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A tomato telomere-to-telomere super-pangenome empowers stress resilience breeding

Nature Genetics (2026)Cite this article

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Abstract

Tomato (Solanum lycopersicum), one of the world’s most valuable vegetable crops, has suffered from diminished genetic diversity and stress resistance. Wild tomatoes serve as an invaluable genetic reservoir, yet their potential for stress resilience remains largely unexploited in tomato breeding. Here we report a genus-wide super-pangenome across 16 tomato species by integrating 20 telomere-to-telomere genomes and 27 published chromosome-scale genomes. Genus-wide population analysis demonstrates broad genetic diversity with limited gene flows among principal clades. Pan-centromere analysis reveals a diverse landscape and dynamic evolution of the mysterious tomato centromeres involving rapid diversification, satellite emergence and repositioning. A comprehensive catalog of structural variants uncovers extensive rearrangements, especially from wild tomatoes, and discovers key molecular markers associated with salinity resistance. Structural-variant-based genome-wide association studies identified a leucine-rich repeat receptor gene SlGMAK conferring gray mold resistance. Our telomere-to-telomere super-pangenome will accelerate exploiting the untapped potential of wild relatives to improve modern tomatoes for stress resilience.

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Fig. 1: Population analysis of wild and cultivated tomatoes.
Fig. 2: T2T genome assemblies of wild and cultivated tomatoes.
Fig. 3: Pan-centromere landscape and diversity of tomatoes.
Fig. 4: Super-pangenome analysis of 20 tomato accessions (16 species).
Fig. 5: Catalog of structural variations in tomato genomes reveals functional SVs affecting salt stress tolerance.
Fig. 6: SV-GWAS identified a GMR gene.

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Data availability

All raw sequencing data and genome assemblies generated in this study have been deposited in the China National Center for Bioinformation (CNCB, https://ngdc.cncb.ac.cn/, BioProject accession PRJCA030093). Whole-genome resequencing, CENH3 ChIP–seq, ATAC-seq and RNA-seq data have also been deposited in the National Center for Biotechnology Information (NCBI, BioProject accession PRJNA1201608). The genome assemblies and annotations are available via Zenodo at https://doi.org/10.5281/zenodo.17878268 (ref. 101). Tomato whole-genome resequencing data used in this study were downloaded from NCBI under BioProject PRJEB5235. Source data are provided with this paper.

Code availability

The scripts used in this study are available via GitHub at https://github.com/ChunmeiShi02/TomatoT2Tsuperpangenome and via Zenodo at https://doi.org/10.5281/zenodo.17935735 (ref. 102).

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Acknowledgements

We thank S. Huang for constructive suggestions on the paper, and the Tomato Genetics Resource Center at the University of California, Davis, for providing seeds for wild tomato accessions. We thank the Bioinformatics Platform at Peking University Institute of Advanced Agricultural Sciences for providing the high-performance computing resources. This work was supported by the Key R&D Program of Shandong Province (project 2025CXPT174 and 2025CXPT160 to C.Y.), the National Natural Science Foundation of China (32500545 to W.C.), the Shandong Provincial Natural Science Foundation (project SYS202206), the Yuandu Scholars Program, and the Taishan Scholars Program and Natural Science Foundation for Distinguished Young Scholars (ZR2023JQ010 to L.G.) of Shandong Province.

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  1. These authors contributed equally: Chunmei Shi, Shaoying Chen, Jingxuan Wang, Weikai Chen, Congying Sun.

Authors and Affiliations

  1. Shandong Key Laboratory of Precision Molecular Crop Design and Breeding, Peking University Institute of Advanced Agricultural Sciences, Shandong Laboratory of Advanced Agricultural Sciences in Weifang, Weifang, China

    Chunmei Shi, Shaoying Chen, Jingxuan Wang, Weikai Chen, Congying Sun, Shenhao Liao, Huan Wang, Yupei Mu, Xin Shu, Dian Meng, Jiaojiao Zhao, Liepeng Dong, Lihua Zhao, Shuguo Hou, Li Guo & Changxian Yang

  2. State Key Laboratory of Maize Bio-breeding, College of Plant Protection, China Agricultural University, Beijing, China

    Qiang Guo

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C.Y. and L.G. conceived and supervised the project. Q.G. collected material phenotypes. D.M. and X.S. prepared the biological materials for sequencing. C. Shi, S.C., J.W. and W.C. performed bioinformatic analyses and prepared tables and figures. C. Sun conducted gene functional analysis. S.L., H.W., Y.M., X.S., J.Z. and L.D. carried out molecular experiments. C. Shi, L.G., C.Y. and W.C. wrote and revised the paper. L.Z. and S.H. participated in discussion and result interpretation. All authors read and approve the final paper.

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Correspondence to Li Guo or Changxian Yang.

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Nature Genetics thanks Michael Bevan and Xingtan Zhang for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data

Extended Data Fig. 1 An overview of the tomato graph super-pangenome in this study.

a, The SL6.0 T2T genome enables comprehensive population analysis across 294 wild and cultivated tomato accessions. b, Construction of the super-pangenome and investigation of pan-centromere evolution. c, A graph-based super-pangenome facilitates discovering genetic variations associated with salt tolerance and grey mold resistance. d, Editing and establishing new editing systems in wild species or cultivated varieties for de novo crop domestication.

Extended Data Fig. 2 Genome assembly and annotation of S. lycopersicum T2T gap-free genome.

a, Whole-genome coverage of HiFi reads across the SL6.0 assembly. Regions with read depth below 100 or above 250 were marked by black shades. The GC content was shown as a blue curve. 5S rDNA was marked by blue boxes. Satellites were marked by red boxes. b, Examples of gap-closures on Chr04 and Chr05 for SL6.0 genome assembly. c. Comparison of the annotated proteomes from SL6.0 and SL5.0 genome.

Extended Data Fig. 3 Genome statistics and correlation with transposons in 20 wild and cultivated tomato genomes.

a, Genome size and N50 length statistics for the genomes analyzed in the study. b, Correlation between the size genomes and the length of TE across the 20 newly assembled genomes. c-f, Correlation between genome size and the length of different TE types, including Gypsy (c), DNA (d), LINE (e), and Copia (f) elements. Pearson correlation coeficients, the 95% confdence interval are shown for each comparison.

Extended Data Fig. 4 Evolution of centromeres in wild and cultivated tomatoes.

a-b, Distribution of Gypsy and specific satellites as well as CENH3 enrichment on chromosomes Chr02 (a) and Chr03 (b). Six species from five clades are taken as representatives. The Clade5 includes a closely related wild species and a widely-used domesticated tomato. The centromeres are marked with grey background boxes.

Extended Data Fig. 5 A proposed evolutionary model of satellite-based centromeres in tomatoes.

a, Evolution of specific satellites in wild and cultivated tomatoes. The boxes represent the type of specific 24-bp (Sat24) or 53-bp (Sat53) repeats. The circles showing presence of specific satellite for each chromosome (column) and accession (row). b, Comparison of two 45S rDNA monomers from S. lycopersicum and N. benthamiana illustrating the origin of specific Sat53 and centromere-specific CEN33/43 satellites, respectively. c, A proposed evolutionary pathway for formation of satellite-type centromeres in cultivated tomatoes. The centromere of Solanum ancestor was probably dominated by Gypsy retrotransposons; then Sat24 emerged in ancient wild tomatoes (for example JUG) and acted as centromeres. After that, the Sat24 degenerated while the Sat53 emerged in LYC, probably originated from the subrepeat of 45S rDNA; then Sat53 expanded approaching to original centromeres, which then employed CENH3 protein in wild tomatoes (for example PER). After that, the satellite-type centromeres (most exclusively dominated by Sat53) formed and matured in cultivated tomatoes, although there were only one or two.

Extended Data Fig. 6 Pan-NLRome analysis of 20 wild and cultivated tomatoes.

a, Statistics of pan- and core-NLR size across 20 tomato genomes, classified using OrthoFinder. The x-axis indicates the number of tomato accessions, while the y-axis indicates the number of gene families. The central line denotes the median, and the edges of the box define the first and third quartiles. The whiskers extend to the range of datapoints within 1.5 times the interquartile range (IQR) (the same for all subsequent boxplots) b, Core, softcore, dispensable and private NLR genes from 20 tomato genomes. Core NLR genes (present in 20 accessions), soft core NLR genes (present in 18-19 accessions), Dispensable NLR genes (present in 2-17 accessions) and private NLR genes (present in only one accession). c, Presence and absence information of NLR genes in 20 tomato genomes. d, Pan-NLRome landscape of tomato species from different clades. e, The microsyntenic relationships of one NLR gene clusters on Chr05 in three tomato accessions. SLL A, M82; SLL B, Heinz 1706; SLL C, TS-60; SLL D, AC.

Extended Data Fig. 7 Structural variation landscape and Pan-SV analysis of wild and cultivated tomatoes.

a, SV size distribution. TRA: translocation. INV: inversion. DEL: deletion. INS: insertion. b, Variation of SV count in the pan- and core-SV along as additional tomato genomes are incorporated. c, Compositions of the pan-SV and individual genomes. The histogram shows the number of SVs in the 46 genomes with different frequencies. The pie shows the proportion of the SVs marked by each composition. d, Presence and absence information of pan SV across the 46 genomes. Red pentagrams represent published genomes. e, Number of private SVs in wild and cultivated tomatoes, showing a higher abundance of private SVs in wild tomatoes. Statistical significance was determined using two-tailed Student’s t-test.

Extended Data Fig. 8 Landscape and functional effects of structural variants.

a, Genomic distribution of the SV in relation to the gene. b, SV distribution with respect to transposable elements (TE). c, Frequency distribution of two SVs (upper panel) and three haplotypes (lower panel) on SlHAK gene across 294 wild and cultivated accessions. n indicates the number of individuals per species; d, Na⁺ and K⁺ contents in roots and leaves under salt stress. From left to right panel, Na⁺ and K⁺ contents in roots, Na⁺ and K⁺ contents in leaves for 56 accessions carrying three haplotypes under salt stress. Numbers in brackets indicate the number of accessions per haplotype. Statistical significance was determined using two-tailed Student’s t-test. e, Frequency distribution of SVs on known genes across 294 wild and cultivated accessions. n indicates the number of individuals per species.

Extended Data Fig. 9 Pangenome assisted gene discovery and functional analysis for grey mold resistance in tomatoes.

a, Phenotype of tomato leaves after B. cinerea infection. The scale bar = 1 cm. b, Frequency distribution of lesion area on leaves of 209 accession after B. cinerea infection. c, Comparison of lesion area on leaves of 209 tomato accessions after B. cinerea inoculation. Scattered colors represent tomato species including 16 wild and one cultivated (SLC and SLL) species. n represent the number of accessions each clade. d, PCR validation of a 937-bp deletion in 24 tomato accessions. Numbers 1-24 correspond to accessions in Supplementary Table 21. Three independent experiments were conducted with similar results. e, Functional domains of SlGMAK were determined using Interpro (https://www.ebi.ac.uk/interpro/) and SMART (https://smart.embl.de/) (upper panel). The putative transmembrane (TM) region was predicted with DeeTMHMM (https://dtu.biolib.com/DeepTMHMM/) (lower panel). f, Expression pattern of SlGMAK gene in various tomato tissues using RNA-seq and RT-qPCR. 20 critical developmental stages (roots, stems, leaves, flowers and fruits) of MicroTom accession RNA-seq download from NCBI under the BioProject PRJCA001514 (n = 3). Upper right panel, quantitative of SlGMAK gene expression using RT-qPCR (n = 3). g-h, Transient overexpression of SlGMAK in tomato (g) and N. benthamiana (h) leaves. In g, leaves phenotype (left panel), relative expression levels of SlGMAK (middle panel) (n = 3) and lesion area (right panel) (n = 8) on leaves of tomato after B. cinerea infection. In h, leaves phenotype (left panel), relative expression levels of SlGMAK (middle panel) (n = 3) and lesion area (right panel) (n = 7) on leaves of N. benthamiana after B. cinerea infection. Scale bar = 1 cm. i, VIGS of SlGMAK in tomato plants. Phenotype of leaves (left panel), relative expression levels of SlGMAK (right upper panel) (n = 3) and lesion area (right lower panel) (n = 4) on leaves after B. cinerea infection in empty vector (EV) and VIGS-treated tomato plants. The scale bar = 1 cm. In f, g, h and i, all data are presented as mean ± SD with n for the number of biological repeats. Statistical significance was determined by two-sided Student’s t-tests.

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Source Data Figs. 5 and 6 and Extended Data Fig. 9

Statistical source data for Figs. 5 and 6 and Extended Data Fig. 9.

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Unprocessed gels for Extended Data Fig. 9d.

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Shi, C., Chen, S., Wang, J. et al. A tomato telomere-to-telomere super-pangenome empowers stress resilience breeding. Nat Genet (2026). https://doi.org/10.1038/s41588-026-02508-y

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