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The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor

Nature Genetics volume 51, pages 1044–1051 (2019)Cite this article

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Abstract

Modern tomatoes have narrow genetic diversity limiting their improvement potential. We present a tomato pan-genome constructed using genome sequences of 725 phylogenetically and geographically representative accessions, revealing 4,873 genes absent from the reference genome. Presence/absence variation analyses reveal substantial gene loss and intense negative selection of genes and promoters during tomato domestication and improvement. Lost or negatively selected genes are enriched for important traits, especially disease resistance. We identify a rare allele in the TomLoxC promoter selected against during domestication. Quantitative trait locus mapping and analysis of transgenic plants reveal a role for TomLoxC in apocarotenoid production, which contributes to desirable tomato flavor. In orange-stage fruit, accessions harboring both the rare and common TomLoxC alleles (heterozygotes) have higher TomLoxC expression than those homozygous for either and are resurgent in modern tomatoes. The tomato pan-genome adds depth and completeness to the reference genome, and is useful for future biological discovery and breeding.

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Fig. 1: Pan-genome of tomato.
Fig. 2: PAVs of genes in wild and cultivated tomatoes.
Fig. 3: Gene selection preference during tomato domestication and improvement.
Fig. 4: Variation of TomLoxC expression under different promoter alleles.
Fig. 5: Involvement of TomLoxC in apocarotenoid biosynthesis.

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Data availability

Raw genome and RNA-Seq reads have been deposited into the National Center for Biotechnology Information Sequence Read Archive under accession codes SRP150040, SRP186721 and SRP172989, respectively. The nonreference genome sequences and annotated genes of the tomato pan-genome and SNPs called from the RIL population are available via the Dryad Digital Repository (https://doi.org/10.5061/dryad.m463f7k).

Change history

  • 23 May 2019

    In the version of the article originally published, the URL https://doi.org/10.5061/dryad.m463f7k in the ‘Data availability’ section was hyperlinked incorrectly. In addition, the copyright holder was listed as ‘The Author(s)’, but the copyright line should have read ‘This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply, 2019’. The errors have been corrected in the HTML and PDF versions of the article.

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Acknowledgements

This research was supported by grants from the US National Science Foundation (IOS-1339287 to Z.F. and J.J.G.; IOS-1539831 to Z.F., J.J.G. and H.J.K.; and IOS-1564366 to E.v.d.K., J.C. and D.M.T.), BARD, the US–Israel Binational Agricultural Research and Development Fund, a Vaadia-BARD Postdoctoral Fellowship Award (FI-508-14 to I.G.) and the USDA Agricultural Research Service.

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Author notes

  1. These authors contributed equally: Lei Gao, Itay Gonda.

Authors and Affiliations

  1. Boyce Thompson Institute for Plant Research, Cornell University, Ithaca, NY, USA

    Lei Gao, Itay Gonda, Honghe Sun, Qiyue Ma, Kan Bao, Kaitlin A. Stromberg, Yimin Xu, James J. Giovannoni & Zhangjun Fei

  2. Unit of Aromatic and Medicinal Plants, Newe Ya’ar Research Center, Agricultural Research Organization, Ramat Yishay, Israel

    Itay Gonda

  3. Horticultural Sciences, Plant Innovation Center, University of Florida, Gainesville, FL, USA

    Denise M. Tieman & Harry J. Klee

  4. Department of Food Science, Cornell University, Ithaca, NY, USA

    Elizabeth A. Burzynski-Chang & Gavin L. Sacks

  5. US Department of Agriculture–Agricultural Research Service, Robert W. Holley Center for Agriculture and Health, Ithaca, NY, USA

    Tara L. Fish, Theodore W. Thannhauser, James J. Giovannoni & Zhangjun Fei

  6. Department of Plant Science, The Pennsylvania State University, University Park, PA, USA

    Majid R. Foolad

  7. Institute for the Conservation and Improvement of Agricultural Biodiversity, Polytechnic University of Valencia, Valencia, Spain

    Maria Jose Diez, Jose Blanca & Joaquin Canizares

  8. Department of Horticulture, University of Georgia, Athens, GA, USA

    Esther van der Knaap

  9. Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, China

    Sanwen Huang

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  1. Lei Gao
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Contributions

Z.F., J.J.G., H.J.K., S.H. and E.v.d.K. designed and managed the project. I.G., E.A.B.-C., K.A.S., T.L.F., G.L.S., T.W.T., D.M.T., Y.X., M.J.D., J.B., J.C., M.R.F. and E.v.d.K. collected samples and performed experiments. L.G., I.G., H.S., Q.M. and K.B. performed data analyses. L.G. and I.G. wrote the manuscript. Z.F. and J.J.G. revised the manuscript.

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Correspondence to James J. Giovannoni or Zhangjun Fei.

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Gao, L., Gonda, I., Sun, H. et al. The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. Nat Genet 51, 1044–1051 (2019). https://doi.org/10.1038/s41588-019-0410-2

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