The genetic architecture of the maize progenitor, teosinte, and how it was altered during maize domestication

English version

Autoři: Qiuyue Chen ^aff001; Luis Fernando Samayoa ^aff002; Chin Jian Yang ^aff001; Peter J. Bradbury ^aff003; Bode A. Olukolu ^aff004; Michael A. Neumeyer ^aff001; Maria Cinta Romay ^aff005; Qi Sun ^aff005; Anne Lorant ^aff006; Edward S. Buckler ^aff003; Jeffrey Ross-Ibarra ^aff006; James B. Holland ^aff002; John F. Doebley ^aff001
Působiště autorů: Laboratory of Genetics, University of Wisconsin–Madison, Madison, Wisconsin, United States of America ^aff001; Department of Crop Science, North Carolina State University, Raleigh, North Carolina, United States of America ^aff002; US Department of Agriculture–Agricultural Research Service, Cornell University, Ithaca, New York, United States of America ^aff003; Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, Tennessee, United States of America ^aff004; Genomic Diversity Facility, Cornell University, Ithaca, New York, United States of America ^aff005; Department of Evolution and Ecology, University of California, Davis, California, United States of America ^aff006; US Department of Agriculture–Agricultural Research Service Plant Science Research Unit, North Carolina State University, Raleigh, North Carolina, United States of America ^aff007
Vyšlo v časopise: The genetic architecture of the maize progenitor, teosinte, and how it was altered during maize domestication. PLoS Genet 16(5): e32767. doi:10.1371/journal.pgen.1008791
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008791

Souhrn

The genetics of domestication has been extensively studied ever since the rediscovery of Mendel’s law of inheritance and much has been learned about the genetic control of trait differences between crops and their ancestors. Here, we ask how domestication has altered genetic architecture by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. We observed a strongly reduced number of QTL for domestication traits in maize relative to teosinte, which is consistent with the previously reported depletion of additive variance by selection during domestication. We also observed more dominance in maize than teosinte, likely a consequence of selective removal of additive variants. We observed that large effect QTL have low minor allele frequency (MAF) in both maize and teosinte. Regions of the genome that are strongly differentiated between teosinte and maize (high F_ST) explain less quantitative variation in maize than teosinte, suggesting that, in these regions, allelic variants were brought to (or near) fixation during domestication. We also observed that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of the additive variance in both teosinte and maize is “missing” in the sense that it cannot be ascribed to detectable QTL and only 25% of variance maps to specific QTL. This latter result suggests that morphological evolution during domestication is largely attributable to very large numbers of QTL of very small effect.

Klíčová slova:

Crop genetics – Domestic animals – Heredity – Maize – Natural selection – Plant genomics – Population genetics – Quantitative trait loci

Zdroje

1. Darwin C. On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. H. Milford; Oxford University Press; 1859.

2. Burger JC, Chapman MA, Burke JM. Molecular insights into the evolution of crop plants. Am J Bot. 2008; 95 : 113–122. doi: 10.3732/ajb.95.2.113 21632337

3. Doebley JF, Gaut BS, Smith BD. The molecular genetics of crop domestication. Cell. 2006; 127 : 1309–1321. doi: 10.1016/j.cell.2006.12.006 17190597

4. Gross BL, Olsen KM. Genetic perspectives on crop domestication. Trends Plant Sci. 2010; 15 : 529–537. doi: 10.1016/j.tplants.2010.05.008 20541451

5. Meyer RS, Purugganan MD. Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet. 2013; 14 : 840–852. doi: 10.1038/nrg3605 24240513

6. Olsen KM, Wendel JF. A bountiful harvest: genomic insights into crop domestication phenotypes. Ann Rev Plant Biol. 2013; 64 : 47–70.

7. Swinnen G, Goossens A, Pauwels L. Lessons from domestication: targeting cis-regulatory elements for crop improvement. Trends Plant Sci. 2016; 21 : 506–515. doi: 10.1016/j.tplants.2016.01.014 26876195

8. Yang CJ, Samayoa LF, Bradbury PJ, Olukolu BA, Xue W, York AM, et al. The genetic architecture of teosinte catalyzed and constrained maize domestication. Proc Natl Acad Sci USA. 2019; 116 : 5643–5652. doi: 10.1073/pnas.1820997116 30842282

9. Matsuoka Y, Vigouroux Y, Goodman MM, Sanchez J, Buckler E, Doebley J. A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA. 2002; 99 : 6080–6084. doi: 10.1073/pnas.052125199 11983901

10. Piperno DR, Ranere AJ, Holst I, Iriarte J, Dickau R. Starch grain and phytolith evidence for early ninth millennium B.P. maize from the Central Balsas River Valley, Mexico. Proc Natl Acad Sci USA. 2009; 106 : 5019–5024. doi: 10.1073/pnas.0812525106 19307570

11. Walsh B, Lynch M. Evolution and Selection of Quantitative Traits. Oxford University Press; 2018.

12. Jiao Y, Peluso P, Shi J, Liang T, Stitzer MC, Wang B, et al. Improved maize reference genome with single-molecule technologies. Nature. 2017; 546 : 524. doi: 10.1038/nature22971 28605751

13. Ou S, Liu J, Chougule KM, Fungtammasan A, Seetharam A, Stein J, et al. Effect of sequence depth and length in long-read assembly of the maize inbred NC358. BioRxiv [Preprint]. 2019 bioRxiv 858365 [posted 2019 Nov 29; revised 2019 Dec 3; cited 2020 Feb 10]: [24 p.]. Available from: https://www.biorxiv.org/content/10.1101/858365v2 https://doi.org/10.1101/858365

14. Springer NM, Anderson SN, Andorf CM, Ahern KR, Bai F, Barad O, et al. The maize W22 genome provides a foundation for functional genomics and transposon biology. Nat Genet. 2018; 50 : 1282. doi: 10.1038/s41588-018-0158-0 30061736

15. Sun S, Zhou Y, Chen J, Shi J, Zhao HM, Zhao HN, et al. Extensive intraspecific gene order and gene structural variations between Mo17 and other maize genomes. Nat Genet. 2018; 50 : 1289. doi: 10.1038/s41588-018-0182-0 30061735

16. Bukowski R, Guo X, Lu Y, Zou C, He B, Rong Z, et al. Construction of the third-generation Zea mays haplotype map. Gigascience. 2018; 7: gix134.

17. Chen Q, Yang CJ, York AM, Xue W, Daskalska LL, DeValk CA, et al. TeoNAM: a nested association mapping population for domestication and agronomic trait analysis in maize. Genetics. 2019; 213 : 1065–1078. doi: 10.1534/genetics.119.302594 31481533

18. Yu J, Holland JB, McMullen MD, Buckler ES. Genetic design and statistical power of nested association mapping in maize. Genetics. 2008; 178 : 539–551. doi: 10.1534/genetics.107.074245 18202393

19. Pyhäjärvi T, Hufford MB, Mezmouk S, Ross-Ibarra J. Complex patterns of local adaptation in teosinte. Genome Biol Evol. 2013; 5 : 1594–1609. doi: 10.1093/gbe/evt109 23902747

20. Schneeberger R, Tsiantis M, Freeling M, Langdale JA. The rough sheath2 gene negatively regulates homeobox gene expression during maize leaf development. Development. 1998; 125 : 2857–2865. 9655808

21. Becraft PW, Freeling M. Genetic analysis of Rough sheath1 developmental mutants of maize. Genetics. 1994; 136 : 295–311. 8138166

22. Weir BS, Cockerham CC. Estimating F‐statistics for the analysis of population structure. Evolution. 1984; 38 : 1358–1370. doi: 10.1111/j.1558-5646.1984.tb05657.x 28563791

23. Fang Z, Pyhäjärvi T, Weber AL, Dawe RK, Glaubitz JC, González JD, et al. Megabase-scale inversion polymorphism in the wild ancestor of maize. Genetics. 2012; 191 : 883–894. doi: 10.1534/genetics.112.138578 22542971

24. Buckler ES, Thornsberry JM, Kresovich S. Molecular diversity, structure and domestication of grasses. Genet Res. 2001; 77 : 213–218.

25. Hufford MB, Xu X, Van Heerwaarden J, Pyhäjärvi T, Chia JM, Cartwright RA, et al. Comparative population genomics of maize domestication and improvement. Nat Genet. 2012; 44 : 808. doi: 10.1038/ng.2309 22660546

26. Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, et al. The effects of artificial selection on the maize genome. Science. 2005; 308 : 1310–1314. doi: 10.1126/science.1107891 15919994

27. Dempewolf H, Baute G, Anderson J, Kilian B, Smith C, Guarino L. Past and future use of wild relatives in crop breeding. Crop Sci. 2017; 57 : 1070–1082.

28. Tanksley SD, McCouch SR. Seed banks and molecular maps: unlocking genetic potential from the wild. Science. 1997; 277 : 1063–1066. doi: 10.1126/science.277.5329.1063 9262467

29. Shannon LM, Chen Q, Doebley JF. A BC2S3 maize-teosinte RIL population for QTL mapping. Maize Genet Coop News Lett. 2019; 93.

30. Tian J, Wang C, Xia J, Wu L, Xu G, Wu W, et al. Teosinte ligule allele narrows plant architecture and enhances high-density maize yields. Science. 2019; 365 : 658–664. doi: 10.1126/science.aax5482 31416957

31. Desai MM, Fisher DS. Beneficial mutation–selection balance and the effect of linkage on positive selection. Genetics. 2007; 176 : 1759–1798. doi: 10.1534/genetics.106.067678 17483432

32. Perfeito L, Fernandes L, Mota C, Gordo I. Adaptive mutations in bacteria: high rate and small effects. Science. 2007; 317 : 813–815. doi: 10.1126/science.1142284 17690297

33. Kemper KE, Visscher PM, Goddard ME. Genetic architecture of body size in mammals. Genome Biol. 2012; 13 : 244. doi: 10.1186/gb-2012-13-4-244 22546202

34. Brown PJ, Upadyayula N, Mahone GS, Tian F, Bradbury PJ, Myles S, et al. Distinct genetic architectures for male and female inflorescence traits of maize. PLoS Genet. 2011; 7: e1002383. doi: 10.1371/journal.pgen.1002383 22125498

35. Troth A, Puzey JR, Kim RS, Willis JH, Kelly JK. Selective trade-offs maintain alleles underpinning complex trait variation in plants. Science. 2018; 361 : 475–478. doi: 10.1126/science.aat5760 30072534

36. Stetter MG, Thornton K, Ross-Ibarra J. Genetic architecture and selective sweeps after polygenic adaptation to distant trait optima. PLoS Genet. 2018; 14: e1007794. doi: 10.1371/journal.pgen.1007794 30452452

37. Avendaño López AN, de Jesús Sánchez González J, Ruíz Corral JA, De La Cruz Larios L, Santacruz-Ruvalcaba F, Sánchez Hernández CV, et al. Seed dormancy in Mexican teosinte. Crop Sci. 2011; 51 : 2056–2066.

38. Née G, Xiang Y, Soppe WJ. The release of dormancy, a wake-up call for seeds to germinate. Curr Opin Plant Biol. 2017; 35 : 8–14. doi: 10.1016/j.pbi.2016.09.002 27710774

39. Rendón-Anaya M, Herrera-Estrella A. The advantage of parallel selection of domestication genes to accelerate crop improvement. Genome Biol. 2018; 19 : 147. doi: 10.1186/s13059-018-1537-7 30266085

40. Hernández Xolocotzi E. Maize and man in the greater southwest. Econ Bot. 1985; 39 : 416–430.

41. Logan AL, Hastorf CA, Pearsall DM. “Let’s drink together”: early ceremonial use of maize in the Titicaca Basin. Lat Am Antiq. 2012; 23 : 235–258.

42. Louette D, Charrier A, Berthaud J. In situ conservation of maize in Mexico: genetic diversity and maize seed management in a traditional community. Econ Bot. 1997; 51 : 20–38.

43. Perales H, Brush SB, Qualset CO. Dynamic management of maize landraces in Central Mexico. Econ Bot. 2003; 57 : 21.

44. Pressoir G, Berthaud J. Patterns of population structure in maize landraces from the Central Valleys of Oaxaca in Mexico. Heredity. 2004; 92 : 88. doi: 10.1038/sj.hdy.6800387 14666127

45. Watterson GA. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 1975; 7 : 256–276. doi: 10.1016/0040-5809(75)90020-9 1145509

46. Clark RM, 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. doi: 10.1093/molbev/msi228 16079248

47. Yang N, Xu XW, Wang RR, Peng WL, Cai L, Song JM, et al. Contributions of Zea mays subspecies mexicana haplotypes to modern maize. Nat Commun. 2017; 8 : 1–10. doi: 10.1038/s41467-016-0009-6 28232747

48. Crnokrak P, Roff DA. Dominance variance: associations with selection and fitness. Heredity. 1995; 75 : 530.

49. Merilä J, Sheldon BC. Genetic architecture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity. 1999; 83 : 103–109. doi: 10.1046/j.1365-2540.1999.00585.x 10469197

50. Li D, Wang X, Zhang X, Chen Q, Xu G, Xu D, et al. The genetic architecture of leaf number and its genetic relationship to flowering time in maize. New Phytol. 2016; 210 : 256–268. doi: 10.1111/nph.13765 26593156

51. Shannon LM. The genetic architecture of maize domestication and range expansion. [PhD Dissertation] The University of Wisconsin-Madison; 2012.

52. Liang Y, Liu Q, Wang X, Huang C, Xu G, Hey S, et al. ZmMADS69 functions as a flowering activator through the ZmRap2.7-ZCN8 regulatory module and contributes to maize flowering time adaptation. New Phytol. 2019; 221 : 2335–2347. doi: 10.1111/nph.15512 30288760

53. Claeys H, Vi SL, Xu X, Satoh-Nagasawa N, Eveland AL, Goldshmidt A, et al. Control of meristem determinacy by trehalose 6-phosphate phosphatases is uncoupled from enzymatic activity. Nat Plants. 2019; 5 : 352. doi: 10.1038/s41477-019-0394-z 30936436

54. Young AI. Solving the missing heritability problem. PLoS Genet. 2019; 15: e1008222. doi: 10.1371/journal.pgen.1008222 31233496

55. Visscher PM. Sizing up human height variation. Nat Genet. 2008; 40 : 489. doi: 10.1038/ng0508-489 18443579

56. Allen HL, Estrada K, Lettre G, Berndt SI, Weedon MN, Rivadeneira F, et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature. 2010; 467 : 832. doi: 10.1038/nature09410 20881960

57. Wood AR, Esko T, Yang J, Vedantam S, Pers TH, Gustafsson S, et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet. 2014; 46 : 1173. doi: 10.1038/ng.3097 25282103

58. Eichler EE, Flint J, Gibson G, Kong A, Leal SM, Moore JH, et al. Missing heritability and strategies for finding the underlying causes of complex disease. Nat Rev Genet. 2010; 11 : 446. doi: 10.1038/nrg2809 20479774

59. Yang J, Bakshi A, Zhu Z, Hemani G, Vinkhuyzen AA, Lee SH, et al. Genetic variance estimation with imputed variants finds negligible missing heritability for human height and body mass index. Nat Genet. 2015; 47 : 1114. doi: 10.1038/ng.3390 26323059

60. Fisher RA. The correlation between relatives on the supposition of mendelian inheritance. Trans R Soc Edinb. 1918; 52 : 399–433.

61. Wainschtein P, Jain DP, Yengo L, Zheng Z, Cupples LA, Shadyab AH, et al. Recovery of trait heritability from whole genome sequence data. BioRxiv [Preprint]. 2019 bioRxiv 588020 [posted 2019 Mar 25; cited 2020 Feb 10]: [23 p.]. Available from: https://www.biorxiv.org/content/10.1101/588020v1 https://doi.org/10.1101/588020

62. Felsenstein J. The evolutionary advantage of recombination. Genetics. 1974; 78 : 737–756. 4448362

63. Hill WG, Robertson A. The effect of linkage on limits to artificial selection. Genet Res. 1966; 8 : 269–294. 5980116

64. Cutter AD, Payseur BA. Genomic signatures of selection at linked sites: unifying the disparity among species. Nat Rev Genet. 2013; 14 : 262. doi: 10.1038/nrg3425 23478346

65. Kliman RM, Hey J. Reduced natural selection associated with low recombination in Drosophila melanogaster. Mol Biol Evol. 1993; 10 : 1239–1258. doi: 10.1093/oxfordjournals.molbev.a040074 8277853

66. Xue S, Bradbury PJ, Casstevens T, Holland JB. Genetic architecture of domestication-related traits in maize. Genetics. 2016; 204 : 99–113. doi: 10.1534/genetics.116.191106 27412713

67. Clark RM, Linton E, Messing J, Doebley JF. Pattern of diversity in the genomic region near the maize domestication gene tb1. Proc Natl Acad Sci USA. 2004; 101 : 700–707. doi: 10.1073/pnas.2237049100 14701910

68. 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. doi: 10.1038/ng.942 21946354

69. Tian F, Stevens NM, Buckler ES. Tracking footprints of maize domestication and evidence for a massive selective sweep on chromosome 10. Proc Natl Acad Sci USA. 2009; 106 : 9979–9986. doi: 10.1073/pnas.0901122106 19528660

70. 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. doi: 10.1093/bioinformatics/btm308 17586829

71. Rodgers-Melnick E, Vera DL, Bass HW, Buckler ES. Open chromatin reveals the functional maize genome. Proc Natl Acad Sci USA. 2016; 113: E3177–E3184. doi: 10.1073/pnas.1525244113 27185945

72. Speed D, Balding DJ. MultiBLUP: improved SNP-based prediction for complex traits. Genome Res. 2014; 24 : 1550–1557. doi: 10.1101/gr.169375.113 24963154

73. Speed D, Hemani G, Johnson MR, Balding DJ. Improved heritability estimation from genome-wide SNPs. Am J Hum Genet. 2012; 91 : 1011–1021. doi: 10.1016/j.ajhg.2012.10.010 23217325

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