequencing approach. Mol. Breed. 34: 2109–2118.

    Not in our library

28. 28.

    Hao C. Y. Wang Y. Q. Hou J. Feuillet C. Balfourier F., 2012 Association mapping and haplotype analysis of a 3.1-Mb genomic region involved in Fusarium head blight resistance on wheat chromosome 3BS. PLoS ONE 7: e46444.

    Not in our library10.1371/journal.pone.0046444

29. 29.

    Hodson D. P., 2011 Shifting boundaries: challenges for rust monitoring. Euphytica 179: 93–104.

    Not in our library

30. 30.

    Holsinger K. E. Weir B. S., 2009 Genetics in geographically structured populations: defining, estimating and interpreting F-ST. Nat. Rev. Genet. 10: 639–650.

    Not in our library10.1038/nrg2611

31. 31.

    Hovmoller M. S. Yahyaoui A. H. Milus E. A. Justesen A. F., 2008 Rapid global spread of two aggressive strains of a wheat rust fungus. Mol. Ecol. 17: 3818–3826.

    Not in our library10.1111/j.1365-294x.2008.03886.x

32. 32.

    Jia G. Q. Huang X. H. Zhi H. Zhao Y. Zhao Q., 2013 A haplotype map of genomic variations and genome-wide association studies of agronomic traits in foxtail millet (Setaria italica). Nat. Genet. 45: 957–961.

    Not in our library10.1038/ng.2673

33. 33.

    Johnson R., 1984 A critical analysis of durable resistance. Annu. Rev. Phytopathol. 22: 309–330.

    Not in our library

34. 34.

    Kang H. M. Zaitlen N. A. Wade C. M. Kirby A. Heckerman D., 2008 Efficient control of population structure in model organism association mapping. Genetics 178: 1709–1723.

    Not in our library10.1534/genetics.107.080101

35. 35.
    Extent of genome-wide linkage disequilibrium in Australian Holstein-Friesian cattle based on a high-density SNP panel · 2008

    No notice
36. 36.

    Kollers S. Rodemann B. Ling J. Korzun V. Ebmeyer E., 2013 Whole genome association mapping of Fusarium head blight resistance in European winter wheat (Triticum aestivum L.). PLoS ONE 8: e57500.

    Not in our library10.1371/journal.pone.0057500

37. 37.

    Kolmer J. A., 1996 Genetics of resistance to wheat leaf rust. Annu. Rev. Phytopathol. 34: 435–455.

    Not in our library10.1146/annurev.phyto.34.1.435

38. 38.

    Kolmer J. A. Chen X. Yue J., 2009 Diseases which challenge global wheat production-the wheat rusts, pp 89−124 in Wheat: Science and Trade, edited by Carver B. F. Wiley-Blackwell, Ames, IA.

    Not in our library

39. 39.

    Krasileva K. V. Buffalo V. Bailey P. Pearce S. Ayling S., 2013 Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biol. 14: R66.

    Not in our library10.1186/gb-2013-14-6-r66

40. 40.

    Krattinger S. G. Lagudah E. S. Spielmeyer W. Singh R. P. Huerta-Espino J., 2009 A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323: 1360–1363.

    Not in our library10.1126/science.1166453

41. 41.

    Kulwal P. Ishikawa G. Benscher D. Feng Z. Y. Yu L. X., 2012 Association mapping for pre-harvest sprouting resistance in white winter wheat. Theor. Appl. Genet. 125: 793–805.

    Not in our library10.1007/s00122-012-1872-0

42. 42.

    Lagudah E. S. Krattinger S. G. Herrera-Foessel S. Singh R. P. Huerta-Espino J., 2009 Gene-specific markers for the wheat gene Lr34/Yr18/Pm38 which confers resistance to multiple fungal pathogens. Theor. Appl. Genet. 119: 889–898.

    Not in our library10.1007/s00122-009-1097-z

43. 43.

    Larsson S. J. Lipka A. E. Buckler E. S., 2013 Lessons from Dwarf8 on the strengths and weaknesses of structured association mapping. PLoS Genet. 9: e1003246.

    Not in our library10.1371/journal.pgen.1003246

44. 44.
    GLIDERS - A web-based search engine for genome-wide linkage disequilibrium between HapMap SNPs · 2009

    Not checked
45. 45.

    Letta T. Maccaferri M. Badebo A. Ammar K. Ricci A., 2013 Searching for novel sources of field resistance to Ug99 and Ethiopian stem rust races in durum wheat via association mapping. Theor. Appl. Genet. 126: 1237–1256.

    Not in our library10.1007/s00122-013-2050-8

46. 46.

    Line R. F., 2002 Stripe rust of wheat and barley in North America: a retrospective historical review. Annu. Rev. Phytopathol. 40: 75–118.

    Not in our library10.1146/annurev.phyto.40.020102.111645

47. 47.

    Line R. F. Qayoum A., 1992 Virulence, Aggressiveness, Evolution and Distribution of races of Puccinia striiformis (the Cause of Stripe Rust of Wheat) in North America, 1968–1987. Technical, Vol. 1788 United States Department of Agriculture, Washington, DC.

    Not in our library

48. 48.

    Lipka A. E. Tian F. Wang Q. S. Peiffer J. Li M., 2012 GAPIT: genome association and prediction integrated tool. Bioinformatics 28: 2397–2399.

    Not in our library10.1093/bioinformatics/bts444

49. 49.
    Genome-Wide Association Study and Pathway-Level Analysis of Tocochromanol Levels in Maize Grain · 2013

    No notice
50. 50.

    Lowe I. Cantu D. Dubcovsky J., 2011 a Durable resistance to the wheat rusts: integrating systems biology and traditional phenotype-based research methods to guide the deployment of resistance genes. Euphytica 179: 69–79.

    Not in our library10.1007/s10681-010-0311-z

51. 51.

    Lowe I. Jankuloski D. L. Chao S. Chen X. See D., 2011 b Mapping and validation of QTL which confer partial resistance to broadly virulent post-2000 North American races of stripe rust in hexaploid wheat. Theor. Appl. Genet. 123: 143–157.

    Not in our library10.1007/s00122-011-1573-0

52. 52.

    Maccaferri M. Ricci A. Salvi S. Milner S. G. Noli E., 2014 A high-density, SNP-based consensus map of tetraploid wheat as a bridge to integrate durum and bread wheat genomics and breeding. Plant Biotechnol. J. DOI: 10.1111/pbi.12288.

    Not in our library10.1111/pbi.12288

53. 53.

    McIntosh, R. A., Y. Yamazaki, J. Dubcovsky, W. J. Rogers, C. F. Morris et al., 2013 Catalogue of gene symbols for wheat in 12th International Wheat Genetics Symposium, edited by R.A. McIntosh, Yokohama, Japan.

    Not in our library

54. 54.

    McNeal F. Konzak C. Smith E. Tate W. Russell T., 1971 A Uniform System for Recording and Processing Cereal Research Data. USDA, Agricultural Research Service, Washington, DC.

    Not in our library

55. 55.

    Milus E. A. Kristensen K. Hovmoller M. S., 2009 Evidence for increased aggressiveness in a recent widespread strain of Puccinia striiformis f. sp. tritici causing stripe rust of wheat. Phytopathology 99: 89–94.

    Not in our library10.1094/phyto-99-1-0089

56. 56.

    Mohan A. Kulwal P. Singh R. Kumar V. Mir R. R., 2009 Genome-wide QTL analysis for pre-harvest sprouting tolerance in bread wheat. Euphytica 168: 319–329.

    Not in our library

57. 57.

    Monaco M. K. Stein J. Naithani S. Wei S. Dharmawardhana P., 2014 Gramene 2013: comparative plant genomics resources. Nucleic Acids Res. 42: D1193–D1199.

    Not in our library10.1093/nar/gkt1110

58. 58.

    Nemri A. Atwell S. Tarone A. M. Huang Y. S. Zhao K., 2010 Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping. Proc. Natl. Acad. Sci. USA 107: 10302–10307.

    Not in our library10.1073/pnas.0913160107

59. 59.

    Peiffer J. A. Flint-Garcia S. A. De Leon N. McMullen M. D. Kaeppler S. M., 2013 The genetic architecture of maize stalk strength. PLoS ONE 8: e67066.

    Not in our library10.1371/journal.pone.0067066

60. 60.

    Peiffer J. A. Romay M. C. Gore M. A. Flint-Garcia S. A. Zhang Z. W., 2014 The genetic architecture of maize height. Genetics 196: 1337.

    Not in our library10.1534/genetics.113.159152

61. 61.

    Percival J., 1921 The Wheat Plant: A Monograph. Duckworth and Co., London.

    Not in our library

62. 62.

    Pritchard J. K. Stephens M. Donnelly P., 2000 Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

    Not in our library10.1093/genetics/155.2.945

63. 63.

    R Core Team, 2013 R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

    Not in our library

64. 64.

    Reif J. C. Gowda M. Maurer H. P. Longin C. F. H. Korzun V., 2011 Association mapping for quality traits in soft winter wheat. Theor. Appl. Genet. 122: 961–970.

    Not in our library10.1007/s00122-010-1502-7

65. 65.

    Reimer S. Pozniak C. J. Clarke F. R. Clarke J. M. Somers D. J., 2008 Association mapping of yellow pigment in an elite collection of durum wheat cultivars and breeding lines. Genome 51: 1016–1025.

    Not in our library10.1139/g08-083

66. 66.

    Rexroad C. E. Vallejo R. L., 2009 Estimates of linkage disequilibrium and effective population size in rainbow trout. BMC Genet. 10: 83.

    Not in our library10.1186/1471-2156-10-83

67. 67.

    Saintenac C. Jiang D. Wang S. Akhunov E., 2013 Sequence-based mapping of the polyploid wheat genome. G3 (Bethesda). 3: 1105–1114.

    Not in our library10.1534/g3.113.005819

68. 68.

    Santra D. K. Chen X. M. Santra M. Campbell K. G. Kidwell K. K., 2008 Identification and mapping QTL for high-temperature adult-plant resistance to stripe rust in winter wheat (Triticum aestivum L.) cultivar ’Stephens’. Theor. Appl. Genet. 117: 793–802.

    Not in our library10.1007/s00122-008-0820-5

69. 69.

    Sharma-Poudyal D. Chen X. Rupp R. A., 2013 Potential oversummering and overwintering regions for the wheat stripe rust pathogen in the contiguous United States. Int. J. Biometeorol. 58: 987–997.

    Not in our library10.1007/s00484-013-0683-6

70. 70.

    Shifman S. Kuypers J. Kokoris M. Yakir B. Darvasi A., 2003 Linkage disequilibrium patterns of the human genome across populations. Hum. Mol. Genet. 12: 771–776.

    Not in our library10.1093/hmg/ddg088

71. 71.

    Singh R. P. Huerta-Espino J. Rajaram S., 2000 Achieving near-immunity to leaf and stripe rusts in wheat by combining slow rusting resistance genes. Acta Phytopathol Hun 35: 133–139.

    Not in our library

72. 72.

    Singh R. P. Huerta-Espino J. William H. M., 2005 Genetics and breeding for durable resistance to leaf and stripe rusts in wheat. Turk. J. Agric. For. 29: 121–127.

    Not in our library

73. 73.

    Somers D. J. Isaac P. Edwards K., 2004 A high-density microsatellite consensus map for bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 109: 1105–1114.

    Not in our library10.1007/s00122-004-1740-7

74. 74.

    Song Q. J. Shi J. R. Singh S. Fickus E. W. Costa J. M., 2005 Development and mapping of microsatellite (SSR) markers in wheat. Theor. Appl. Genet. 110: 550–560.

    Not in our library10.1007/s00122-004-1871-x

75. 75.

    Sosnowski O. Charcosset A. Joets J., 2012 BioMercator V3: an upgrade of genetic map compilation and quantitative trait loci meta-analysis algorithms. Bioinformatics 28: 2082–2083.

    Not in our library10.1093/bioinformatics/bts313

76. 76.

    Stewart N. C. Via L. E., 1993 A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14: 748–749.

    Not in our library

77. 77.

    Stich B. Mohring J. Piepho H. P. Heckenberger M. Buckler E. S., 2008 Comparison of mixed-model approaches for association mapping. Genetics 178: 1745–1754.

    Not in our library10.1534/genetics.107.079707

78. 78.

    Sukhwinder-Singh M. V. Hernandez J. Crossa P. K. Singh N. S. Bains, 2012 Multi-trait and multi-environment QTL analyses for resistance to wheat diseases. PLoS One 7: e38008.

    Not in our library10.1371/journal.pone.0038008

79. 79.

    Sved J. A., 1971 Linkage disequilibrium and homozigosity of chromosome segments in finite populations. Theor. Popul. Biol. 2: 125–141.

    Not in our library10.1016/0040-5809(71)90011-6

80. 80.

    Tengberg M., 1999 Crop husbandry at Miri Qalat, Makran, SW Pakistan (4000–2000 B.C.). Veg. Hist. Archeobot. 8: 3–12.

    Not in our library

81. 81.

    Turner S. Armstrong L. L. Bradford Y. Carlson C. S. Crawford D. C., 2011 Quality control procedures for genome wide association studies. Curr. Protoc. Hum. Genet. Chapter 1, Unit 1.19.

    Not in our library10.1002/0471142905.hg0119s68

82. 82.
    Genome-wide association mapping of flowering time and northern corn leaf blight (<it>Setosphaeria turcica</it>) resistance in a vast commercial maize germplasm set · 2012

    Not checked
83. 83.

    Vazquez M. D. Peterson C. J. Riera-Lizarazu O. Chen X. M. Heesacker A., 2012 Genetic analysis of adult plant, quantitative resistance to stripe rust in wheat cultivar ’Stephens’ in multi-environment trials. Theor. Appl. Genet. 124: 1–11.

    Not in our library10.1007/s00122-011-1681-x

84. 84.

    Wallace J. G. Larsson S. J. Buckler E. S., 2014 Entering the second century of maize quantitative genetics. Heredity 112: 30–38.

    Not in our library10.1038/hdy.2013.6

85. 85.

    Wan A. M. Chen X. M., 2014 Virulence characterization of Puccinia striiformis f. sp. tritici using a new set of Yr single-gene line differentials in the United States in 2010. Plant Dis. 98: 1534–1542.

    Not in our library10.1094/pdis-01-14-0071-re

86. 86.

    Wang J. R. Luo M. C. Chen Z. X. You F. M. Wei Y. M., 2013 Aegilops tauschii single nucleotide polymorphisms shed light on the origins of wheat D-genome genetic diversity and pinpoint the geographic origin of hexaploid wheat. New Phytol. 198: 925–937.

    Not in our library10.1111/nph.12164

87. 87.

    Wang M. H. Jiang N. Jia T. Y. Leach L. Cockram J., 2012 Genome-wide association mapping of agronomic and morphologic traits in highly structured populations of barley cultivars. Theor. Appl. Genet. 124: 233–246.

    Not in our library10.1007/s00122-011-1697-2

88. 88.
    Characterization of polyploid wheat genomic diversity using a high‐density 90 000 single nucleotide polymorphism array · 2014

    No notice
89. 89.

    Weir B. S., 1996 Genetic Data Analysis II. Sinauer Publishers, Sunderland, MA.

    Not in our library

90. 90.

    Yao J. Wang L. X. Liu L. H. Zhao C. P. Zheng Y. L., 2009 Association mapping of agronomic traits on chromosome 2A of wheat. Genetica 137: 67–75.

    Not in our library10.1007/s10709-009-9351-5

91. 91.

    Yu J. M. Pressoir G. Briggs W. H. Bi I. V. Yamasaki M., 2006 A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat. Genet. 38: 203–208.

    Not in our library10.1038/ng1702

92. 92.

    Zhang G. Karns R. Sun G. Indugula S. R. Cheng H., 2012 Finding missing heritability in less significant Loci and allelic heterogeneity: genetic variation in human height. PLoS ONE 7: e51211.

    Not in our library10.1371/journal.pone.0051211

93. 93.

    Zhang Z. W. Ersoz E. Lai C. Q. Todhunter R. J. Tiwari H. K., 2010 Mixed linear model approach adapted for genome-wide association studies. Nat. Genet. 42: 355–360.

    Not in our library10.1038/ng.546

94. 94.

    Zhao K. Tung C. W. Eizenga G. C. Wright M. H. Ali M. L., 2011 Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat. Commun. 2: 467.

    Not in our library10.1038/ncomms1467

95. 95.

    Zuk O. Schaffner S. F. Samocha K. Do R. Hechter E., 2014 Searching for missing heritability: designing rare variant association studies. Proc. Natl. Acad. Sci. USA 111: E455–E464.

    Not in our library10.1073/pnas.1322563111

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