Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity

Abstract

Most fruits in our daily diet are the products of domestication and breeding. Here we report a map of genome variation for a major fruit that encompasses 3.6 million variants, generated by deep resequencing of 115 cucumber lines sampled from 3,342 accessions worldwide. Comparative analysis suggests that fruit crops underwent narrower bottlenecks during domestication than grain crops. We identified 112 putative domestication sweeps; 1 of these regions contains a gene involved in the loss of bitterness in fruits, an essential domestication trait of cucumber. We also investigated the genomic basis of divergence among the cultivated populations and discovered a natural genetic variant in a β-carotene hydroxylase gene that could be used to breed cucumbers with enhanced nutritional value. The genomic history of cucumber evolution uncovered here provides the basis for future genomics-enabled breeding.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Cucumber populations.
Figure 2: Detection and functional annotation of domestication sweeps.
Figure 3: Population divergence and identification of a key mutation responsible for the accumulation of β-carotene in the fruit of the Xishuangbanna cucumbers.

Accession codes

Primary accessions

Sequence Read Archive

Referenced accessions

NCBI Reference Sequence

References

  1. Morrell, P.L., Buckler, E.S. & Ross-Ibarra, J. Crop genomics: advances and applications. Nat. Rev. Genet. 13, 85–96 (2011).

    Article  PubMed  Google Scholar 

  2. Chia, J.M. et al. Maize HapMap2 identifies extant variation from a genome in flux. Nat. Genet. 44, 803–807 (2012).

    Article  CAS  PubMed  Google Scholar 

  3. Huang, X. et al. A map of rice genome variation reveals the origin of cultivated rice. Nature 490, 497–501 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Huang, X. et al. Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat. Genet. 44, 32–39 (2012).

    Article  Google Scholar 

  5. Hufford, M.B. et al. Comparative population genomics of maize domestication and improvement. Nat. Genet. 44, 808–811 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Jiao, Y. et al. Genome-wide genetic changes during modern breeding of maize. Nat. Genet. 44, 812–815 (2012).

    Article  CAS  PubMed  Google Scholar 

  7. Lam, H.M. et al. Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat. Genet. 42, 1053–1059 (2010).

    Article  CAS  PubMed  Google Scholar 

  8. Xu, X. et al. Resequencing 50 accessions of cultivated and wild rice yields markers for identifying agronomically important genes. Nat. Biotechnol. 30, 105–111 (2012).

    Article  CAS  Google Scholar 

  9. Cao, J. et al. Whole-genome sequencing of multiple Arabidopsis thaliana populations. Nat. Genet. 43, 956–963 (2011).

    Article  CAS  PubMed  Google Scholar 

  10. Atwell, S. et al. Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465, 627–631 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sebastian, P., Schaefer, H., Telford, I.R. & Renner, S.S. Cucumber (Cucumis sativus) and melon (C. melo) have numerous wild relatives in Asia and Australia, and the sister species of melon is from Australia. Proc. Natl. Acad. Sci. USA 107, 14269–14273 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Lv, J. et al. Genetic diversity and population structure of cucumber (Cucumis sativus L.). PLoS ONE 7, e46919 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Huang, S. et al. The genome of the cucumber, Cucumis sativus L. Nat. Genet. 41, 1275–1281 (2009).

    Article  CAS  PubMed  Google Scholar 

  14. Li, Z. et al. RNA-Seq improves annotation of protein-coding genes in the cucumber genome. BMC Genomics 12, 540 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Li, X. et al. Construction of wild cucumber substitution lines. Acta Horticulturae Sinica 38, 886–892 (2011).

    CAS  Google Scholar 

  16. Ren, Y. et al. An integrated genetic and cytogenetic map of the cucumber genome. PLoS ONE 4, e5795 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Qi, C., Yuan, Z. & Li, Y. A new type of cucumber—Cucumis sativus L. var. Xishuangbannanesis. Acta Horticulturae Sinica 10, 259–264 (1983).

    Google Scholar 

  18. Tajima, F. Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460 (1983).

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Doebley, J.F., Gaut, B.S. & Smith, B.D. The molecular genetics of crop domestication. Cell 127, 1309–1321 (2006).

    Article  CAS  PubMed  Google Scholar 

  20. Tang, H., Sezen, U. & Paterson, A.H. Domestication and plant genomes. Curr. Opin. Plant Biol. 13, 160–166 (2010).

    Article  CAS  PubMed  Google Scholar 

  21. Gross, B.L. & Olsen, K.M. Genetic perspectives on crop domestication. Trends Plant Sci. 15, 529–537 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Gutenkunst, R.N., Hernandez, R.D., Williamson, S.H. & Bustamante, C.D. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 5, e1000695 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Ross-Ibarra, J., Tenaillon, M. & Gaut, B.S. Historical divergence and gene flow in the genus Zea. Genetics 181, 1399–1413 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Caicedo, A.L. et al. Genome-wide patterns of nucleotide polymorphism in domesticated rice. PLoS Genet. 3, 1745–1756 (2007).

    Article  CAS  PubMed  Google Scholar 

  25. Konishi, S. et al. An SNP caused loss of seed shattering during rice domestication. Science 312, 1392–1396 (2006).

    Article  CAS  PubMed  Google Scholar 

  26. Li, C., Zhou, A. & Sang, T. Rice domestication by reducing shattering. Science 311, 1936–1939 (2006).

    Article  CAS  PubMed  Google Scholar 

  27. Wang, H. et al. The origin of the naked grains of maize. Nature 436, 714–719 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Horiguchi, G., Gonzalez, N., Beemster, G.T., Inze, D. & Tsukaya, H. Impact of segmental chromosomal duplications on leaf size in the grandifolia-D mutants of Arabidopsis thaliana. Plant J. 60, 122–133 (2009).

    Article  CAS  PubMed  Google Scholar 

  29. Balkema-Boomstra, A.G. et al. Role of cucurbitacin C in resistance to spider mite (Tetranychus urticae) in cucumber (Cucumis sativus L.). J. Chem. Ecol. 29, 225–235 (2003).

    Article  CAS  PubMed  Google Scholar 

  30. Barham, W.S. The inheritance of a bitter principle in cucumbers. Proc. Amer. Soc. Hort. Sci. 62, 441–442 (1953).

    Google Scholar 

  31. Kang, H. et al. Fine genetic mapping localizes cucumber scab resistance gene Ccu into an R gene cluster. Theor. Appl. Genet. 122, 795–803 (2011).

    Article  CAS  PubMed  Google Scholar 

  32. Bo, K. et al. Inheritance and mapping of the ore gene controlling the quantity of β-carotene in cucumber (Cucumis sativus L.) endocarp. Mol. Breed. 30, 335–344 (2012).

    Article  CAS  Google Scholar 

  33. Walter, M.H. & Strack, D. Carotenoids and their cleavage products: biosynthesis and functions. Nat. Prod. Rep. 28, 663–692 (2011).

    Article  CAS  PubMed  Google Scholar 

  34. Guo, S. et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat. Genet. 45, 51–58 (2013).

    Article  CAS  PubMed  Google Scholar 

  35. Murray, M.G. & Thompson, W.F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 8, 4321–4325 (1980).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Li, R. et al. SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967 (2009).

    Article  CAS  PubMed  Google Scholar 

  37. Yang, L. et al. Chromosome rearrangements during domestication of cucumber as revealed by high-density genetic mapping and draft genome assembly. Plant J. 71, 895–906 (2012).

    Article  CAS  PubMed  Google Scholar 

  38. Li, R. et al. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20, 265–272 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Li, R. et al. SNP detection for massively parallel whole-genome resequencing. Genome Res. 19, 1124–1132 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Xia, Q. et al. Complete resequencing of 40 genomes reveals domestication events and genes in silkworm (Bombyx). Science 326, 433–436 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lai, J. et al. Genome-wide patterns of genetic variation among elite maize inbred lines. Nat. Genet. 42, 1027–1030 (2010).

    Article  CAS  PubMed  Google Scholar 

  42. Birney, E., Clamp, M. & Durbin, R. GeneWise and Genomewise. Genome Res. 14, 988–995 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).

    Article  CAS  PubMed  Google Scholar 

  44. Falush, D., Stephens, M. & Pritchard, J.K. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Evanno, G., Regnaut, S. & Goudet, J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620 (2005).

    Article  CAS  PubMed  Google Scholar 

  46. Anderson, M.J. PCO: A FORTRAN Computer Program for Principal Coordinate Analysis (Department of Statistics, University of Auckland, Auckland, New Zealand, 2003).

  47. Barrett, J.C., Fry, B., Maller, J. & Daly, M.J. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263–265 (2005).

    CAS  PubMed  Google Scholar 

  48. Xu, Z., Kaplan, N.L. & Taylor, J.A. TAGster: efficient selection of LD tag SNPs in single or multiple populations. Bioinformatics 23, 3254–3255 (2007).

    Article  CAS  PubMed  Google Scholar 

  49. Chen, H., Patterson, N. & Reich, D. Population differentiation as a test for selective sweeps. Genome Res. 20, 393–402 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. de Meeûs, T. & Goudet, J. A step-by-step tutorial to use HierFstat to analyse populations hierarchically structured at multiple levels. Infect. Genet. Evol. 7, 731–735 (2007).

    Article  PubMed  Google Scholar 

  51. Cunningham, F.X. Jr. & Gantt, E. A portfolio of plasmids for identification and analysis of carotenoid pathway enzymes: Adonis aestivalis as a case study. Photosynth. Res. 92, 245–259 (2007).

    Article  CAS  PubMed  Google Scholar 

  52. Tian, L. & DellaPenna, D. Characterization of a second carotenoid β-hydroxylase gene from Arabidopsis and its relationship to the LUT1 locus. Plant Mol. Biol. 47, 379–388 (2001).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank J. Ross-Ibarra (University of California, Davis) and J.-Y. Li (Chinese Academy of Agricultural Sciences (CAAS)) for critical comments, D. DellaPenna (Michigan State University) for assistance in β-carotene pathway analysis and the three anonymous referees for their constructive comments. We thank F. Cunningham (University of Maryland) for providing the pAC-BETA plasmid. This work was supported by funding from the National Program on Key Basic Research Projects in China (the 973 Program; 2012CB113900), the National Natural Science Foundation of China (NSFC; 31225025) the National High-Tech Research Development Program in China (the 863 Program; 2010AA10A108 and 2012AA100101), and other NSFC grants (31030057, 30972011, 31101550, 31071797, 31171961, 31272161 and 31322047), the Chinese Ministry of Agriculture (the 948 program; 2008-Z42), the Chinese Ministry of Finance (1251610601001) and CAAS (seed grant to S.H.).

Author information

Authors and Affiliations

Authors

Contributions

S.H. and Z.Z. conceived and designed the experiments. J.Q., D.S., H.M., X.G., S.W., Y.L., T.L., Y.S., X.Y., H.C., X.X., K.H., J.C. and L.T. performed the experiments. Z.Z., J.Q., X. Liu, B.X., X. Li, P.Z., J.Y., Y.D., Z.F., L.M., T.S., S.S.R., W.J.L., S.K. and S.H. analyzed the data. S.H., Z.Z., X. Liu and J.Q. wrote the manuscript. Z.F., T.S., S.S.R., W.J.L. and S.K. revised the manuscript.

Corresponding authors

Correspondence to Zhonghua Zhang or Sanwen Huang.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Note, Supplementary Tables 2, 3, 5, 6 and 14, and Supplementary Figures 1–14 (PDF 4631 kb)

Supplementary Table 1

Summary of the sampled core collection (XLS 63 kb)

Supplementary Table 4

Presence and absence variation (PAV) genes identified in the core collection of 115 cucumber accessions (XLS 144 kb)

Supplementary Table 7

The SNP loci chosen for validation by PCR and Sanger sequencing (XLS 57 kb)

Supplementary Table 8

Putative regions identified to be under domestication sweeps (XLS 74 kb)

Supplementary Table 9

Genes within the putative regions identified to be under domestication sweeps (XLS 541 kb)

Supplementary Table 10

Summary of the genes present within Bt region (XLS 79 kb)

Supplementary Table 11

Highly differentiated regions across the cultivated groups (XLS 58 kb)

Supplementary Table 12

Genes located in the highly differentiated regions (XLS 1100 kb)

Supplementary Table 13

Genes containing nonsynonymous SNPs of significantly high FST values (XLS 443 kb)

Supplementary Dataset

Supplementary dataset for Supplementary Figures 1–5 and 7–10 (XLSX 6505 kb)

Source data

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Qi, J., Liu, X., Shen, D. et al. A genomic variation map provides insights into the genetic basis of cucumber domestication and diversity. Nat Genet 45, 1510–1515 (2013). https://doi.org/10.1038/ng.2801

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ng.2801

This article is cited by

Search

Quick links

Nature Briefing: Translational Research

Sign up for the Nature Briefing: Translational Research newsletter — top stories in biotechnology, drug discovery and pharma.

Get what matters in translational research, free to your inbox weekly. Sign up for Nature Briefing: Translational Research