The Genomic Signature of Crop-Wild Introgression in Maize

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The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize-mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

Vyšlo v časopise: The Genomic Signature of Crop-Wild Introgression in Maize. PLoS Genet 9(5): e32767. doi:10.1371/journal.pgen.1003477
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003477

Souhrn

Zdroje

1. StebbinsGL (1959) The role of hybridization in evolution. P Am Philos Soc 103: 231–251.

2. AndersonE (1948) Hybridization of the habitat. Evolution 2: 1–9.

3. AndersonE, StebbinsGL (1954) Hybridization as an evolutionary stimulus. Evolution 8: 378–388.

4. ArnoldML (2004) Transfer and origin of adaptations through natural hybridization: Were Anderson and Stebbins right? Plant Cell 16: 562–570.

5. ArnoldML, MartinNH (2010) Hybrid fitness across time and habitats. Trends Ecol Evol 25: 530–536.

6. ArnoldML (2004) Natural hybridization and the evolution of domesticated, pest and disease organisms. Mol Ecol 13: 997–1007.

7. EllstrandNC, HerediaSM, Leak-GarciaJA, HeratyJM, BurgerJC, et al. (2010) Crops gone wild: evolution of weeds and invasives from domesticated ancestors. Evol Appl 3: 494–504.

8. GrantBR, GrantPR (1996) High survival of Darwin's finch hybrids: Effects of beak morphology and diets. Ecology 77: 500–509.

9. GrantPR, GrantBR (2010) Conspecific versus heterospecific gene exchange between populations of Darwin's finches. Philos T Roy Soc B 365: 1065–1076.

10. WhitneyKD, RandellRA, RiesebergLH (2006) Adaptive introgression of herbivore resistance traits in the weedy sunflower Helianthus annuus. Am Nat 167: 794–807.

11. WhitneyKD, RandellRA, RiesebergLH (2010) Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. New Phytol 187: 230–239.

12. HeiserCB (1951) Hybridization in the annual sunflowers - Helianthus-annuusXH-debilis var-cucumerifolius. Evolution 5: 42–51.

13. KimSC, RiesebergLH (1999) Genetic architecture of species differences in annual sunflowers: Implications for adaptive trait introgression. Genetics 153: 965–977.

14. KimM, CuiM-L, CubasP, GilliesA, LeeK, et al. (2008) Regulatory genes control a key morphological and ecological trait transferred between species. Science 322: 1116–1119.

15. DasmahapatraKK, WaltersJR, BriscoeAD, DaveyJW, WhibleyA, et al. (2012) Butterfly genome reveals promiscuous exchange of mimicry adaptations among species. Nature 487: 94–98.

16. Pardo-DiazC, SalazarC, BaxterSW, MerotC, Figueiredo-ReadyW, et al. (2012) Adaptive introgression across species boundaries in Heliconius butterflies. PLoS Genet 8: e1002752 doi:10.1371/journal.pgen.1002752.

17. DurandEY, PattersonN, ReichD, SlatkinM (2011) Testing for ancient admixture between closely related populations. Mol Biol Evol 28: 2239–2252.

18. GreenRE, KrauseJ, BriggsAW, MaricicT, StenzelU, et al. (2010) A draft sequence of the Neandertal genome. Science 328: 710–722.

19. HeZ, ZhaiW, WenH, TangT, WangY, et al. (2011) Two evolutionary histories in the genome of rice: the roles of domestication genes. PLoS Genet 7: e1002100 doi:10.1371/journal.pgen.1002100.

20. KulathinalRJ, StevisonLS, NoorMAF (2009) The genomics of speciation in Drosophila: diversity, divergence, and introgression estimated using low-coverage genome sequencing. PLoS Genet 5: e1000550 doi:10.1371/journal.pgen.1000550.

21. ReichD, GreenRE, KircherM, KrauseJ, PattersonN, et al. (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468: 1053–1060.

22. SunY, CorcoranP, MenkisA, WhittleCA, AnderssonSGE, et al. (2012) Large-scale introgression shapes the evolution of the mating-type chromosomes of the filamentous ascomycete Neurospora tetrasperma. PLoS Genet 8: e1002820 doi:10.1371/journal.pgen.1002820.

23. ArnaudJF, ViardF, DelescluseM, CuguenJ (2003) Evidence for gene flow via seed dispersal from crop to wild relatives in Beta vulgaris (Chenopodiaceae): consequences for the release of genetically modified crop species with weedy lineages. P Roy Soc Lond B Bio 270: 1565–1571.

24. Ellstrand NC (2003) Dangerous Liaisons? When Cultivated Plants Mate with Their Wild Relatives. Baltimore, Maryland: The Johns Hopkins University Press. 244 p.

25. GutierrezA, CantamuttoM, PovereneM (2011) Persistence of sunflower crop traits and fitness in Helianthus petiolaris populations. Plant Biol 13: 821–830.

26. MorrellPL, Williams-CoplinTD, LattuAL, BowersJE, ChandlerJM, et al. (2005) Crop-to-weed introgression has impacted allelic composition of johnsongrass populations with and without recent exposure to cultivated sorghum. Mol Ecol 14: 2143–2154.

27. XiaHB, WangW, XiaH, ZhaoW, LuBR (2011) Conspecific crop-weed introgression influences evolution of weedy rice (Oryza sativa f. spontanea) across a geographical range. PLoS ONE 6: e16189 doi:10.1371/journal.pone.0016189.

28. FujinoK, WuJ, SekiguchiH, ItoT, IzawaT, et al. (2010) Multiple introgression events surrounding the Hd1 flowering-time gene in cultivated rice, Oryza sativa L. Mol Genet Genomics 284: 137–146.

29. McNallyKL, ChildsKL, BohnertR, DavidsonRM, ZhaoK, et al. (2009) Genomewide SNP variation reveals relationships among landraces and modern varieties of rice. P Natl Acad Sci USA 106: 12273–12278.

30. ZhaoK, WrightM, KimballJ, EizengaG, McClungA, et al. (2010) Genomic Diversity and introgression in O. sativa reveal the impact of domestication and breeding on the rice genome. PLoS ONE 5: e10780 doi:10.1371/journal.pone.0010780.

31. CornilleA, GladieuxP, SmuldersMJM, Roldán-RuizI, LaurensF, et al. (2012) New insight into the history of domesticated apple: secondary contribution of the European wild apple to the genome of cultivated varieties. PLoS Genet 8: e1002703 doi:10.1371/journal.pgen.1002703.

32. LuoMC, YangZL, YouFM, KawaharaT, WainesJG, et al. (2007) The structure of wild and domesticated emmer wheat populations, gene flow between them, and the site of emmer domestication. Theor Appl Genet 114: 947–959.

33. MylesS, BoykoAR, OwensCL, BrownPJ, GrassiF, et al. (2011) Genetic structure and domestication history of the grape. P Natl Acad Sci USA 108: 3530–3535.

34. MatsuokaY, VigourouxY, GoodmanMM, SanchezGJ, BucklerE, et al. (2002) A single domestication for maize shown by multilocus microsatellite genotyping. P Natl Acad Sci USA 99: 6080–6084.

35. PipernoDR, RanereAJ, HolstI, IriarteJ, DickauR (2009) Starch grain and phytolith evidence for early ninth millennium BP maize from the Central Balsas River Valley, Mexico. P Natl Acad Sci USA 106: 5019–5024.

36. van HeerwaardenJ, DoebleyJ, BriggsWH, GlaubitzJC, GoodmanMM, et al. (2011) Genetic signals of origin, spread, and introgression in a large sample of maize landraces. P Natl Acad Sci USA 108: 1088–1092.

37. VigourouxY, GlaubitzJC, MatsuokaY, GoodmanMM, JesusSG, et al. (2008) Population structure and genetic diversity of New World maize races assessed by DNA microsatellites. Am J Bot 95: 1240–1253.

38. HuffordMB, Martinez-MeyerE, GautBS, EguiarteLE, TenaillonMI (2012) Past and present distributions of wild and domesticated Zea mays: a chance to revisit maize history. PLoS ONE 7: e47659 doi:10.1371/journal.pone.0047659.

39. Ross-IbarraJ, TenaillonM, GautBS (2009) Historical divergence and gene flow in the genus Zea. Genetics 181: 1397–1409.

40. Wilkes HG (1967) Teosinte: The Closest Relative of Maize. Cambridge, Massachusetts: The Bussey Institute of Harvard University. 159 p.

41. WilkesHG (1977) Hybridization of maize and teosinte, in Mexico and Guatemala and improvement of maize. Econ Bot 31: 254–293.

42. LauterN, GustusC, WesterberghA, DoebleyJ (2004) The inheritance and evolution of leaf pigmentation and pubescence in teosinte. Genetics 167: 1949–1959.

43. BarthakurN (1974) Temperature differences between two pigmented types of corn plants. Int J Biometeorol 18: 70–75.

44. CollinsGN (1921) Teosinte in Mexico - The closest wild relative of maize is teosinte - a forage plant hitherto known only as an annual. A perennial form discovered in southern Mexico should prove of value to the breeder. J Hered 12: 339–350.

45. DoebleyJF (1984) Maize introgression into teosinte - a reappraisal. Ann Mo Bot Gard 71: 1100–1113.

46. DoebleyJ (1990) Molecular evidence and the evolution of maize. Econ Bot 44: 6–27.

47. RodriguezJG, SanchezJJ, BaltazarB, De la CruzL, Santacruz-RuvalcabaF, et al. (2006) Characterization of floral morphology and synchrony among Zea species in Mexico. Maydica 51: 383–398.

48. EvansMMS, KermicleJL (2001) Teosinte crossing barrier1, a locus governing hybridization of teosinte with maize. Theor Appl Genet 103: 259–265.

49. KermicleJL, EvansMMS (2010) The Zea mays sexual compatibility gene ga2: naturally occurring alleles, their distribution, and role in reproductive isolation. J Hered 101: 737–749.

50. KermicleJL, TabaS, EvansMMS (2006) The gametophyte-1 locus and reproductive isolation among Zea mays subspecies. Maydica 51: 219–225.

51. BaltazarBM, Sanchez-GonzalezJD, de la Cruz-LariosL, SchoperJB (2005) Pollination between maize and teosinte: an important determinant of gene flow in Mexico. Theor Appl Genet 110: 519–526.

52. EllstrandNC, GarnerLC, HegdeS, GuadagnuoloR, BlancasL (2007) Spontaneous hybridization between maize and teosinte. J Hered 98: 183–187.

53. BartonNH (2001) The role of hybridization in evolution. Mol Ecol 10: 551–568.

54. MalletJ (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20: 229–237.

55. DoebleyJ, GoodmanMM, StuberCW (1987) Patterns of isozyme variation between maize and Mexican annual teosinte. Econ Bot 41: 234–246.

56. GallavottiA, ZhaoQ, KyozukaJ, MeeleyRB, RitterM, et al. (2004) The role of barren stalk1 in the architecture of maize. Nature 432: 630–635.

57. WarburtonML, WilkesG, TabaS, CharcossetA, MirC, et al. (2011) Gene flow among different teosinte taxa and into the domesticated maize gene pool. Genet Resour Crop Ev 58: 1243–1261.

58. FukunagaK, HillJ, VigourouxY, MatsuokaY, SanchezJ, et al. (2005) Genetic diversity and population structure of teosinte. Genetics 169: 2241–2254.

59. DelplanckeM, AlvarezN, EspindolaA, JolyH, BenoitL, et al. (2012) Gene flow among wild and domesticated almond species: insights from chloroplast and nuclear markers. Evol Appl 5: 317–329.

60. HuebnerS, GuentherT, FlavellA, FridmanE, GranerA, et al. (2012) Islands and streams: clusters and gene flow in wild barley populations from the Levant. Mol Ecol 21: 1115–1129.

61. LiZ, ZouJ, MaoK, LinK, LiH, et al. (2012) Population genetic evidence for complex evolutionary histories of four high altitude juniper species in the Qinghai-Tibetan plateau. Evolution 66: 831–845.

62. ScascitelliM, WhitneyKD, RandellRA, KingM, BuerkleCA, et al. (2010) Genome scan of hybridizing sunflowers from Texas (Helianthus annuus and H. debilis) reveals asymmetric patterns of introgression and small islands of genomic differentiation. Mol Ecol 19: 521–541.

63. BaackEJ, RiesebergLH (2007) A genomic view of introgression and hybrid speciation. Curr Opin Genet Dev 17: 513–518.

64. TwyfordAD, EnnosRA (2012) Next-generation hybridization and introgression. Heredity 108: 179–189.

65. ChiaJ-M, SongC, BradburyPJ, CostichD, de LeonN, et al. (2012) Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 44: 803–807.

66. GanalMW, DurstewitzG, PolleyA, BerardA, BucklerES, et al. (2011) 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 6: e28334 doi:10.1371/journal.pone.0028334.

67. ReichD, KumarasamyT, PattersonN, PriceAL, SinghL (2009) Reconstructing Indian population history. Nature 461: 489–494.

68. PriceAL, TandonA, PattersonN, BarnesKC, RafaelsN, et al. (2009) Sensitive detection of chromosomal segments of distinct ancestry in admixed populations. PLoS Genet 5: e1000519 doi:10.1371/journal.pgen.1000519.

69. FalushD, StephensM, PritchardJK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164: 1567–1587.

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

71. HuffordMB, XuX, van HeerwaardenJ, PyhäjärviT, ChiaJ-M, et al. (2012) Comparative population genomics of maize domestication and improvement. Nat Genet 808–811.

72. WhippleCJ, KebromTH, WeberAL, YangF, HallD, et al. (2011) grassy tillers1 promotes apical dominance in maize and responds to shade signals in the grasses. P Natl Acad Sci USA 108: E506–E512.

73. Wills DM, Whipple C, Takuno S, Kursel LE, Shannon LM, et al.. (2013) From many, one: Genetic control of prolificacy during maize domestication. arXiv:1303.0882v1. Available at: http://arxiv.org/abs/1303.0882. Accessed 25 March 2013.

74. DoebleyJ, StecA, HubbardL (1997) The evolution of apical dominance in maize. Nature 386: 485–488.

75. WangH, Nussbaum-WaglerT, LiBL, ZhaoQ, VigourouxY, et al. (2005) The origin of the naked grains of maize. Nature 436: 714–719.

76. WhittSR, WilsonLM, TenaillonMI, GautBS, BucklerES (2002) Genetic diversity and selection in the maize starch pathway. P Natl Acad Sci USA 99: 12959–12962.

77. CoopG, WitonskyD, Di RienzoA, PritchardJK (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics 185: 1411–1423.

78. Pyhäjärvi T, Hufford MB, Mezmouk S, Ross-Ibarra J (2012) Complex patterns of local adaptation in teosinte. arXiv:1208.0634v1. Available at: http://arxiv.org/abs/1208.0634. Accessed 28 February 2013.

79. MooseSP, LauterN, CarlsonSR (2004) The maize macrohairless1 locus specifically promotes leaf blade macrohair initiation and responds to factors regulating leaf identity. Genetics 166: 1451–1461.

80. CookJP, McMullenMD, HollandJB, TianF, BradburyP, et al. (2012) Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiol 158: 824–834.

81. Flint-GarciaSA, ThuilletAC, YuJM, PressoirG, RomeroSM, et al. (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44: 1054–1064.

82. GusevA, LoweJK, StoffelM, DalyMJ, AltshulerD, et al. (2009) Whole population, genome-wide mapping of hidden relatedness. Genome Res 19: 318–326.

83. Sanchez-VelasquezLR, EzcurraE, Martinez-RamosM, Alvarez-BuyllaE, LorenteR (2002) Population dynamics of Zea diploperennis, an endangered perennial herb: effect of slash and burn practice. J Ecol 90: 684–692.

84. FreitasFO, BendelG, AllabyRG, BrownTA (2003) DNA from primitive maize landraces and archaeological remains: implications for the domestication of maize and its expansion into South America. J Archaeol Sci 30: 901–908.

85. MolinaJ, SikoraM, GarudN, FlowersJM, RubinsteinS, et al. (2011) Molecular evidence for a single evolutionary origin of domesticated rice. P Natl Acad Sci USA 108: 8351–8356.

86. BadrA, MullerK, Schafer-PreglR, El RabeyH, EffgenS, et al. (2000) On the origin and domestication history of barley (Hordeum vulgare). Mol Biol Evol 17: 499–510.

87. MorrellPL, CleggMT (2007) Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent. P Natl Acad Sci USA 104: 3289–3294.

88. KwakM, KamiJA, GeptsP (2009) The putative Mesoamerican domestication center of Phaseolus vulgaris is located in the Lerma-Santiago Basin of Mexico. Crop Sci 49: 554–563.

89. HeunM, SchaferPreglR, KlawanD, CastagnaR, AccerbiM, et al. (1997) Site of einkorn wheat domestication identified by DNA fingerprinting. Science 278: 1312–1314.

90. CurratM, RuediM, PetitRJ, ExcoffierL (2008) The hidden side of invasions: Massive introgression by local genes. Evolution 62: 1908–1920.

91. ExcoffierL, FollM, PetitRJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol S 40: 481–501.

92. GavriletsS (1997) Hybrid zones with Dobzhansky-type epistatic selection. Evolution 51: 1027–1035.

93. Saghai-MaroofMA, SolimanKM, JorgensenRA, AllardRW (1984) Ribosomal DNA spacer-length polymorphisms in barley - Mendelian inheritance, chromosomal location, and population-dynamics. P Natl Acad Sci USA 81: 8014–8018.

94. R Development Core Team (2012) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

95. ThorntonK (2003) libsequence: a C++ class library for evolutionary genetic analysis. Bioinformatics 19: 2325–2327.

96. WeirBS, CockerhamCC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38: 1358–1370.

97. GoudetJ (2005) HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Mol Ecol Notes 5: 184–186.

98. LeeM, SharopovaN, BeavisWD, GrantD, KattM, et al. (2002) Expanding the genetic map of maize with the intermated B73×Mo17 (IBM) population. Plant Mol Biol 48: 453–461.

99. ScheetP, StephensM (2006) A fast and flexible statistical model for large-scale population genotype data: Applications to inferring missing genotypes and haplotypic phase. Am J Hum Genet 78: 629–644.