Multiregional origins of the domesticated tetraploid wheats

English version

Autoři: Hugo R. Oliveira ^aff001; Lauren Jacocks ^aff001; Beata I. Czajkowska ^aff001; Sandra L. Kennedy ^aff001; Terence A. Brown ^aff001
Působiště autorů: School of Earth and Environmental Sciences, Manchester Institute of Biotechnology, University of Manchester, Manchester, England, United Kingdom ^aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227148

Souhrn

We used genotyping-by-sequencing (GBS) to investigate the evolutionary history of domesticated tetraploid wheats. With a panel of 189 wild and domesticated wheats, we identified 1,172,469 single nucleotide polymorphisms (SNPs) with a read depth ≥3. Principal component analyses (PCAs) separated the Triticum turgidum and Triticum timopheevii accessions, as well as wild T. turgidum from the domesticated emmers and the naked wheats, showing that SNP typing by GBS is capable of providing robust information on the genetic relationships between wheat species and subspecies. The PCAs and a neighbour-joining analysis suggested that domesticated tetraploid wheats have closest affinity with wild emmers from the northern Fertile Crescent, consistent with the results of previous genetic studies on the origins of domesticated wheat. However, a more detailed examination of admixture and allele sharing between domesticates and different wild populations, along with genome-wide association studies (GWAS), showed that the domesticated tetraploid wheats have also received a substantial genetic input from wild emmers from the southern Levant. Taking account of archaeological evidence that tetraploid wheats were first cultivated in the southern Levant, we suggest that a pre-domesticated crop spread from this region to southeast Turkey and became mixed with a wild emmer population from the northern Fertile Crescent. Fixation of the domestication traits in this mixed population would account for the allele sharing and GWAS results that we report. We also propose that feralization of the component of the pre-domesticated population that did not acquire domestication traits has resulted in the modern wild population from southeast Turkey displaying features of both the domesticates and wild emmer from the southern Levant, and hence appearing to be the sole progenitor of domesticated tetraploids when the phylogenetic relationships are studied by methods that assume a treelike pattern of evolution.

Klíčová slova:

Cereal crops – Crop genetics – Domestic animals – Genome-wide association studies – Genomic libraries – Phylogenetic analysis – Tetraploidy – Wheat

Zdroje

1. Zohary D, Hopf M, Weiss E. Domestication of plants in the Old World, 4th ed. Oxford: Oxford University Press; 2012.

2. Laidò G, Mangini G, Taranto F, Gadaleta A, Blanco A, Cattivelli L, et al. Genetic diversity and population structure of tetraploid wheats (Triticum turgidum L.) estimated by SSR, DArT and pedigree data. PloS ONE. 2013; 8(6): e67280. doi: 10.1371/journal.pone.0067280 23826256

3. Oliveira HR, Hagenblad J, Leino MW, Leigh FJ, Lister DL, Penã-Chocarro L, et al. Wheat in the Mediterranean revisited–tetraploid wheat landraces assessed with elite bread wheat Single Nucleotide Polymorphism markers. BMC Genet. 2014; 15(1): 54.

4. Sahri A, Chentoufi L, Arbaoui M, Ardisson M, Belqadi L, Birouk A, et al. Towards a comprehensive characterization of durum wheat landraces in Moroccan traditional agrosystems: analysing genetic diversity in the light of geography, farmers’ taxonomy and tetraploid wheat domestication history. BMC Evol Biol. 2014; 14(1): 264.

5. El Baidouri M, Murat F, Veyssiere M, Molinier M, Flores R, Burlot L, et al. Reconciling the evolutionary origin of bread wheat (Triticum aestivum). New Phytol. 2017. 213: 1477–1486. doi: 10.1111/nph.14113 27551821

6. Food and Agriculture Organization of the United Nations (FAOSTAT). Data–crops. 2019. http://www.fao.org/faostat/en/#data/QC/

7. Harlan JR, Zohary D Distribution of wild wheats and barley. Science. 1966; 153: 1074–1080. doi: 10.1126/science.153.3740.1074 17737582

8. Nevo E. Evolution of wild emmer wheat and crop improvement. J Syst Evol. 2014; 52: 673–696.

9. Maan S. Cytoplasmic and cytogenetic relationships among tetraploid Triticum species. Euphytica. 1973; 22: 287–300.

10. Mori N, Kondo Y, Ishii T, Kawahara T, Valkoun J, Nakamura C. Genetic diversity and origin of timopheevi wheat inferred by chloroplast DNA fingerprinting. Breeding Sci. 2009; 59: 571–578.

11. Feldman M, Kislev ME. Domestication of emmer wheat and evolution of free-threshing tetraploid wheat. Israel J Plant Sci. 2007; 55: 207–221.

12. Özkan H, Willcox G, Graner A, Salamini F, Kilian B. Geographic distribution and domestication of wild emmer wheat (Triticum dicoccoides). Genet Resour Crop Evol. 2011; 58: 11–53.

13. Arranz-Otaegui A, Colledge S, Zapata L, Teira-Mayolini LC, Ibáñez JJ. Regional diversity on the timing for the initial appearance of cereal cultivation and domestication in southwest Asia. Proc Natl Acad Sci USA. 2016; 113: 14001–14006. doi: 10.1073/pnas.1612797113 27930348

14. Arranz-Otaegui A, Colledge S, Ibáñez JJ, Zapata L. Crop husbandry activities and wild plant gathering, use and consumption at the EPPNB Tell Qarassa North (south Syria). Veget Hist Archaeobot. 2016; 25: 629–645.

15. Fuller DQ, Willcox G, Allaby RG. Cultivation and domestication had multiple origins: arguments against the core area hypothesis for the origins of agriculture in the Near East. World Archaeol. 2011; 43: 628–652.

16. Weide A. On the Identification of domesticated emmer wheat, Triticum turgidum subsp. dicoccum (Poaceae), in the Aceramic Neolithic of the Fertile Crescent. Arch Inf. 2015; 38: 381–424.

17. Riehl S, Zeidi M, Conard NJ. Emergence of agriculture in the foothills of the Zagros Mountains of Iran. Science. 2013; 341: 65–67. doi: 10.1126/science.1236743 23828939

18. Weide A, Riehl S, Zeidi M, Conard NJ. A systematic review of wild grass exploitation in relation to emerging cereal cultivation throughout the Epipalaeolithic and aceramic Neolithic of the Fertile Crescent. PLoS ONE. 2018; 13: e0189811. doi: 10.1371/journal.pone.0189811 29293519

19. Antolín F, Jacomet S, Buxó R. The hard knock life: archaeobotanical data on farming practices during the Neolithic (5400–2300 cal BC) in the NE of the Iberian Peninsula. J Archaeol Sci. 2015; 61: 90–104.

20. Özkan H, Brandolini A, Schäfer-Pregl R, Salamini F. AFLP analysis of a collection of tetraploid wheats indicates the origin of emmer and hard wheat domestication in southeast Turkey. Mol Biol Evol. 2002; 19: 1797–1801. doi: 10.1093/oxfordjournals.molbev.a004002 12270906

21. Heun M, Schäfer-Pregl R, Klawan D, Castagna R, Accerbi M, Borghi B, et al. Site of einkorn wheat domestication identified by DNA fingerprinting. Science. 1997; 278: 1312–1314.

22. Mori N, Ishi T, Ishido T, Hirosawa S, Watatani H, et al. Origins of domesticated emmer and common wheat inferred from chloroplast DNA fingerprinting. In: Pogna NE, Romano M, Pogna EA, Galterio G, editors. Proceedings of the 10th International Wheat Genetics Symposium, Paestum, Italy. Rome: Instituto Sperimentale per la Cerealicoltura; 2003. pp. 25–28.

23. Ozkan H, Brandolini A, Pozzi C, Effgen S, Wunder J, Salamini F. A reconsideration of the domestication geography of tetraploid wheats. Theor Appl Genet. 2005; 110: 1052–1060. doi: 10.1007/s00122-005-1925-8 15714326

24. Luo M-C, Yang Z-L, You F, Kawahara T, Waines J, Dvorak J. The structure of wild and domesticated emmer wheat populations, gene flow between them, and the site of emmer domestication. Theor Appl Genet. 2007; 114: 947–959. doi: 10.1007/s00122-006-0474-0 17318496

25. Nave M, Azni R, Çakır E, Portnoy V, Sela H, Pourkheirandish M, et al. Wheat domestication in light of haplotype analyses of the Brittle rachis 1 genes (BTR1-A and BTR1-B). Plant Sci. 2019; 285: 193–199. doi: 10.1016/j.plantsci.2019.05.012 31203884

26. Civáň P, Ivaničová Z, Brown TA. Reticulated origin of domesticated emmer wheat supports a dynamic model for the emergence of agriculture in the Fertile Crescent. PLoS ONE. 2013; 8: e81955. doi: 10.1371/journal.pone.0081955 24312385

27. Allaby RG, Fuller DQ, Brown TA. The genetic expectations of a protracted model for the origins of domesticated crops. Proc Natl Acad Sci USA. 2008; 105: 13982–13986. doi: 10.1073/pnas.0803780105 18768818

28. Allaby RG, Brown TA, Fuller DQ. A simulation of the effect of inbreeding on crop domestication genetics with comments on the integration of archaeobotany and genetics. Veget Hist Archaeobot. 2010; 19: 151–158.

29. Poets AM, Fang Z, Clegg MT, Morrell PL. Barley landraces are characterized by geographically heterogeneous genomic origins. Genome Biol. 2015; 16: 173. doi: 10.1186/s13059-015-0712-3 26293830

30. Pankin A, Altmüller J, Becker C, von Korff M. Targeted resequencing reveals genomic signatures of barley domestication. New Phytol. 2018; 218: 1247–1259. doi: 10.1111/nph.15077 29528492

31. Civán P, Brown TA. Role of genetic introgression during the evolution of cultivated rice (Oryza sativa L.). BMC Evol. Biol. 2018; 18: 57. doi: 10.1186/s12862-018-1180-7 29688851

32. Kim C, Guo H, Kong W, Chandnani R, Shuang L-S, Paterson AH. Application of technology to a variety of crop breeding programs. Plant Sci. 2016; 242: 14–22. doi: 10.1016/j.plantsci.2015.04.016 26566821

33. Scheben A, Batley J, Edwards D. Genotyping-by-sequencing approaches to characterize crop genomes: choosing the right tool for the right application. Plant Biotech J. 2017; 15: 149–161.

34. Khoshbakht K. Esfahanian emmer (Triticum ispahanicum Heslot)–a case of an extinct on-farm crop. In: Buerkert A, Gebauer J, editors. Agrobiodiversity and genetic erosion: contributions in honor of Prof Dr Karl Hammer. Kassel: Kassel University Press; 2009. pp. 189–195.

35. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS ONE. 2011; 6: e19379. doi: 10.1371/journal.pone.0019379 21573248

36. Li H, Durbin R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 2009; 25: 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

37. Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, et al. TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS ONE. 2014; 9: e90346. doi: 10.1371/journal.pone.0090346 24587335

38. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011; 27: 2156–2158. doi: 10.1093/bioinformatics/btr330 21653522

39. 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

40. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Huber W, Liaw A, et al. gplots: various R programming tools for plotting data. 2019. https://rdrr.io/cran/gplots/

41. Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000; 155: 945–959. 10835412

42. ESRI. ArcGIS Desktop: Release 10. Redlands, CA: Environmental Systems Research Institute 2011

43. Bush WS, Moore JH. Genome-wide association studies. PLoS Comp. Biol. 2012; 8(12): e1002822.

44. Turner SD. qqman: an R package for visualizing GWAS results using Q-Q and manhattan plots. J Open Source Softw. 2018; 3(25): 731.

45. Mascher M, Wu S, Amand PS, Stein N, Poland J. Application of genotyping-by-sequencing on semiconductor sequencing platforms: a comparison of genetic and reference-based marker ordering in barley. PloS ONE. 2013; 8(10): e76925. doi: 10.1371/journal.pone.0076925 24098570

46. Allaby RB, Banerjee M, Brown TA. Evolution of the high molecular wheat glutenin loci of the A, B, D and G genomes of wheat. Genome. 1999; 42: 296–307. 10231962

47. Nei M, Li W-H. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA. 1979; 76: 5269–5273. doi: 10.1073/pnas.76.10.5269 291943

48. Tajima F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989; 123: 585–595. 2513255

49. Czajkowska BI. Oliveira HR, Brown TA. A discriminatory test for the wheat B and G genomes reveals misclassified accessions of Triticum timopheevii and Triticum turgidum. PLoS ONE. 2019; 14(4); e0215175. doi: 10.1371/journal.pone.0215175 30969996

50. Poyarkova H. Morphology, geography and infraspecific taxonomics of Triticum dicoccoides Körn: a retrospective of 80 years of research. Euphytica. 1988; 38: 11–23.

51. Badaeva ED, Keilwagen J, Knüpffer H, Waßermann L, Dedkova OS, Mitrofanova OP, et al. Chromosomal passports provide new insights into diffusion of emmer wheat. PloS ONE. 2015; 10(5): e0128556. doi: 10.1371/journal.pone.0128556 26024381

52. Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005; 14: 2611–2620. doi: 10.1111/j.1365-294X.2005.02553.x 15969739

53. Xu 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

54. Zhang X, Zhang J, He X, Wang Y, Ma X, Yin D. Genome-wide association study of major agronomic traits related to domestication in peanut. Front Plant Sci. 2017; 8: 1611. doi: 10.3389/fpls.2017.01611 29018458

55. Oladzad A, Porch T, Rosas JC, Moghaddam SM, Beaver J, Beebe SE, et al. Single and multi-trait GWAS identify genetic factors associated with production traits in common bean under abiotic stress environments. G3. 2019; 9: 1881–1892. doi: 10.1534/g3.119.400072 31167806

56. Clayton WD, Vorontsova MS, Harman KT, Williamson H. GrassBase—the online world grass flora. 2009. http://www.kew.org/data/grasses-db.html

57. Gornicki P, Zhu H, Wang J, Challa GS, Zhang Z, Gill BS, et al. The chloroplast view of the evolution of polyploid wheat. New Phytol. 2014; 204: 704–714. doi: 10.1111/nph.12931 25059383

58. Bhagyalakshmi K, Vinod KK, Kumar M, Arumugachamy S, Prabhakaran A, Raveendran TS. Interspecific hybrids from wild x cultivated Triticum crosses–a study on the cytological behaviour and molecular relations. J Crop Sci Biotechnol. 2008; 11: 257–262.

59. Wagenaar EB. Studies on the genome constitution of Triticum timopheevi ZHUK. II. The T. timopheevi complex and its origin. Evolution. 1966; 20: 150–164. doi: 10.1111/j.1558-5646.1966.tb03351.x 28563623

60. Gill BS, Friebe B. Cytogenetics, phylogeny and evolution of cultivated wheats. http://www.fao.org/3/y4011e/y4011e07.htm

61. Blumler MA. Introgression of durum into wild emmer and the agricultural origin question. In: Damania AB, Valkoun J, Willcox G, Qualset CO, editors. The origin of agriculture and crop domestication. Aleppo, Syria: ICARDA, IPGRI, FSAO and UC/GRCP; 1998. pp. 252–268.

62. Bushuk W, Kerber ER. The role of Triticum carthlicum in the origin of bread wheat based on gliadin electrophorograms. Can J Plant Sci. 1978; 58: 1019–1024.

63. Matsuoka Y. 2011. 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. doi: 10.1093/pcp/pcr018 21317146

64. Allaby RG, Brown TA. AFLP data and the origins of domesticated crops. Genome. 2003; 46: 448–453. doi: 10.1139/g03-025 12834061

65. Brown TA, Jones MK, Powell W, Allaby RG. The complex origins of domesticated crops in the Fertile Crescent. Trends Ecol Evol. 2009; 24; 103–109. doi: 10.1016/j.tree.2008.09.008 19100651

66. Purugganan MD, Fuller DQ. Archaeological data reveal slow rates of evolution during plant domestication. Evolution. 2011; 65: 171–183. doi: 10.1111/j.1558-5646.2010.01093.x 20666839

67. Brown TA. The role of humans in a protracted transition from hunting-gathering to plant domestication in the Fertile Crescent. Front Plant Sci. 2018; 9: 1287. doi: 10.3389/fpls.2018.01287 30245699

Multiregional origins of the domesticated tetraploid wheats

Souhrn

Klíčová slova:

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