Genomic analyses provide insights into the history of tomato breeding

Abstract

The histories of crop domestication and breeding are recorded in genomes. Although tomato is a model species for plant biology and breeding, the nature of human selection that altered its genome remains largely unknown. Here we report a comprehensive analysis of tomato evolution based on the genome sequences of 360 accessions. We provide evidence that domestication and improvement focused on two independent sets of quantitative trait loci (QTLs), resulting in modern tomato fruit 100 times larger than its ancestor. Furthermore, we discovered a major genomic signature for modern processing tomatoes, identified the causative variants that confer pink fruit color and precisely visualized the linkage drag associated with wild introgressions. This study outlines the accomplishments as well as the costs of historical selection and provides molecular insights toward further improvement.

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Figure 1: Genome-wide relationship and fruit morphology in cultivated tomato and its wild relatives.
Figure 2: Evolution of fruit mass during domestication and improvement.
Figure 3: A major genomic signature of modern processing tomatoes and three causative variants for pink fruit.
Figure 4: Introgressions and sweeps.

Accession codes

Primary accessions

Sequence Read Archive

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Acknowledgements

We thank J. Maloof (University of California, Davis) for providing tomato RNA sequencing data and L.A. Mueller and N. Menda (Cornell University) for setting up a genome browser of SNPs. This work was supported by funding from the National Program on Key Basic Research Projects in China (973 program; 2012CB113900 and 2011CB100600), the National Science Fund for Distinguished Young Scholars (31225025 to S.H.), the National HighTech Research Development Program in China (863 Program; 2012AA100101 and 2012AA100105), the National Natural Science Foundation of China (31272160, 31230064, 31272171 and 31171962), the Chinese Ministry of Finance (1251610601001), CAAS (an Agricultural Science and Technology Innovation Program grant to S.H.), the China Agriculture Research System (CARS-25-A-09 and CARS-25-A-15), the Special Fund for Agro-Scientific Research in the Public Interest of China (201303115), the Major Special Science and Technology Project during the Twelfth Five-Year Plan Period of Xinjiang (201230116-3) and the US National Science Foundation Plant Genome Program (IOS-0923312). This work was also supported by the Shenzhen municipal and Dapeng district governments.

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Contributions

S.H., Y.D., Z.Y. and Jingfu Li conceived and designed the research. T.L., G.Z., J.Z., X.X., Q.Y., Z. Zheng, Y.L., S.L., T.W. and Yuyang Zhang performed DNA sequencing and biological experiments. T.L., G.Z., Z. Zhang, K.L., Yancong Zhang, C.L., Y.X., X.W., Z.H., D.Z., Junming Li, G.X., C.Z., A.M., M.C., Z.F., J.J.G., R.T.C., A.W. and T.S. performed the data analysis. S.H., G.Z., T.L., J.Z., X.X., Q.Y. and Z. Zhang wrote the manuscript. Y.D., Z.Y., Jingfu Li, Z. Zhang, C.L., Y.X., A.M., M.C., Z.F., J.J.G., R.T.C., D.Z. and T.S. revised the manuscript.

Corresponding authors

Correspondence to Jingfu Li or Zhibiao Ye or Yongchen Du or Sanwen Huang.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Spectra of fruit weight for three tomato groups.

Supplementary Figure 2 Determination of ΔK using STRUCTURE.

ΔK analysis for a different number of clusters (K) for a tomato population consisting of 331 accessions (excluding 10 wild accessions). ΔK showed a peak at 2, suggesting two clusters as the optimal option. Source data

Supplementary Figure 3 Principal-component analysis (PCA) of 331 tomato accessions.

A total of 2,340,973 whole-genome SNPs (MAF > 10%, missing ≤ 5%) were used for PCA. Two-dimension coordinates were plotted for the 331 tomato accessions. CER (orange) and BIG (blue) accessions have a relatively concentrated distribution, whereas PIM accessions (green) are dispersed widely. Source data

Supplementary Figure 4 Distribution of private SNPs in three tomato groups.

Private SNPs are presented for each chromosome in PIM (green), CER (orange) and BIG (blue). Source data

Supplementary Figure 5 Genome-wide average LD decay in three tomato groups.

LD decay is estimated by the squared correlations of allele frequency (r2) against distance between polymorphic sites in PIM (green), CER (orange) and BIG (blue). Source data

Supplementary Figure 6 Distribution of fruit weight and size of the 500 F2 individuals.

(a) Frequency distribution of fruit weight in the F2 population. The fruit weight of both parents and the F1 are shown. (b) Fruit appearances of individuals from the F2 population. The two bulks (big bulk and small bulk) are constructed by selecting the fruits shown in the first and last two rows, respectively. Source data

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6, Supplementary Tables 2, 3, 5, 6 and 11, and Supplementary Note. (PDF 1319 kb)

Supplementary Tables 1, 4 and 7–10

Supplementary Tables 1, 4 and 7–10. (XLS 4822 kb)

Supplementary Data Set

Scripts and pipelines. (ZIP 226 kb)

Source data

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Lin, T., Zhu, G., Zhang, J. et al. Genomic analyses provide insights into the history of tomato breeding. Nat Genet 46, 1220–1226 (2014). https://doi.org/10.1038/ng.3117

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