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

Authors: GAO, LEI - Boyce Thompson Institute; GONDA, ITAY - Boyce Thompson Institute; SUN, HONGHE - Boyce Thompson Institute; MA, QIYUE - Boyce Thompson Institute; BAO, KAN - Boyce Thompson Institute; TIEMAN, DENISE - University Of Florida; BURZYNSKI-CHANG, ELIZABETH - Cornell University; Fish, Tara; STROMBERG, KAITLIN - Boyce Thompson Institute; SACKS, GAVIN - Cornell University; Thannhauser, Theodore - Ted; FOOLAD, MAJID - Pennsylvania State University; JOSE DIEZ, MARIA - Polytechnic University Of Valencia (UPV); BLANCA, JOSE - Polytechnical University Of Valencia; CANIZARES, JOAQUIN - Polytechnic University Of Valencia (UPV); XU, YIMIN - Boyce Thompson Institute; VAN DER KNAAP, ESTHER - University Of Georgia; HUANG, SANWEN - Chinese Academy Of Agricultural Sciences; KLEE, HARRY - University Of Florida; Giovannoni, James; 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. https://doi.org/10.1038/s41588-019-0410-2.
DOI: https://doi.org/10.1038/s41588-019-0410-2

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.