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

Lei Gao, Itay Gonda, Honghe Sun, Qiyue Ma, Kan Bao, Denise M. Tieman, Elizabeth A. Burzynski-Chang, Tara L. Fish, Kaitlin A. Stromberg, Gavin L. Sacks, Theodore W. Thannhauser, Majid R. Foolad, Maria Jose Diez, Jose Blanca, Joaquin Canizares, Yimin Xu, Esther van der Knaap, Sanwen Huang, Harry J. Klee, James J. Giovannoni & 1 others Zhangjun Fei

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Pages (from-to)1044-1051
Number of pages8
JournalNature Genetics
Volume51
Issue number6
DOIs
StatePublished - Jun 1 2019

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Lycopersicon esculentum
Fruit
Alleles
Genome
Genes
Disease Resistance
Quantitative Trait Loci
Genetically Modified Plants
Heterozygote
Breeding

All Science Journal Classification (ASJC) codes

  • Genetics

Cite this

Gao, L., Gonda, I., Sun, H., Ma, Q., Bao, K., Tieman, D. M., ... Fei, Z. (2019). The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. Nature Genetics, 51(6), 1044-1051. https://doi.org/10.1038/s41588-019-0410-2
Gao, Lei ; Gonda, Itay ; Sun, Honghe ; Ma, Qiyue ; Bao, Kan ; Tieman, Denise M. ; Burzynski-Chang, Elizabeth A. ; Fish, Tara L. ; Stromberg, Kaitlin A. ; Sacks, Gavin L. ; Thannhauser, Theodore W. ; Foolad, Majid R. ; Diez, Maria Jose ; Blanca, Jose ; Canizares, Joaquin ; Xu, Yimin ; van der Knaap, Esther ; Huang, Sanwen ; Klee, Harry J. ; Giovannoni, James J. ; Fei, Zhangjun. / The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. In: Nature Genetics. 2019 ; Vol. 51, No. 6. pp. 1044-1051.
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Gao, L, Gonda, I, Sun, H, Ma, Q, Bao, K, Tieman, DM, Burzynski-Chang, EA, Fish, TL, Stromberg, KA, Sacks, GL, Thannhauser, TW, Foolad, MR, Diez, MJ, Blanca, J, Canizares, J, Xu, Y, van der Knaap, E, Huang, S, Klee, HJ, Giovannoni, JJ & Fei, Z 2019, 'The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor', Nature Genetics, vol. 51, no. 6, pp. 1044-1051. https://doi.org/10.1038/s41588-019-0410-2

The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. / Gao, Lei; Gonda, Itay; Sun, Honghe; Ma, Qiyue; Bao, Kan; Tieman, Denise M.; Burzynski-Chang, Elizabeth A.; Fish, Tara L.; Stromberg, Kaitlin A.; Sacks, Gavin L.; Thannhauser, Theodore W.; Foolad, Majid R.; Diez, Maria Jose; Blanca, Jose; Canizares, Joaquin; Xu, Yimin; van der Knaap, Esther; Huang, Sanwen; Klee, Harry J.; Giovannoni, James J.; Fei, Zhangjun.

In: Nature Genetics, Vol. 51, No. 6, 01.06.2019, p. 1044-1051.

Research output: Contribution to journalArticle

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AU - Gao, Lei

AU - Gonda, Itay

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AU - Tieman, Denise M.

AU - Burzynski-Chang, Elizabeth A.

AU - Fish, Tara L.

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AU - Sacks, Gavin L.

AU - Thannhauser, Theodore W.

AU - Foolad, Majid R.

AU - Diez, Maria Jose

AU - Blanca, Jose

AU - Canizares, Joaquin

AU - Xu, Yimin

AU - van der Knaap, Esther

AU - Huang, Sanwen

AU - Klee, Harry J.

AU - Giovannoni, James J.

AU - Fei, Zhangjun

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N2 - 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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