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.
Journal article
Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato
Cell, Vol.182(1), pp.145-161.e23
09/Jul/2020
PMID: 32553272
Abstract
Details
- Title
- Major Impacts of Widespread Structural Variation on Gene Expression and Crop Improvement in Tomato
- Creators
- Michael Alonge (null) - Johns Hopkins UniversityXingang Wang (null) - Cold Spring Harbor LaboratoryMatthias Benoit (null) - Cold Spring Harbor LaboratorySebastian Soyk (null) - University of LausanneLara Pereira (null) - University of Georgia (United States, Athens) - UGALei Zhang (null) - University of Georgia (United States, Athens) - UGAHamsini Suresh (null) - Cold Spring Harbor LaboratorySrividya Ramakrishnan (null) - Johns Hopkins UniversityFlorian Maumus (null) - University of Paris-SaclayDanielle Ciren (null) - Cold Spring Harbor LaboratoryYuval Levy (null) - 972WIS_INST___110Tom Hai Harel (null) - The Weizmann Institute of ScienceGili Shalev-Schlosser (null) - The Weizmann Institute of ScienceZiva Amsellem (null) - The Weizmann Institute of ScienceHamid Razifard (null) - University of Massachusetts AmherstAna L. Caicedo (null) - University of Massachusetts AmherstDenise M. Tieman (null) - University of FloridaHarry Klee (null) - University of FloridaMelanie Kirsche (null) - Johns Hopkins UniversitySergey Aganezov (null) - Johns Hopkins UniversityT. Rhyker Ranallo-Benavidez (null) - Johns Hopkins UniversityZachary H. Lemmon (null) - Inari AgricultureJennifer Kim (null) - Cold Spring Harbor LaboratoryGina Robitaille (null) - Cold Spring Harbor LaboratoryMelissa Kramer (null) - Cold Spring Harbor LaboratorySara Goodwin (null) - Cold Spring Harbor LaboratoryW. Richard McCombie (null) - Cold Spring Harbor LaboratorySamuel Hutton (null) - Florida Gulf Coast UniversityJoyce Van Eck (null) - Cornell UniversityJesse Gillis (null) - Cold Spring Harbor LaboratoryYuval Eshed (null) - 972WIS_INST___110Fritz J. Sedlazeck (null) - Baylor College of MedicineEsther van der Knaap (null) - University of Georgia (United States, Athens) - UGAMichael C. Schatz (Corresponding Author) - Johns Hopkins UniversityZachary B. Lippman (Corresponding Author) - Cold Spring Harbor Laboratory
- Resource Type
- Journal article
- Publication Details
- Cell, Vol.182(1), pp.145-161.e23; 09/Jul/2020
- Number of pages
- 17
- Language
- English
- DOI
- https://doi.org/10.1016/j.cell.2020.05.021
- PMID
- 32553272
- Grant note
- We thank members of the Schatz and Lippman labs at JHU and CSHL for helpful discussions. We thank Aleksey Zimin at JHU for helpful discussions about genome assembly. We thank T. Mulligan, A. Krainer, S. Qiao, and K. Schlecht from CSHL for assistance with plant care. We thank S. Muller, R. Wappel, S. Mavruk-Eskipehlivan, and E. Ghiban from the CSHL Genome Center for sequencing support. We thank Sanwen Huang at the Chinese Academy of Agricultural Sciences and Dani Zamir at the Hebrew University for sharing sequencing data and germplasm. We thank Prashant Hosmani, Susan Strickler, Naama Menda, and Lukas Mueller at the Boyce Thompson Institute for Plant Research for providing early access to the SL4.0 reference genome and hosting data on the Solanaceae Genomics Network. We thank Surya Saha and Lukas Mueller for early access to Heinz 1706 PacBio data. This work was supported by the Howard Hughes Medical Institute and grant support from the US National Institutes of Health for their support of the CSHL Cancer Center Next Generation Shared Resource (5P30CA045508-31) and (R01LM012736 and R01MH113005) to J.G. and (UM1 HG008898) to F.J.S., the USDA National Institute of Food and Agriculture (AFRI no. 2018-67013-27896; SCRI no. 2015-51181-24312) to S.H. and (AFRI no. 2016-67013-24452) to S.H. and Z.B.L., the BARD (BARD US-Israel Agricultural Research and Development Fund) (IS-5120-18C) to Y.E. and Z.B.L., the ISF (Israel Science Foundation) (1913/19) to Y.E., and the National Science Foundation Plant Genome Research Program (IOS 1855585) to D.M.T. and H.K.; (IOS 1564366) to A.L.C., D.M.T., and E.v.d.K.; (IOS-1350041) to M.C.S.; and (IOS-1732253) to J.V.E., E.v.d.K., M.C.S., and Z.B.L. Author contributions - M.C.S. and Z.B.L. conceived the project. M.A., X.W., S.S., L.P., L.Z., J.V.E., J.G., Y.E., F.J.S., E.v.d.K., M.C.S., and Z.B.L. designed and planned experiments. M.A., X.W., M.B., S.S., L.P., L.Z., D.C., Y.L., T.H.H., G.S.-S., Z.A., H.R., A.L.C., D.M.T., J.K., G.R., J.V.E., J.G., Y.E., F.J.S., E.v.d.K., M.C.S., and Z.B.L. performed experiments and collected data. M.A., X.W., M.B., S.S., L.P., L.Z., H.S., S.R., F.M., Y.L., T.H.H., G.S.-S., Z.A., D.M.T., H.K., T.R.R.-B., Z.H.L., S.H., J.G., Y.E., F.J.S., E.v.d.K., M.C.S., and Z.B.L. analyzed data. M. Kirsche and S.A. wrote software for SV merging. M. Kramer, S.G., and W.R.M. performed long-read sequencing. M.A., X.W., M.C.S., and Z.B.L. wrote the manuscript with input from M.B., L.P., L.Z., Y.E., and E.v.d.K. All authors read, edited, and approved the manuscript.
- Record Identifier
- 993265599903596
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