Comprehensive genotyping of the USA national maize inbred seed bank

Genome Biology

Volumn 14, Issue 6, 2013, Pages

  Romay, Maria C ^a   Millard, Mark J ^b,c   Glaubitz, Jeffrey C ^a   Peiffer, Jason A ^d   Swarts, Kelly L ^a   Casstevens, Terry M ^a   Elshire, Robert J ^a   Acharya, Charlotte B ^a   Mitchell, Sharon E ^a   Flint Garcia, Sherry A ^b,e   McMullen, Michael D ^b,e   Holland, James B ^b,d   Buckler, Edward S ^a,b   Gardner, Candice A ^b,c  

^a Department of Molecular Biology and Genetics   (United States)

^b AGRICULTURAL RESEARCH SERVICE   (United States)

^c IOWA STATE UNIVERSITY   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

^e UNIVERSITY OF MISSOURI   (United States)

Author keywords

Diversity; Genotyping by sequencing; Germplasm; Maize; Public

Indexed keywords

ARTICLE; GENE CLUSTER; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC DISTANCE; GENETIC TRAIT; GENETIC VARIABILITY; GENOTYPE; GENOTYPING BY SEQUENCING; GERMPLASM; HIGH THROUGHPUT SEQUENCING; INBRED STRAIN; INHERITANCE; MAIZE; NONHUMAN; PLANT BREEDING; PLANT GENOME; SINGLE NUCLEOTIDE POLYMORPHISM; UNITED STATES; ALLELE; BREEDING; CHROMOSOME MAP; CLASSIFICATION; GENETIC MARKER; GENETICS; HEALTH CARE FACILITY; PHENOTYPE; PLANT SEED; QUANTITATIVE TRAIT;

ZEA MAYS;

GENETIC MARKER;

ALLELES; BIOLOGICAL SPECIMEN BANKS; BREEDING; CHROMOSOME MAPPING; GENETIC MARKERS; GENOME, PLANT; GENOTYPE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; LINKAGE DISEQUILIBRIUM; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT, HERITABLE; SEEDS; UNITED STATES; ZEA MAYS;

EID: 84878685948     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2013-14-6-r55     Document Type: Article

References (67)

1. FAOSTAT, http://faostat.fao.org
2. Fu H, Dooner HK. Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 2002, 99:9573-9578. 10.1073/pnas.132259199, 123182, 12060715.
3. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A. Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 2005, 37:997-1002. 10.1038/ng1615, 16056225.
4. Chia J-M, Song C, Bradbury PJ, Costich D, De Leon N, Doebley J, Elshire RJ, Gaut B, Geller L, Glaubitz JC, Gore M, Guill KE, Holland J, Hufford MB, Lai J, Li M, Liu X, Lu Y, McCombie R, Nelson R, Poland J, Prasanna BM, Pyhäjärvi T, Rong T, Sekhon RS, Sun Q, Tenaillon MI, Tian F, Wang J, Xu X, et al. Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 2012, 44:803-807. 10.1038/ng.2313, 22660545.
5. Shull GH. The composition of a field of maize. American Breeders Association Report 1908, 4:296-301.
6. East EM. Inbreeding in corn. Rep Conn Agric Exp Stn 1908, 1:419-428.
7. Liu K, Goodman M, Muse S, Smith JS, Buckler ES, Doebley J. Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites. Genetics 2003, 165:2117-2128. 1462894, 14704191.
8. Flint-Garcia S, Thuillet A-C, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES. Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 2005, 44:1054-1064. 10.1111/j.1365-313X.2005.02591.x, 16359397.
9. Yang X, Gao S, Xu S, Zhang Z, Prasanna BM, Li L, Li J, Yan J. Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol Breed 2010, 28:511-526.
10. Mezmouk S, Dubreuil P, Bosio M, Décousset L, Charcosset A, Praud S, Mangin B. Effect of population structure corrections on the results of association mapping tests in complex maize diversity panels. Theor Appl Genet 2011, 122:1149-1160. 10.1007/s00122-010-1519-y, 3057001, 21221527.
11. Yan J, Warburton M, Crouch J. Association mapping for enhancing maize (Zea mays L.) genetic improvement. Crop Sci 2011, 51:433-449.
12. Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, Flint-Garcia S, Rocheford TR, McMullen MD, Holland JB, Buckler ES. Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 2011, 43:159-162. 10.1038/ng.746, 21217756.
13. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE. A robust, simple Genotyping-by-Sequencing (GBS) approach for high diversity species. PLoS One 2011, 6:e19379. 10.1371/journal.pone.0019379, 3087801, 21573248.
14. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA, Minx P, Reily AD, Courtney L, Kruchowski SS, Tomlinson C, Strong C, Delehaunty K, Fronick C, Courtney B, Rock SM, Belter E, Du F, Kim K, Abbott RM, Cotton M, Levy A, Marchetto P, Ochoa K, Jackson SM, Gillam B, et al. The B73 maize genome: complexity, diversity, and dynamics. Science 2009, 326:1112-1115. 10.1126/science.1178534, 19965430.
15. Park J-H, Gail MH, Weinberg CR, Carroll RJ, Chung CC, Wang Z, Chanock SJ, Fraumeni JF, Chatterjee N. Distribution of allele frequencies and effect sizes and their interrelationships for common genetic susceptibility variants. Proc Natl Acad Sci USA 2011, 108:18026-18031. 10.1073/pnas.1114759108, 3207674, 22003128.
16. Yan J, Kandianis CB, Harjes CE, Bai L, Kim E-H, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, Fernandez MGS, Zaharieva M, Babu R, Fu Y, Palacios N, Li J, Dellapenna D, Brutnell T, Buckler ES, Warburton ML, Rocheford T. Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain. Nat Genet 2010, 42:322-327. 10.1038/ng.551, 20305664.
17. Gibson G. Rare and common variants: twenty arguments. Nat Rev Genet 2012, 13:135-145. 10.1038/nrg3118, 22251874.
18. McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, Sun Q, Flint-Garcia S, Thornsberry J, Acharya C, Bottoms C, Brown P, Browne C, Eller M, Guill K, Harjes C, Kroon D, Lepak N, Mitchell SE, Peterson B, Pressoir G, Romero S, Oropeza Rosas M, Salvo S, Yates H, Hanson M, Jones E, Smith S, Glaubitz JC, Goodman M, Ware D, et al. Genetic properties of the maize nested association mapping population. Science 2009, 325:737-740. 10.1126/science.1174320, 19661427.
19. Ganal MW, Durstewitz G, Polley A, Bérard A, Buckler ES, Charcosset A, Clarke JD, Graner E-M, Hansen M, Joets J, Le Paslier M-C, McMullen MD, Montalent P, Rose M, Schön C-C, Sun Q, Walter H, Martin OC, Falque M. A large maize (Zea mays L.) SNP genotyping array: development and germplasm genotyping, and genetic mapping to compare with the B73 reference genome. PLoS One 2011, 6:e28334. 10.1371/journal.pone.0028334, 3234264, 22174790.
20. Carena MJ, Hallauer AR, Miranda Filho J. Quantitative Genetics in Maize Breeding 2010, New York: Springer New York, 3.
21. Mikel MA, Dudley JW. Evolution of North American Dent Corn from Public to Proprietary Germplasm. Crop Sci 2006, 46:1193-1205.
22. Wright S. Evolution and the Genetics of Populations: Genetics and Biometric Foundations v. 4 (Variability within and Among Natural Populations) 1978, Chicago: University of Chicago Press.
23. Gore MA, Chia J-M, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES. A first-generation haplotype map of maize. Science 2009, 326:1115-1117. 10.1126/science.1177837, 19965431.
24. Lai J, Li R, Xu X, Jin W, Xu M, Zhao H, Xiang Z, Song W, Ying K, Zhang M, Jiao Y, Ni P, Zhang J, Li D, Guo X, Ye K, Jian M, Wang B, Zheng H, Liang H, Zhang X, Wang S, Chen S, Li J, Fu Y, Springer NM, Yang H, Wang J, Dai J, Schnable PS, et al. Genome-wide patterns of genetic variation among elite maize inbred lines. Nat Genet 2010, 42:1027-1030. 10.1038/ng.684, 20972441.
25. Hufford MB, Xu X, Van Heerwaarden J, Pyhäjärvi T, Chia J-M, Cartwright RA, Elshire RJ, Glaubitz JC, Guill KE, Kaeppler SM, Lai J, Morrell PL, Shannon LM, Song C, Springer NM, Swanson-Wagner RA, Tiffin P, Wang J, Zhang G, Doebley J, McMullen MD, Ware D, Buckler ES, Yang S, Ross-Ibarra J. Comparative population genomics of maize domestication and improvement. Nat Genet 2012, 44:808-811. 10.1038/ng.2309, 22660546.
26. Hung H-Y, Shannon LM, Tian F, Bradbury PJ, Chen C, Flint-Garcia SA, McMullen MD, Ware D, Buckler ES, Doebley JF, Holland JB. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci USA 2012, 109:E1913-E1921. 10.1073/pnas.1203189109, 3396540, 22711828.
27. Buckner B, Kelson TL, Robertson DS. Cloning of the y1 locus of maize, a gene involved in the biosynthesis of carotenoids. Plant Cell 1990, 2:867-876. 159937, 12354969.
28. Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES. Genetic diversity and selection in the maize starch pathway. Proc Natl Acad Sci USA 2002, 99:12959-12962. 10.1073/pnas.202476999, 130568, 12244216.
29. James MG, Robertson DS, Myers AM. Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 1995, 7:417-429. 160793, 7773016.
30. Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler KA, Meeley R, Ananiev E, Svitashev S, Bruggemann E, Li B, Hainey CF, Radovic S, Zaina G, Rafalski J, Tingey S V, Miao G, Phillips RL, Tuberosa R. Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA 2007, 104:11376-11381. 10.1073/pnas.0704145104, 2040906, 17595297.
31. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, Browne C, Ersoz E, Flint-Garcia S, Garcia A, Glaubitz JC, Goodman MM, Harjes C, Guill K, Kroon DE, Larsson SJ, Lepak NK, Li H, Mitchell SE, Pressoir G, Peiffer JA, Oropeza Rosas M, Rocheford TR, Romay MC, Romero S, Salvo S, Sanchez Villeda H, Da Silva HS, Sun Q, Tian F, Upadyayula N, et al. The genetic architecture of maize flowering time. Science 2009, 325:714-718. 10.1126/science.1174276, 19661422.
32. Muszynski MG, Dam T, Li B, Shirbroun DM, Hou Z, Bruggemann E, Archibald R, Ananiev E V, Danilevskaya ON. Delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiol 2006, 142:1523-1536. 10.1104/pp.106.088815, 1676038, 17071646.
33. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 2000, 290:344-347. 10.1126/science.290.5490.344, 11030654.
34. Sheehan MJ, Farmer PR, Brutnell TP. Structure and expression of maize phytochrome family homeologs. Genetics 2004, 167:1395-1405. 10.1534/genetics.103.026096, 1470959, 15280251.
35. Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES. Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet 2001, 28:286-289. 10.1038/90135, 11431702.
36. Tenaillon MI, U'Ren J, Tenaillon O, Gaut BS. Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 2004, 21:1214-1225. 10.1093/molbev/msh102, 15014173.
37. Larsson SJ, Lipka AE, Buckler ES. Lessons from Dwarf8 on the Strengths and Weaknesses of Structured Association Mapping. PLoS Genetics 2013, 9:e1003246. 10.1371/journal.pgen.1003246, 3578782, 23437002.
38. Morrell PL, Buckler ES, Ross-Ibarra J. Crop genomics: advances and applications. Nat Rev Genet 2011, 13:85-96.
39. Yan J, Shah T, Warburton ML, Buckler ES, McMullen MD, Crouch J. Genetic characterization and linkage disequilibrium estimation of a global maize collection using SNP markers. PLoS One 2009, 4:e8451. 10.1371/journal.pone.0008451, 2795174, 20041112.
40. Van Inghelandt D, Melchinger AE, Lebreton C, Stich B. Population structure and genetic diversity in a commercial maize breeding program assessed with SSR and SNP markers. Theor Appl Genet 2010, 120:1289-1299. 10.1007/s00122-009-1256-2, 2854351, 20063144.
41. Lu Y, Shah T, Hao Z, Taba S, Zhang S, Gao S, Liu J, Cao M, Wang J, Prakash AB, Rong T, Xu Y. Comparative SNP and haplotype analysis reveals a higher genetic diversity and rapider LD decay in tropical than temperate germplasm in maize. PLoS One 2011, 6:e24861. 10.1371/journal.pone.0024861, 3174237, 21949770.
42. Van Heerwaarden J, Hufford MB, Ross-Ibarra J. Historical genomics of North American maize. Proc Natl Acad Sci USA 2012, 109:12420-12425. 10.1073/pnas.1209275109, 3412004, 22802642.
43. Springer NM, Ying K, Fu Y, Ji T, Yeh C-T, Jia Y, Wu W, Richmond T, Kitzman J, Rosenbaum H, Iniguez AL, Barbazuk WB, Jeddeloh JA, Nettleton D, Schnable PS. Maize inbreds exhibit high levels of copy number variation (CNV) and presence/absence variation (PAV) in genome content. PLoS Genet 2009, 5:e1000734. 10.1371/journal.pgen.1000734, 2780416, 19956538.
44. Lu F, Lipka A, Elshire R, Glaubitz J, Cherney J, Casler M, Buckler E, Costich D. Switchgrass genomic diversity, ploidy and evolution: novel insights from a network-based SNP discovery protocol. PLoS Genet 2013, 9:e1003215. 10.1371/journal.pgen.1003215, 3547862, 23349638.
45. Clark AG, Hubisz MJ, Bustamante CD, Williamson SH, Nielsen R. Ascertainment bias in studies of human genome-wide polymorphism. Genome Res 2005, 15:1496-1502. 10.1101/gr.4107905, 1310637, 16251459.
46. Gravel S, Henn BM, Gutenkunst RN, Indap AR, Marth GT, Clark AG, Yu F, Gibbs RA, Bustamante CD, Altshuler DL, Durbin RM, Abecasis GR, Bentley DR, Chakravarti A, Collins FS, De La Vega FM, Donnelly P, Egholm M, Flicek P, Gabriel SB, Knoppers BM, Lander ES, Lehrach H, Mardis ER, McVean GA, Nickerson DA, Peltonen L, Schafer AJ, Sherry ST, Wang J, et al. Demographic history and rare allele sharing among human populations. Proc Natl Acad Sci USA 2011, 108:11983-11988. 10.1073/pnas.1019276108, 3142009, 21730125.
47. Reif JC, Hallauer AR, Melchinger AE. Heterosis and heterotic patterns in plants. Maydica 2005, 50:215-223.
48. Nelson PT, Coles ND, Holland JB, Bubeck DM, Smith S, Goodman MM. Molecular characterization of maize inbreds with expired U.S. plant variety protection. Crop Sci 2008, 48:1673-1686.
49. Mikel MA. Genetic composition of contemporary U.S. commercial dent corn germplasm. Crop Sci 2011, 51:592-599.
50. Goodman MM. Broadening the genetic diversity in maize breeding by use of exotic germplasm. The Genetics and Exploitation of Heterosis in Crops 1999, 139-148. Coors JG, Pandey S Madison: ASA, CSSA.
51. Salhuana W, Pollak L. Latin American Maize Project (LAMP) and Germplasm Enhancement of Maize (GEM) project: generating useful breeding germplasm 1. Maydica 2006, 51:339-355.
52. Van Inghelandt D, Reif JC, Dhillon BS, Flament P, Melchinger AE. Extent and genome-wide distribution of linkage disequilibrium in commercial maize germplasm. Theor Appl Genet 2011, 123:11-20. 10.1007/s00122-011-1562-3, 21404061.
53. Atwell S, Huang YS, Vilhjálmsson BJ, Willems G, Horton M, Li Y, Meng D, Platt A, Tarone AM, Hu TT, Jiang R, Muliyati NW, Zhang X, Amer MA, Baxter I, Brachi B, Chory J, Dean C, Debieu M, De Meaux J, Ecker JR, Faure N, Kniskern JM, Jones JDG, Michael T, Nemri A, Roux F, Salt DE, Tang C, Todesco M, et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 2010, 465:627-631. 10.1038/nature08800, 3023908, 20336072.
54. Zhao K, Tung C-W, Eizenga GC, Wright MH, Ali ML, Price AH, Norton GJ, Islam MR, Reynolds A, Mezey J, McClung AM, Bustamante CD, McCouch SR. Genome-wide association mapping reveals a rich genetic architecture of complex traits in Oryza sativa. Nat Commun 2011, 2:467. 3195253, 21915109.
55. Durand E, Bouchet S, Bertin P, Ressayre A, Jamin P, Charcosset A, Dillmann C, Tenaillon MI. Flowering time in maize: linkage and epistasis at a major effect locus. Genetics 2012, 190:1547-1562. 10.1534/genetics.111.136903, 3316663, 22298708.
56. Meng X, Muszynski MG, Danilevskaya ON. The FT-like ZCN8 Gene Functions as a Floral Activator and Is Involved in Photoperiod Sensitivity in Maize. The Plant cell 2011, 23:942-960. 10.1105/tpc.110.081406, 3082274, 21441432.
57. Hansey CN, Johnson JM, Sekhon RS, Kaeppler SM, De Leon N. Genetic diversity of a maize association population with restricted phenology. Crop Sci 2011, 51:704-715.
58. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 2007, 23:2633-2635. 10.1093/bioinformatics/btm308, 17586829.
59. Panzea, http://www.panzea.org
60. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, De Bakker PIW, Daly MJ, Sham PC. PLINK: a toolset for whole-genome association and population-based linkage analysis. Am J Hum Genet 2007, 81:559-575. 10.1086/519795, 1950838, 17701901.
61. Bastian M, Heymann S, Jacomy M. Gephi: an open source software for exploring and manipulating networks. AJS 2009, 2:361-362.
62. Venables WN, Ripley BD. Modern Applied Statistics with S 2002, New York: Springer, 4.
63. Weir BS, Cockerham CC. Estimating F-Statistics for the analysis of population structure. Evolution 1984, 38:1358-1370.
64. Gilmour AR, Gogel BJ, Cullis BR, Thompson R. ASReml User Guide Release 3.0 2009, VSN International Ltd.
65. Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z. GAPIT: Genome Association and Prediction Integrated Tool. Bioinformatics 2012, 28:2397-2399. 10.1093/bioinformatics/bts444, 22796960.
66. Zhang Z, Ersoz E, Lai C-Q, Todhunter RJ, Tiwari HK, Gore MA, Bradbury PJ, Yu J, Arnett DK, Ordovas JM, Buckler ES. Mixed linear model approach adapted for genome-wide association studies. Nat Genet 2010, 42:355-360. 10.1038/ng.546, 2931336, 20208535.
67. VanRaden P. Efficient methods to compute genomic predictions. J Dairy Sci 2008, 91:4414-4423. 10.3168/jds.2007-0980, 18946147.