Genomic analysis of 6,000-year-old cultivated grain illuminates the domestication history of barley (original) (raw)

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Acknowledgements

We gratefully acknowledge B. Schäfer for providing photographs of barley spikes and A. Fiebig for sequence data submission. This work was supported by a grant of the Israel Science Foundation (1179/13) to E.W., funding from the Endowed Chair in Molecular Genetics Applied to Crop Improvement at the University of Minnesota and the Triticeae Coordinated Agricultural Project, USDA-NIFA 2011-68002-30029 to G.J.M., and core funding of IPK Gatersleben to N.S. and M.M. R.W., J.R. and I.K.D. were supported by Research Programme funding from the Scottish government and the University of Dundee (R.W.). N.M. and U.D. acknowledge a grant from the Irene Levi Sela CARE Foundation.

Author information

Author notes

1. Martin Mascher, Verena J Schuenemann & Benjamin Kilian
   Present address: Present address: Bayer CropScience, BCS Breeding and Trait Development, Zwijnaarde (Gent), Belgium.,
2. These authors contributed equally to this work.

Authors and Affiliations

1. Leibniz Institute of Plant Genetics and Crop Plant Research (IPK) Gatersleben, Seeland, Germany
   Martin Mascher, Axel Himmelbach, Mona Schreiber, Benjamin Kilian & Nils Stein
2. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
   Martin Mascher
3. Institute for Archaeological Sciences, University of Tübingen, Tübingen, Germany
   Verena J Schuenemann, Ella Reiter, Simone Riehl & Johannes Krause
4. Senckenberg Center for Human Evolution and Paleoenvironment, University of Tübingen, Tübingen, Germany
   Verena J Schuenemann, Simone Riehl & Johannes Krause
5. Institute of Archaeology, Hebrew University, Jerusalem, Israel
   Uri Davidovich
6. Laboratory of Archaeozoology, Zinman Institute of Archaeology, University of Haifa, Haifa, Israel
   Nimrod Marom
7. Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada
   Sariel Hübner
8. Department of Biotechnology, Tel Hai College, Upper Galilee, Israel
   Sariel Hübner
9. Institute of Evolution, University of Haifa, Haifa, Israel
   Abraham Korol & Tzion Fahima
10. Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel
    Abraham Korol & Tzion Fahima
11. Martin (Szusz) Department of Land of Israel Studies and Archaeology, Bar-Ilan University, Ramat-Gan, Israel
    Michal David & Ehud Weiss
12. Department of Biomolecular Engineering, University of California, Santa Cruz, Santa Cruz, California, USA.,
    Samuel H Vohr & Richard E Green
13. Cell and Molecular Sciences, James Hutton Institute, Invergowrie, Dundee, UK
    Ian K Dawson, Joanne Russell & Robbie Waugh
14. Department of Plant Biology, University of Minnesota, St. Paul, Minnesota, USA
    Gary J Muehlbauer
15. Department of Agronomy and Plant Genetics, University of Minnesota, St. Paul, Minnesota, USA
    Gary J Muehlbauer
16. Division of Plant Sciences, University of Dundee, Dundee, UK
    Robbie Waugh
17. Max Planck Institute for the Science of Human History, Jena, Germany
    Johannes Krause

Authors

1. Martin Mascher
2. Verena J Schuenemann
3. Uri Davidovich
4. Nimrod Marom
5. Axel Himmelbach
6. Sariel Hübner
7. Abraham Korol
8. Michal David
9. Ella Reiter
10. Simone Riehl
11. Mona Schreiber
12. Samuel H Vohr
13. Richard E Green
14. Ian K Dawson
15. Joanne Russell
16. Benjamin Kilian
17. Gary J Muehlbauer
18. Robbie Waugh
19. Tzion Fahima
20. Johannes Krause
21. Ehud Weiss
22. Nils Stein

Contributions

E.W., T.F., N.S. and J.K. conceived the study. E.W., T.F., N.S., J.K., V.J.S. and M.M. designed experiments. N.M., U.D., M.D., S.R. and E.W. performed excavations and archaeobotanical analyses. V.J.S., A.H. and E.R. performed the ancient DNA experiments. M.M., S.H., A.K., M.S., S.H.V. and R.E.G. analyzed data. J.R., M.M., I.K.D., B.K., G.J.M., N.S. and R.W. provided exome capture data. M.M., V.J.S., A.H., S.R., T.F., J.K., E.W. and N.S. wrote the manuscript with input from all co-authors. All authors read and approved the manuscript.

Corresponding authors

Correspondence toTzion Fahima, Johannes Krause, Ehud Weiss or Nils Stein.

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Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Plan of Yoram Cave—top plan and sections.

The arrow indicates the entrance to the cave and the human-made wall across it. Note the boulders in the northern room and the relatively horizontal surface in the southern room. Gray shaded borders indicate that the edge of the cave is cut into rock.

Supplementary Figure 2 Photographs from the excavation.

(a) Masada Southern Cave complex, with three caves located in the southeastern cliff of the Masada Horst. The dotted red line marks the easiest trail giving access to the caves. (b) The entrance of Yoram Cave, facing southeast, in an almost vertical cliff, some 4 m above the trail leading to the cave. (c) The south room during excavation of locus 3.

Supplementary Figure 3 Photographs of ancient barley grains used for DNA extraction.

Supplementary Figure 4 Length distribution of sequence fragments.

Supplementary Figure 7 Haplotype of Btr1, Btr2 and Vrs1.

The contigs of the Morex whole-genome sequencing assembly harboring these genes were identified by BLAST searches. Read depth in the deeply sequenced sample JK3014 is shown in black. Position on the respective whole-genome sequencing contig is indicated along the upper axis. Distance (in genomic sequence) from the start codon of each gene is shown along the bottom axis. Btr1 and Btr2 are single-exon genes. Gray bars indicate the positions of the three exons of Vrs1. The positions of SNPs are highlighted by vertical lines. The Morex allele is shown above and the JK3014 allele is shown below the lines. SNPs with a previously reported functional effect are shown in red. JK3014 carries a loss-of-function allele of Btr1, whereas Btr2 and Vrs1 have wild-type alleles. The coding sequences of Btr1 and Btr2 are identical to those in the haplotype of cv. Haruna Nijo as reported by Komatsuda et al. (NCBI GenBank accession KR813337.1). The sequence of Vrs1 matches the Vrs1.b2 allele as designated by Komatsuda et al.22.

Supplementary Figure 8 Relationship between genetic similarity and geographical distance.

(a–f) Scatterplots of genetic similarity and geographical distance between 91 extant wild barley accessions sampled across the Fertile Crescent and archaeological sample JK3014 found at Yoram Cave and sequenced to higher depth using all SNPs (a), a two-rowed cultivated landrace from Israel (b), a two-rowed cultivated landrace from Egypt (c), the ancient sample JK3014 found at Yoram Cave and sequenced to higher depth excluding transition SNPs (d), two-rowed cultivated landraces from Israel excluding transition SNPs (e) and two-rowed cultivated landraces from Egypt excluding transition SNPs (f). The geographical position attributed to each sample is as follows: 31.3141° N, 35.353° E for a and d, 31.7156° N, 35.1871° E for b and e, and 31.193° N, 29.904° E for c and f. Correlation coefficients and P values for the geographically proximate and distant subsets are indicated in blue and red, respectively.

Supplementary Figure 10 ADMIXTURE analysis with K = 5 for domesticated and wild samples.

Top, domesticated samples; bottom, wild samples. Colors in both panels correspond to the same ancestral populations. Sample names and countries of origin are indicated above and below the plots, respectively. Ancient samples are highlighted by blue borders.

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Mascher, M., Schuenemann, V., Davidovich, U. et al. Genomic analysis of 6,000-year-old cultivated grain illuminates the domestication history of barley.Nat Genet 48, 1089–1093 (2016). https://doi.org/10.1038/ng.3611

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• Received: 06 May 2016
• Accepted: 13 June 2016
• Published: 18 July 2016
• Issue date: September 2016
• DOI: https://doi.org/10.1038/ng.3611