Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato.

TitleMajor Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato.
Publication TypeJournal Article
Year of Publication2020
AuthorsAlonge, M, Wang, X, Benoit, M, Soyk, S, Pereira, L, Zhang, L, Suresh, H, Ramakrishnan, S, Maumus, F, Ciren, D, Levy, Y, Harel, THai, Shalev-Schlosser, G, Amsellem, Z, Razifard, H, Caicedo, AL, Tieman, DM, Klee, H, Kirsche, M, Aganezov, S, T Ranallo-Benavidez, R, Lemmon, ZH, Kim, J, Robitaille, G, Kramer, M, Goodwin, S, W McCombie, R, Hutton, S, Van Eck, J, Gillis, J, Eshed, Y, Sedlazeck, FJ, van der Knaap, E, Schatz, MC, Lippman, ZB
Date Published2020 Jul 09
KeywordsAlleles, Crops, Agricultural, Cytochrome P-450 Enzyme System, Ecotype, Epistasis, Genetic, Fruit, Gene Duplication, Gene Expression Regulation, Plant, Genome, Plant, Genomic Structural Variation, Genotype, Inbreeding, Molecular Sequence Annotation, Phenotype, Plant Breeding, Quantitative Trait Loci, Solanum lycopersicum

Structural variants (SVs) underlie important crop improvement and domestication traits. However, resolving the extent, diversity, and quantitative impact of SVs has been challenging. We used long-read nanopore sequencing to capture 238,490 SVs in 100 diverse tomato lines. This panSV genome, along with 14 new reference assemblies, revealed large-scale intermixing of diverse genotypes, as well as thousands of SVs intersecting genes and cis-regulatory regions. Hundreds of SV-gene pairs exhibit subtle and significant expression changes, which could broadly influence quantitative trait variation. By combining quantitative genetics with genome editing, we show how multiple SVs that changed gene dosage and expression levels modified fruit flavor, size, and production. In the last example, higher order epistasis among four SVs affecting three related transcription factors allowed introduction of an important harvesting trait in modern tomato. Our findings highlight the underexplored role of SVs in genotype-to-phenotype relationships and their widespread importance and utility in crop improvement.

Alternate JournalCell
PubMed ID32553272
PubMed Central IDPMC7354227
Grant ListT32 GM007057 / GM / NIGMS NIH HHS / United States
R01 MH113005 / MH / NIMH NIH HHS / United States
/ HHMI / Howard Hughes Medical Institute / United States
R50 CA243890 / CA / NCI NIH HHS / United States
P30 CA045508 / CA / NCI NIH HHS / United States
R01 LM012736 / LM / NLM NIH HHS / United States
UM1 HG008898 / HG / NHGRI NIH HHS / United States

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