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Genetics and Consequences of Crop Domestication

Flint-Garcia SA
Journal of Agricultural and Food Chemistry
January 1, 2013

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Task Force #12

Journal of Agricultural and Food Chemistry. 2013;61(35):8267-8276

Abstract: Phenotypic variation has been manipulated by humans during crop domestication, which occurred primarily between 3000 and 10000 years ago in the various centers of origin around the world. The process of domestication has profound consequences on crops, where the domesticate has moderately reduced genetic diversity relative to the wild ancestor across the genome, and severely reduced diversity for genes targeted by domestication. The question that remains is whether reduction in genetic diversity has affected crop production today. A case study in maize (Zea mays) demonstrates the application of understanding relationships between genetic diversity and phenotypic diversity in the wild ancestor and the domesticate. As an outcrossing species, maize has tremendous genetic variation. The complementary combination of genome-wide association mapping (GWAS) approaches, large HapMap data sets, and germplasm resources is leading to important discoveries of the relationship between genetic diversity and phenotypic variation and the impact of domestication on trait variation.

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References

  1. Clark, R. M.; Tavaré, S.; Doebley, J. Estimating a nucleotide substitution rate for maize from polymorphism at a major domestication locus Mol. Biol. Evol. 2005, 22, 2304– 2312 LINK
  2. Styles, E. D.; Ceska, O. Flavonoid pigments in genetic strains of maize Phytochemistry 1972, 11, 3019– 3021 LINK
  3. Chopra, S.; Athma, P.; Peterson, T. Alleles of the maize P gene with distinct tissue specificities encode Myb-homologous proteins with C-terminal replacements Plant Cell 1996, 8, 1149– 1158 LINK
  4. Tollefson, J. J. Evaluating maize for resistance to Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae) Maydica 2007, 52, 311– 318 LINK
  5. Falconer, D. S.; Mackay, T. F. Introduction to Quantitative Genetics; Longman Group: Essex, UK, 1996.
  6. Mackay, T. F. The genetic architecture of quantitative traits Annu. Rev. Genet. 2001, 35, 303– 339 LINK
  7. Studer, A. J.; Doebley, J. F. Do large effect QTL fractionate? A case study at the maize domestication QTL teosinte branched1 Genetics 2011, 188, 673– 681 LINK
  8. Mackay, T. F. C. The genetic architecture of quantitative traits Annu. Rev. Genet. 2001, 35, 303– 339 LINK
  9. Holland, J. B. Genetic architecture of complex traits in plants Curr. Opin. Plant Biol. 2007, 10, 156– 161 LINK
  10. Tanksley, S. D.; Nelson, J. C. Advanced backcross QTL analysis: a method for the simultaneous discovery and transfer of valuable QTLs from unadapted germplasm into elite breeding lines Theor. Appl. Genet. 1996, 92, 191– 203 LINK
  11. Flint-Garcia, S. A.; Thornsberry, J. M.; Buckler, E. S. Structure of linkage disequilibrium in plants Annu. Rev. Plant Biol. 2003, 54, 357– 374 LINK
  12. Flint-Garcia, S. A.; Thuillet, A.-C.; Yu, J.; Pressoir, G.; Romero, S. M.; Mitchell, S. E.; Doebley, J.; Kresovich, S.; Goodman, M. M.; Buckler, E. S. Maize association population: a high-resolution platform for quantitative trait locus dissection Plant J. 2005, 44, 1054– 1064 LINK
  13. Bernardo, R. Breeding for Quantitative Traits; Stemma Press: Minneapolis, MN, 2002.
  14. Charlesworth, D.; Willis, J. H. The genetics of inbreeding depression. Nat. Rev. Genet. 2009, 10, 783– 796 LINK
  15. Birchler, J. A.; Yao, H.; Chudalayandi, S.; Vaiman, D.; Veitia, R. A. Heterosis Plant Cell Online 2010, 22, 2105– 2112 LINK
  16. Shull, G. H. A pure line method of corn breeding Am. Breeders Assoc. Rep. 1909, 5, 51– 59
  17. Sleper, D. A.; Poehlman, J. M. Breeding Field Crops; Wiley: New York, 2006.
  18. Fehr, W. R. Principles of Cultivar Development; McGraw-Hill: New York, 1987.
  19. Allard, R. W. Principles of Plant Breeding; Wiley: New York, 1999.
  20. Doebley, J. F.; Gaut, B. S.; Smith, B. D. The molecular genetics of crop domestication Cell 2006, 127, 1309– 1321 LINK
  21. Donald, C. M. The breeding of crop ideotypes Euphytica 1968, 17, 385– 403 LINK
  22. Tanksley, S. D.; McCouch, S. R. Seed banks and molecular maps: unlocking genetic potential from the wild Science 1997, 277, 1063– 1066 LINK
  23. Paran, I.; van der Knaap, E. Genetic and molecular regulation of fruit and plant domestication traits in tomato and pepper J. Exp. Bot. 2007, 58, 3841– 3852 LINK
  24. Rodríguez, G. R.; Muños, S.; Anderson, C.; Sim, S.-C.; Michel, A.; Causse, M.; Gardener, B. B. M.; Francis, D.; van der Knaap, E. Distribution of SUN, OVATE, LC, and FAS in the tomato germplasm and the relationship to fruit shape diversity Plant Physiol. 2011, 156, 275– 285 LINK
  25. Goodman, M. M.; Brown, W. L. Races of corn. In Corn and Corn Improvement, 3rd ed.; Agronomy No. 18; Sprague, G. F.; Dudley, J. W., Eds.; ASA-CSSA-SSSA: Madison, WI, 1988; pp 33– 79.
  26. Troyer, A. F. Background of U.S. hybrid corn Crop Sci. 1999, 39, 601– 626 LINK
  27. Vavilov, N. I. Studies on the origin of cultivated plants. Bull. Appl. Bot. 1926, 16.
  28. Rosenthal, J. P.; Dirzo, R. Effects of life history, domestication and agronomic selection on plant defence against insects: evidence from maizes and wild relatives Evol. Ecol. 1997, 11, 337– 355 LINK
  29. Panthee, D. R.; Chen, F. Genomics of fungal disease resistance in tomato Curr. Genomics 2010, 11, 30– 39 LINK
  30. Lenne, J. M.; Wood, D. Plant disease and the use of wild germplasm Annu. Rev. Phytopathol. 1991, 29, 35– 63 LINK
  31. Harlan, J. Genetic resources in wild relatives of crops Crop Sci. 1976, 16, 329– 333 LINK
  32. Hoisington, D.; Khairallah, M.; Reeves, T.; Ribaut, J.-M.; Skovmand, B.; Suketoshi, T.; Warburton, M. Plant genetic resources: what can they contribute toward increased crop productivity? Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 5937– 5943 LINK
  33. Moeller, D. A.; Tiffin, P. Geographic variation in adaptation at the molecular level: a case study of plant immunity genes Evolution 2008, 62, 3069– 3081 LINK
  34. Darwin, C. The Origin of Species by Means of Natural Selection; J. Murray: London, UK, 1859.
  35. Darwin, C. The Variation of Plants and Animals under Domestication; J. Murray: London, UK, 1868.
  36. Tenaillon, M. I.; U’Ren, J.; Tenaillon, O.; Gaut, B. S. Selection versus demography: a multilocus investigation of the domestication process in maize Mol. Biol. Evol. 2004, 21, 1214– 1225 LINK
  37. Innan, H.; Kim, Y. Pattern of polymorphism after strong artificial selection in a domestication event Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 10667– 10672 LINK
  38. Paterson, A. H.; Lin, Y.-R.; Li, Z.; Schertz, K. F.; Doebley, J. F.; Pinson, S. R. M.; Liu, S.-C.; Stansel, J. W.; Irvine, J. E. Convergent domestication of cereal crops by independent mutations at corresponding genetic loci Science 1995, 269, 1714– 1718 LINK
  39. Morrell, P. L.; Clegg, M. T. Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 3289– 3294 LINK
  40. Purugganan, M. D.; Fuller, D. Q. The nature of selection during plant domestication Nature 2009, 457, 843– 848 LINK
  41. Komatsuda, T.; Pourkheirandish, M.; He, C.; Azhaguvel, P.; Kanamori, H.; Perovic, D.; Stein, N.; Graner, A.; Wicker, T.; Tagiri, A.; Lundqvist, U.; Fujimura, T.; Matsuoka, M.; Matsumoto, T.; Yano, M. Six-rowed barley originated from a mutation in a homeodomain-leucine zipper I-class homeobox gene Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 1424– 1429 LINK
  42. Taketa, S.; Amano, S.; Tsujino, Y.; Sato, T.; Saisho, D.; Kakeda, K.; Nomura, M.; Suzuki, T.; Matsumoto, T.; Sato, K.; Kanamori, H.; Kawasaki, S.; Takeda, K. Barley grain with adhering hulls is controlled by an ERF family transcription factor gene regulating a lipid biosynthesis pathway Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 4062– 4067 LINK
  43. Sang, T. Genes and mutations underlying domestication transitions in grasses Plant Physiol. 2009, 149, 63– 70 LINK
  44. Matsuoka, Y. Evolution of polyploid triticum wheats under cultivation: the role of domestication, natural hybridization and allopolyploid speciation in their diversification Plant Cell Physiol. 2011, 52, 750– 764 LINK
  45. Harlan, J. R.; de Wet, M. J.; Price, E. G. Comparative evolution of cereals Evolution 1973, 27, 311– 325 LINK
  46. Simons, K. J.; Fellers, J. P.; Trick, H. N.; Zhang, Z.; Tai, Y.-S.; Gill, B. S.; Faris, J. D. Molecular characterization of the major wheat domestication gene Q Genetics 2006, 172, 547– 555 LINK
  47. Peng, J.; Ronin, Y.; Fahima, T.; Röder, M. S.; Li, Y.; Nevo, E.; Korol, A. Domestication quantitative trait loci in Triticum dicoccoides, the progenitor of wheat Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 2489– 2494 LINK
  48. Maccaferri, M.; Sanguineti, M. C.; Noli, E.; Tuberosa, R. Population structure and long-range linkage disequilibrium in a durum wheat elite collection Mol. Breed. 2005, 15, 271– 290 LINK
  49. Crossa, J.; Burgueño, J.; Dreisigacker, S.; Vargas, M.; Herrera-Foessel, S. A.; Lillemo, M.; Singh, R. P.; Trethowan, R.; Warburton, M.; Franco, J.; Reynolds, M.; Crouch, J. H.; Ortiz, R. Association analysis of historical bread wheat germplasm using additive genetic covariance of relatives and population structure Genetics 2007, 177, 1889– 1913 LINK
  50. Hillel, J.; Feldman, M. W.; Simchen, G. Mating systems and population structure in two closely related species of the wheat group I. Variation between and within populations Heredity 1973, 30, 141– 167 LINK
  51. Caicedo, A. L.; Williamson, S. H.; Hernandez, R. D.; Boyko, A.; Fledel-Alon, A.; York, T. L.; Polato, N. R.; Olsen, K. M.; Nielsen, R.; McCouch, S. R.; Bustamante, C. D.; Purugganan, M. D. Genome-wide patterns of nucleotide polymorphism in domesticated rice PLoS Genet. 2007, 3, e163 LINK
  52. Oka, H.-I.; Morishima, H. Phylogenetic differentiation of cultivated rice, XXIII. Potentiality of wild progenitors to evolve the indica and japonica types of rice cultivars Euphytica 1982, 31, 41– 50 LINK
  53. Molina, J.; Sikora, M.; Garud, N.; Flowers, J. M.; Rubinstein, S.; Reynolds, A.; Huang, P.; Jackson, S.; Schaal, B. A.; Bustamante, C. D.; Boyko, A. R.; Purugganan, M. D. Molecular evidence for a single evolutionary origin of domesticated rice Proc. Natl. Acad. Sci. U.S.A. 2011, 108, 8351– 8356 LINK
  54. Li, C.; Zhou, A.; Sang, T.Rice domestication by reducing shattering Science 2006, 311, 1936– 1939 LINK
  55. Sugimoto, K.; Takeuchi, Y.; Ebana, K.; Miyao, A.; Hirochika, H.; Hara, N.; Ishiyama, K.; Kobayashi, M.; Ban, Y.; Hattori, T.; Yano, M. Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 5792– 5797 LINK
  56. Ashikari, M.; Sakakibara, H.; Lin, S.; Yamamoto, T.; Takashi, T.; Nishimura, A.; Angeles, E. R.; Qian, Q.; Kitano, H.; Matsuoka, M. Cytokinin oxidase regulates rice grain production Science 2005, 309, 741– 745 LINK
  57. Kovach, M. J.; Sweeney, M. T.; McCouch, S. R. New insights into the history of rice domestication Trends Genet. 2007, 23, 578– 587 LINK
  58. Hymowitz, T.; Kaizuma, N. Soybean seed protein electrophoresis profiles from 15 Asian countries or regions: hypotheses on paths of dissemination of soybeans from China Econ. Bot. 1981, 35, 10– 23 LINK
  59. Xu, D.; Abe, J.; Gai, J.; Shimamoto, Y. Diversity of chloroplast DNA SSRs in wild and cultivated soybeans: evidence for multiple origins of cultivated soybean Theor. Appl. Genet. 2002, 105, 645– 653 LINK
  60. Zhao, T. J.; Gai, J. Y. The origin and evolution of cultivated soybeans Glycine max (L.) Merr. Sci. Agric. Sinica 2004, 37, 954– 962
  61. Guo, J.; Wang, Y.; Song, C.; Zhou, J.; Qiu, L.; Huang, H.; Wang, Y. A single origin and moderate bottleneck during domestication of soybean (Glycine max): implications from microsatellites and nucleotide sequences Ann. Bot. 2010, 106, 505– 514 LINK
  62. Hyten, D. L.; Song, Q.; Zhu, Y.; Choi, I.-Y.; Nelson, R. L.; Costa, J. M.; Specht, J. E.; Shoemaker, R. C.; Cregan, P. B. Impacts of genetic bottlenecks on soybean genome diversity Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 16666– 16671 LINK
  63. Stupar, R. M. Into the wild: the soybean genome meets its undomesticated relative Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 21947– 21948 LINK
  64. Broich, S.; Palmer, R. A cluster analysis of wild and domesticated soybean phenotypes Euphytica 1980, 29, 23– 32 LINK
  65. Liu, B.; Fujita, T.; Yan, Z.-H.; Sakamoto, S.; Xu, D.; Abe, J. QTL mapping of domestication-related traits in soybean (Glycine max) Ann. Bot. 2007, 100, 1027– 1038 LINK
  66. Liu, B.; Watanabe, S.; Uchiyama, T.; Kong, F.; Kanazawa, A.; Xia, Z.; Nagamatsu, A.; Arai, M.; Yamada, T.; Kitamura, K.; Masuta, C.; Harada, K.; Abe, J. The soybean stem growth habit gene Dt1 is an ortholog of Arabidopsis TERMINAL FLOWER1 Plant Physiol. 2010, 153, 198– 210 LINK
  67. Tian, Z.; Wang, X.; Lee, R.; Li, Y.; Specht, J. E.; Nelson, R. L.; McClean, P. E.; Qiu, L.; Ma, J. Artificial selection for determinate growth habit in soybean Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 8563– 8568 LINK
  68. Peralta, I. E.; Spooner, D. M. History, origin and early cultivation of tomato (Solanaceae). In Genetic Improvement of Solanaceous Crops; Razdan, M. K.; Mattoo, A. K., Eds.; Science Publishers: Enfield, NH, 2007; Vol. 2, pp 1– 27.
  69. Blanca, J.; Cañizares, J.; Cordero, L.; Pascual, L.; Diez, M. J.; Nuez, F. Variation revealed by SNP genotyping and morphology provides insight into the origin of the tomato PLoS ONE 2012, 7, e48198 LINK
  70. Miller, J. C.; Tanksley, S. D. RFLP analysis of phylogenetic relationships and genetic variation in the genus Lycopersicon Theor. Appl. Genet. 1990, 80, 437– 448 LINK
  71. Doganlar, S.; Frary, A.; Daunay, M.-C.; Lester, R. N.; Tanksley, S. D. Conservation of gene function in the Solanaceae as revealed by comparative mapping of domestication traits in eggplant Genetics 2002, 161, 1713– 1726 LINK
  72. Zhang, N.; Brewer, M.; Knaap, E. Fine mapping of fw3.2 controlling fruit weight in tomato Theor. Appl. Genet. 2012, 125, 273– 284 LINK
  73. Gepts, P. Origin and evolution of common bean: past events and recent trends HortScience 1998, 33, 1124– 1130
  74. Kaplan, L.; Lynch, T. F. Phaseolus (Fabaceae) in archaeology: AMS radiocarbon dates and their significance for pre-Columbian agriculture Econ. Bot. 1999, 53, 261– 272 LINK
  75. Singh, S.; Gepts, P.; Debouck, D. Races of common bean (Phaseolus vulgaris, Fabaceae) Econ. Bot. 1991, 45, 379– 396 LINK
  76. Papa, R.; Bellucci, E.; Rossi, M.; Leonardi, S.; Rau, D.; Gepts, P.; Nanni, L.; Attene, G. Tagging the signatures of domestication in common bean (Phaseolus vulgaris) by means of pooled DNA samples Ann. Bot. 2007, 100, 1039– 1051 LINK
  77. Blair, M. W.; Soler, A.; Cortés, A. J. Diversification and population structure in common beans (Phaseolus vulgaris L.) PLoS ONE 2012, 7, e49488 LINK
  78. Smith, B. D. Origins of agriculture in eastern North America Science 1989, 246, 1566– 1571 LINK
  79. Burke, J. M.; Burger, J. C.; Chapman, M. A. Crop evolution: from genetics to genomics Curr. Opin. Genet. Dev. 2007, 17, 525– 532 LINK
  80. Burke, J. M.; Tang, S.; Knapp, S. J.; Rieseberg, L. H. Genetic analysis of sunflower domestication Genetics 2002, 161, 1257– 1267 LINK
  81. Chapman, M. A.; Burke, J. M. Evidence of selection on fatty acid biosynthetic genes during the evolution of cultivated sunflower Theor. Appl. Genet. 2012, 125, 897– 907 LINK
  82. Blackman, B. K.; Rasmussen, D. A.; Strasburg, J. L.; Raduski, A. R.; Burke, J. M.; Knapp, S. J.; Michaels, S. D.; Rieseberg, L. H. Contributions of flowering time genes to sunflower domestication and improvement Genetics 2011, 187, 271– 287 LINK
  83. USDA-NASS National Statistics for Corn; http://www.nass.usda.gov (accessed Oct 15, 2012).
  84. FAO Crops Primary Equivalent; http://faostat.fao.org.
  85. Matsuoka, Y.; Vigouroux, Y.; Goodman, M. M.; Sanchez, G. J.; Buckler, E.; Doebley, J. A single domestication for maize shown by multilocus microsatellite genotyping Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 6080– 6084 LINK
  86. Vigouroux, V.; Glaubitz, J. C.; Matsuoka, Y.; Goodman, M. M.; Sánchez, G, J.; Doebley, J. Population structure and genetic diversity of new world maize races assessed by DNA microsatellites Am. J. Bot. 2008, 95, 1240– 1253 LINK
  87. Schnable, P. S.; Ware, D.; Fulton, R. S.; Stein, J. C.; Wei, F.; Pasternak, S.; Liang, C.; Zhang, J.; Fulton, L.; Graves, T. A.; Minx, P.; Reily, A. D.; Courtney, L.; Kruchowski, S. S.; Tomlinson, C.; Strong, C.; Delehaunty, K.; Fronick, C.; Courtney, B.; Rock, S. M.; Belter, E.; Du, F.; Kim, K.; Abbott, R. M.; Cotton, M.; Levy, A.; Marchetto, P.; Ochoa, K.; Jackson, S. M.; Gillam, B.; Chen, W.; Yan, L.; Higginbotham, J.; Cardenas, M.; Waligorski, J.; Applebaum, E.; Phelps, L.; Falcone, J.; Kanchi, K.; Thane, T.; Scimone, A.; Thane, N.; Henke, J.; Wang, T.; Ruppert, J.; Shah, N.; Rotter, K.; Hodges, J.; Ingenthron, E.; Cordes, M.; Kohlberg, S.; Sgro, J.; Delgado, B.; Mead, K.; Chinwalla, A.; Leonard, S.; Crouse, K.; Collura, K.; Kudrna, D.; Currie, J.; He, R.; Angelova, A.; Rajasekar, S.; Mueller, T.; Lomeli, R.; Scara, G.; Ko, A.; Delaney, K.; Wissotski, M.; Lopez, G.; Campos, D.; Braidotti, M.; Ashley, E.; Golser, W.; Kim, H.; Lee, S.; Lin, J.; Dujmic, Z.; Kim, W.; Talag, J.; Zuccolo, A.; Fan, C.; Sebastian, A.; Kramer, M.; Spiegel, L.; Nascimento, L.; Zutavern, T.; Miller, B.; Ambroise, C.; Muller, S.; Spooner, W.; Narechania, A.; Ren, L.; Wei, S.; Kumari, S.; Faga, B.; Levy, M. J.; McMahan, L.; Van Buren, P.; Vaughn, M. W.; Ying, K.; Yeh, C.-T.; Emrich, S. J.; Jia, Y.; Kalyanaraman, A.; Hsia, A.-P.; Barbazuk, W. B.; Baucom, R. S.; Brutnell, T. P.; Carpita, N. C.; Chaparro, C.; Chia, J.-M.; Deragon, J.-M.; Estill, J. C.; Fu, Y.; Jeddeloh, J. A.; Han, Y.; Lee, H.; Li, P.; Lisch, D. R.; Liu, S.; Liu, Z.; Nagel, D. H.; McCann, M. C.; SanMiguel, P.; Myers, A. M.; Nettleton, D.; Nguyen, J.; Penning, B. W.; Ponnala, L.; Schneider, K. L.; Schwartz, D. C.; Sharma, A.; Soderlund, C.; Springer, N. M.; Sun, Q.; Wang, H.; Waterman, M.; Westerman, R.; Wolfgruber, T. K.; Yang, L.; Yu, Y.; Zhang, L.; Zhou, S.; Zhu, Q.; Bennetzen, J. L.; Dawe, R. K.; Jiang, J.; Jiang, N.; Presting, G. G.; Wessler, S. R.; Aluru, S.; Martienssen, R. A.; Clifton, S. W.; McCombie, W. R.; Wing, R. A.; Wilson, R. K. The B73 maize genome: complexity, diversity, and dynamics Science 2009, 326, 1112– 1115 LINK
  88. Paterson, A. H.; Bowers, J. E.; Chapman, B. A. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 9903– 9908 LINK
  89. Feschotte, C.; Jiang, N.; Wessler, S. R. Plant transposable elements: where genetics meets genomics Nat. Rev. Genet. 2002, 3, 329– 341 LINK
  90. ENCODE: An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489, 57– 74 LINK
  91. Tenaillon, M. I.; Sawkins, M. C.; Long, A. D.; Gaut, R. L.; Doebley, J. F.; Gaut, B. S. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.) Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 9161– 9166 LINK
  92. Liu, K.; Goodman, M. M.; Muse, S. V.; Smith, J. S.; Buckler, E. S.; Doebley, J. F. Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites Genetics 2003, 165, 2117– 2128 LINK
  93. Gore, M. A.; Chia, J.-M.; Elshire, R. J.; Sun, Q.; Ersoz, E. S.; Hurwitz, B. L.; Peiffer, J. A.; McMullen, M. D.; Grills, G. S.; Ross-Ibarra, J.; Ware, D. H.; Buckler, E. S. A first-generation haplotype map of maize Science 2009, 326, 1115– 1117 LINK
  94. Fu, H.; Dooner, H. K. Intraspecific violation of genetic colinearity and its implications in maize Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 9573– 9578 LINK
  95. 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 LINK
  96. Chia, J.-M.; Song, C.; Bradbury, P. J.; Costich, D.; de Leon, N.; Doebley, J.; Elshire, R. J.; Gaut, B.; Geller, L.; Glaubitz, J. C.; Gore, M.; Guill, K. E.; Holland, J.; Hufford, M. B.; Lai, J.; Li, M.; Liu, X.; Lu, Y.; McCombie, R.; Nelson, R.; Poland, J.; Prasanna, B. M.; Pyhajarvi, T.; Rong, T.; Sekhon, R. S.; Sun, Q.; Tenaillon, M. I.; Tian, F.; Wang, J.; Xu, X.; Zhang, Z.; Kaeppler, S. M.; Ross-Ibarra, J.; McMullen, M. D.; Buckler, E. S.; Zhang, G.; Xu, Y.; Ware, D. Maize HapMap2 identifies extant variation from a genome in flux Nat. Genet. 2012, 40, 803– 807 LINK
  97. Swanson-Wagner, R. A.; Eichten, S. R.; Kumari, S.; Tiffin, P.; Stein, J. C.; Ware, D.; Springer, N. M. Pervasive gene content variation and copy number variation in maize and its undomesticated progenitor Genome Res. 2010, 20, 1689– 1699 LINK
  98. Beadle, G. W. The ancestry of corn Sci. Am. 1980, 242, 112– 119 LINK
  99. Beadle, G. W. The mystery of maize Field Mus. Natl. Hist. Bull. 1972, 43, 2– 11
  100. Doebley, J.; Stec, A. Genetic analysis of the morphological differences between maize and teosinte Genetics 1991, 129, 285– 295 LINK
  101. Hubbard, L.; McSteen, P.; Doebley, J.; Hake, S. Expression patterns and mutant phenotype of teosinte branched1 correlate with growth suppression in maize and teosinte Genetics 2002, 162, 1927– 1935 LINK
  102. Wang, R. L.; Stec, A.; Hey, J.; Lukens, L.; Doebley, J. The limits of selection during maize domestication Nature 1999, 398, 236– 239 LINK
  103. Studer, A.; Zhao, Q.; Ross-Ibarra, J.; Doebley, J. Identification of a functional transposon insertion in the maize domestication gene tb1 Nat. Genet. 2011, 43, 1160– 1163 LINK
  104. Dorweiler, J.; Stec, A.; Kermicle, J.; Doebley, J. Teosinte glume architecture 1: a genetic locus controlling a key step in maize evolution Science 1993, 262, 233– 235 LINK
  105. Wang, H.; Nussbaum-Wagler, T.; Li, B.; Zhao, Q.; Vigouroux, Y.; Faller, M.; Bomblies, K.; Lukens, L.; Doebley, J. F. The origin of the naked grains of maize Nature 2005, 436, 714– 719 LINK
  106. Wright, S. I.; Vroh Bi, I.; Schroeder, S. G.; Yamasaki, M.; Doebley, J. F.; McMullen, M. D.; Gaut, B. S. The effects of artificial selection on the maize genome Science 2005, 308, 1310– 1314 LINK
  107. Hufford, M. B.; Xu, X.; van Heerwaarden, J.; Pyhajarvi, T.; Chia, J.-M.; Cartwright, R. A.; Elshire, R. J.; Glaubitz, J. C.; Guill, K. E.; Kaeppler, S. M.; Lai, J.; Morrell, P. L.; Shannon, L. M.; Song, C.; Springer, N. M.; Swanson-Wagner, R. A.; Tiffin, P.; Wang, J.; Zhang, G.; Doebley, J.; McMullen, M. D.; Ware, D.; Buckler, E. S.; Yang, S.; Ross-Ibarra, J. Comparative population genomics of maize domestication and improvement Nat. Genet. 2012, 44, 808– 811 LINK
  108. Remington, D. L.; Thornsberry, J. M.; Matsuoka, Y.; Wilson, L. M.; Whitt, S. R.; Doebley, J.; Kresovich, S.; Goodman, M. M.; Buckler, E. S. Structure of linkage disequilibrium and phenotypic associations in the maize genome Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 11479– 11484 LINK
  109. Thornsberry, J. M.; Goodman, M. M.; Doebley, J.; Kresovich, S.; Nielsen, D.; Buckler, E. S. Dwarf8 polymorphisms associate with variation in flowering time Nat. Genet. 2001, 28, 286– 289 LINK
  110. Hansey, C. N.; Johnson, J. M.; Sekhon, R. S.; Kaeppler, S. M.; de Leon, N. Genetic diversity of a maize association population with restricted phenology Crop Sci. 2011, 51, 704– 715 LINK
  111. Yang, X.; Yan, J.; Shah, T.; Warburton, M.; Li, Q.; Li, L.; Gao, Y.; Chai, Y.; Fu, Z.; Zhou, Y.; Xu, S.; Bai, G.; Meng, Y.; Zheng, Y.; Li, J. Genetic analysis and characterization of a new maize association mapping panel for quantitative trait loci dissection Theor. Appl. Genet. 2010, 121, 417– 431 LINK
  112. Andersen, J. R.; Schrag, T.; Melchinger, A. E.; Zein, I.; Lübberstedt, T. Validation of Dwarf8 polymorphisms associated with flowering time in elite European inbred lines of maize (Zea mays L.) Theor. Appl. Genet. 2005, 111, 206– 217 LINK
  113. Camus-Kulandaivelu, L.; Veyrieras, J. B.; Madur, D.; Combes, V.; Fourmann, M.; Barraud, S.; Dubreuil, P.; Gouesnard, B.; Manicacci, D.; Charcosset, A. Maize adaptation to temperate climate: relationship between population structure and polymorphism in the Dwarf8 gene Genetics 2006, 172, 2449– 2463 LINK
  114. Palaisa, K. A.; Morgante, M.; Williams, M.; Rafalski, A. Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci Plant Cell 2003, 15, 1795– 1806 LINK
  115. Yan, J.; Kandianis, C. B.; Harjes, C. E.; Bai, L.; Kim, E.-H.; Yang, X.; Skinner, D. J.; Fu, Z.; Mitchell, S.; Li, Q.; Fernandez, M. G. S.; Zaharieva, M.; Babu, R.; Fu, Y.; Palacios, N.; Li, J.; DellaPenna, D.; Brutnell, T.; Buckler, E. S.; Warburton, M. L.; Rocheford, T. Rare genetic variation at Zea mays crtRB1 increases β-carotene in maize grain Nat. Genet. 2010, 42, 322– 327 LINK
  116. Yan, J.; Warburton, M.; Crouch, J. Association mapping for enhancing maize (Zea mays L.) genetic improvement Crop Sci. 2011, 51, 433– 449 LINK
  117. Cook, J. P.; McMullen, M. D.; Holland, J. B.; Tian, F.; Bradbury, P.; Ross-Ibarra, J.; Buckler, E. S.; Flint-Garcia, S. A. Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels Plant Physiol. 2012, 158, 824– 834 LINK
  118. Krill, A. M.; Kirst, M.; Kochian, L. V.; Buckler, E. S.; Hoekenga, O. A. Association and linkage analysis of aluminum tolerance genes in maize PLoS ONE 2010, 5, e9958 LINK
  119. Szalma, S. J.; Buckler, E. S.; Snook, M. E.; McMullen, M. D. Association analysis of flavonoid structural loci for maysin and chlorogenic acid synthesis in maize silks Theor. Appl. Genet. 2005, 110, 1324– 1333 LINK
  120. Wilson, L. M.; Whitt, S. R.; Ibáñez, A. M.; Rocheford, T. R.; Goodman, M. M.; Buckler, E. S. I. Dissection of maize kernel composition and starch production by candidate gene association Plant Cell 2004, 16, 2719– 2733 LINK
  121. Harjes, C. E.; Rocheford, T. R.; Bai, L.; Brutnell, T. P.; Kandianis, C. B.; Sowinski, S. G.; Stapleton, A. E.; Vallabhaneni, R.; Williams, M.; Wurtzel, E. T.; Yan, J.; Buckler, E. S. Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification Science 2008, 319, 330– 333 LINK
  122. Butron, A.; Chen, Y. C.; Rottinghaus, G. E.; McMullen, M. D. Genetic variation at bx1 controls DIMBOA content in maize Theor. Appl. Genet. 2010, 120, 721– 734 LINK
  123. Zhang, N.; Gur, A.; Gibon, Y.; Sulpice, R.; Flint-Garcia, S.; McMullen, M. D.; Stitt, M.; Buckler, E. S. Genetic analysis of central carbon metabolism unveils an amino acid substitution that alters maize NAD-dependent isocitrate dehydrogenase activity PLoS ONE 2010, 5, e9991 LINK
  124. Yu, J.; Holland, J. B.; McMullen, M. D.; Buckler, E. S. Genetic design and statistical power of nested association mapping in maize Genetics 2008, 178, 539– 551 LINK
  125. McMullen, M. D.; Kresovich, S.; Villeda, H. S.; 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, S. E.; Peterson, B.; Pressoir, G.; Romero, S.; Rosas, M. O.; Salvo, S.; Yates, H.; Hanson, M.; Jones, E.; Smith, S.; Glaubitz, J. C.; Goodman, M.; Ware, D.; Holland, J. B.; Buckler, E. S. Genetic properties of the maize nested association mapping population Science 2009, 325, 737– 740 LINK
  126. Buckler, E. S.; Holland, J. B.; Bradbury, P. J.; Acharya, C. B.; Brown, P. J.; Browne, C.; Ersoz, E.; Flint-Garcia, S.; Garcia, A.; Glaubitz, J. C.; Goodman, M. M.; Harjes, C.; Guill, K.; Kroon, D. E.; Larsson, S.; Lepak, N. K.; Li, H.; Mitchell, S. E.; Pressoir, G.; Peiffer, J. A.; Rosas, M. O.; Rocheford, T. R.; Romay, M. C.; Romero, S.; Salvo, S.; Villeda, H. S.; Sofia da Silva, H.; Sun, Q.; Tian, F.; Upadyayula, N.; Ware, D.; Yates, H.; Yu, J.; Zhang, Z.; Kresovich, S.; McMullen, M. D. The genetic architecture of maize flowering time Science 2009, 325, 714– 718 LINK
  127. Kump, K. L.; Bradbury, P. J.; Wisser, R. J.; Buckler, E. S.; Belcher, A. R.; Oropeza-Rosas, M. A.; Zwonitzer, J. C.; Kresovich, S.; McMullen, M. D.; Ware, D.; Balint-Kurti, P. J.; Holland, J. B. Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population Nat. Genet. 2011, 43, 163– 168 LINK
  128. Poland, J. A.; Bradbury, P. J.; Buckler, E. S.; Nelson, R. J. Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize Proc. Natl. Acad. Sci. 2011, 108, 6893– 6898 LINK
  129. Tian, F.; Bradbury, P. J.; Brown, P. J.; Hung, H.; Sun, Q.; Flint-Garcia, S.; Rocheford, T. R.; McMullen, M. D.; Holland, J. B.; Buckler, E. S. Genome-wide association study of leaf architecture in the maize nested association mapping population Nat. Genet. 2011, 43, 159– 162 LINK
  130. Brown, P. J.; Upadyayula, N.; Mahone, G. S.; Tian, F.; Bradbury, P. J.; Myles, S.; Holland, J. B.; Flint-Garcia, S.; McMullen, M. D.; Buckler, E. S.; Rocheford, T. R. Distinct genetic architectures for male and female inflorescence traits of maize PLoS Genet. 2011, 7, e1002383 LINK
  131. Zheng, P.; Allen, W. B.; Roesler, K.; Williams, M. E.; Zhang, S.; Li, J.; Glassman, K.; Ranch, J.; Nubel, D.; Solawetz, W.; Bhattramakki, D.; Llaca, V.; Deschamps, S.; Zhong, G.-Y.; Tarczynski, M. C.; Shen, B. A phenylalanine in DGAT is a key determinant of oil content and composition in maize Nat. Genet. 2008, 40, 367– 372 LINK
  132. Whitt, S. R.; Wilson, L. M.; Tenaillon, M. I.; Gaut, B. S.; Buckler, E. S. Genetic diversity and selection in the maize starch pathway Proc. Natl. Acad. Sci. U.S.A. 2002, 20, 12959– 12962 LINK
  133. Flint-Garcia, S. A.; Bodnar, A. L.; Scott, M. P. Wide variability in kernel composition, seed characteristics, and zein profiles among diverse maize inbreds, landraces, and teosinte Theor. Appl. Genet. 2009, 119, 1129– 1142 LINK
  134. Kruijt, M.; Brandwagt, B. F.; de Wit, P. J. G. M. Rearrangements in the Cf-9 disease resistance gene cluster of wild tomato have resulted in three genes that mediate Avr9 responsiveness Genetics 2004, 168, 1655– 1663 LINK
  135. Verlaan, M. G.; Hutton, S. F.; Ibrahem, R. M.; Kormelink, R.; Visser, R. G. F.; Scott, J. W.; Edwards, J. D.; Bai, Y. The tomato yellow leaf curl virus resistance genes Ty-1 and Ty-3 are allelic and code for DFDGD-Class RNA-Dependent RNA polymerases PLoS Genet. 2013, 9, e1003399 LINK
  136. Vidavski, F. S. Exploitation of resistance genes found in wild tomato species to produce resistant cultivars; pile up of resistant genes. In Tomato leaf Curl Virus Disease: Management, Molecular Biology, Breeding for Resistance; Czosnek, H., Ed.; Kluwer: Dordrecht, The Netherlands, 2007; pp 363– 372. LINK
  137. Meihls, L. N.; Higdon, M. L.; Siegfried, B. D.; Miller, N. J.; Sappington, T. W.; Ellersieck, M. R.; Spencer, T. A.; Hibbard, B. E. Increased survival of western corn rootworm on transgenic corn within three generations of on-plant greenhouse selection Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 19177– 19182 LINK
  138. Meihls, L. N.; Higdon, M. L.; Ellersieck, M.; Hibbard, B. E. Selection for resistance to mCry3A-expressing transgenic corn in western corn rootworm J. Econ. Entomol. 2011, 104, 1045– 1054 LINK
  139. Lefko, S. A.; Nowatzki, T. M.; Thompson, S. D.; Binning, R. R.; Pascual, M. A.; Peters, M. L.; Simbro, E. J.; Stanley, B. H. Characterizing laboratory colonies of western corn rootworm (Coleoptera: Chrysomelidae) selected for survival on maize containing event DAS-59122-7 J. Appl. Entomol. 2008, 132, 189– 204 LINK