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ARS Home » Northeast Area » Ithaca, New York » Robert W. Holley Center for Agriculture & Health » Plant, Soil and Nutrition Research » Research » Publications at this Location » Publication #362764

Research Project: Genetics, Epigenetics, Genomics, and Biotechnology for Fruit and Vegetable Quality

Location: Plant, Soil and Nutrition Research

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

item GAO, LEI - Boyce Thompson Institute
item GONDA, ITAY - Boyce Thompson Institute
item SUN, HONGHE - Boyce Thompson Institute
item MA, QIYUE - Boyce Thompson Institute
item BAO, KAN - Boyce Thompson Institute
item TIEMAN, DENISE - University Of Florida
item BURZYNSKI-CHANG, ELIZABETH - Cornell University
item Fish, Tara
item STROMBERG, KAITLIN - Boyce Thompson Institute
item SACKS, GAVIN - Cornell University
item Thannhauser, Theodore - Ted
item FOOLAD, MAJID - Pennsylvania State University
item JOSE DIEZ, MARIA - Polytechnic University Of Valencia (UPV)
item BLANCA, JOSE - Polytechnical University Of Valencia
item CANIZARES, JOAQUIN - Polytechnic University Of Valencia (UPV)
item XU, YIMIN - Boyce Thompson Institute
item VAN DER KNAAP, ESTHER - University Of Georgia
item HUANG, SANWEN - Chinese Academy Of Agricultural Sciences
item KLEE, HARRY - University Of Florida
item Giovannoni, James
item FEI, ZHANGJUN - Boyce Thompson Institute

Submitted to: Nature Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/13/2019
Publication Date: 5/13/2019
Citation: Gao, L., Gonda, I., Sun, H., Ma, Q., Bao, K., Tieman, D., Burzynski-Chang, E., Fish, T., Stromberg, K., Sacks, G., Thannhauser, T.W., Foolad, M., Jose Diez, M., Blanca, J., Canizares, J., Xu, Y., Van Der Knaap, E., Huang, S., Klee, H., Giovannoni, J.J., Fei, Z. 2019. The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. Nature Genetics. 51:1044-1051.

Interpretive Summary: Development of a complete genome sequence for an organism typically involves sequencing and assembly of a single genotype . Once a high quality genome sequence is developed it serves as a reference for re-sequencing of additional genotypes of the species. Among the multitude of uses of genome sequences, re-sequencing efforts help identify genetic variations though major genetic differences such as novel genes are often lost. With sufficient sequencing of additional genotypes there is an opportunity to identify unique sequences constituting e a pan-genome incorporating the full spectrum of novelty captured in sequenced genomes of the species. We present a tomato pan-genome developed from re-sequencing of 725 tomato accessions. We identified 4,873 genes absent in the original tomato reference genome. Among these we found a rare gene influencing flavor chemistry and prevalent in wild tomatoes but absent in many cultivated accessions. While still uncommon, this gene has become more prevalent in modern varieties in concert with renewed breeding efforts focused on flavor as a response to consumer dissatisfaction with tomato quality.

Technical 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 TomLoxC promoter selected against during domestication. QTL mapping and analysis of transgenic plants reveal a novel 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.