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Redesigning the tomato fruit shape for mechanized production

Nature Plants volume 9, pages 1659–1674 (2023)Cite this article

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An Author Correction to this article was published on 08 January 2024

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Abstract

Crop breeding for mechanized harvesting has driven modern agriculture. In tomato, machine harvesting for industrial processing varieties became the norm in the 1970s. However, fresh-market varieties whose fruits are suitable for mechanical harvesting are difficult to breed because of associated reduction in flavour and nutritional qualities. Here we report the cloning and functional characterization of fs8.1, which controls the elongated fruit shape and crush resistance of machine-harvestable processing tomatoes. FS8.1 encodes a non-canonical GT-2 factor that activates the expression of cell-cycle inhibitor genes through the formation of a transcriptional module with the canonical GT-2 factor SlGT-16. The fs8.1 mutation results in a lower inhibitory effect on the cell proliferation of the ovary wall, leading to elongated fruits with enhanced compression resistance. Our study provides a potential route for introducing the beneficial allele into fresh-market tomatoes without reducing quality, thereby facilitating mechanical harvesting.

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Fig. 1: fs8.1-mediated shape change confers enhanced fruit resistance to squeezing.
Fig. 2: FS8.1 encodes a GT-2-like protein that lacks the duplicate trihelix domains.
Fig. 3: FS8.1 regulates fruit shape via activation of SlKRP2 expression.
Fig. 4: FS8.1 activates SlKRP2 expression by interacting with SlGT-16 and SlGT-34.
Fig. 5: FS8.1 increases the transcriptional activity of SlGT-16.
Fig. 6: Editing of FS8.1 improves the CR of fresh-market tomato fruits without compromising quality.

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Data availability

The RNA-seq data have been deposited in the Genome Sequence Archive (GSA; https://ngdc.cncb.ac.cn/gsa/) at the Beijing Institute of Genomics (BIG) Data Center, Chinese Academy of Sciences, under accession number CRA008400. The sequence data of the following genes (and their accession numbers) in this article can be found in the Sol Genomics Network (SGN): FS8.1 (Solyc08g061910), SlGT-16 (Solyc04g071360), SlGT-34 (Solyc12g056510), SlGT-30 (Solyc11g005380), SlGT-26 (Solyc09g009250), SlGT-26L (Solyc10g083567), SlKRP1 (Solyc03g044480), SlKRP2 (Solyc02g090680), SlKRP4 (Solyc12g098310) and SP (Solyc06g074350). Materials used in this study are available upon request. Source data are provided with this paper.

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Acknowledgements

We thank J. Li for assistance with the fruit CR measurements. This work was supported by the National Key Research and Development Program of China (2022YFF1003000 and 2021YFF1000103 to L.D.), the National Natural Science Foundation of China (31991183 to C.L., 32072582 to L.D., U22A20459 to C.L. and 31772319 to L.S.) and the Beijing Joint Research Program for Germplasm Innovation and New Variety Breeding (G20220628003 to C.L.).

Author information

Author notes

  1. These authors contributed equally: Qiang Zhu, Lei Deng and Jie Chen.

Authors and Affiliations

  1. State Key Laboratory of Plant Genomics, National Center for Plant Gene Research (Beijing), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    Qiang Zhu, Lei Deng, Chuanlong Sun, Zeqian Chang, Tianxia Yang, Hongling Jiang & Chuanyou Li

  2. CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing, China

    Qiang Zhu, Chuanlong Sun, Zeqian Chang, Tianxia Yang & Chuanyou Li

  3. College of Life Sciences, Shandong Agricultural University, Tai’an, China

    Lei Deng, Chuanlong Sun & Chuanyou Li

  4. College of Horticulture, China Agricultural University, Beijing, China

    Jie Chen & Liang Sun

  5. Instituto de Investigaciones en Ciencias Agrarias de Rosario (IICAR-CONICET-UNR), Rosario, Argentina

    Gustavo R. Rodríguez

  6. College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China

    Huawei Zhai

  7. Institute of Plant Breeding, Department of Horticulture, University of Georgia, Athens, GA, USA

    Yasin Topcu & Esther van der Knaap

  8. Batı Akdeniz Agricultural Research Institute, Antalya, Turkey

    Yasin Topcu

  9. Department of Horticulture and Crop Science, The Ohio State University, Columbus, OH, USA

    David Francis

  10. Gulf Coast Research and Education Center, University of Florida, Gainesville, FL, USA

    Samuel Hutton

  11. Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (North China), Ministry of Agriculture, Beijing Vegetable Research Center, Beijing Academy of Agriculture and Forestry Sciences, Beijing, China

    Chang-Bao Li

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  1. Qiang Zhu
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Contributions

C.L. conceived and supervised the project. Q.Z. and L.D. performed most of the experiments. J.C., G.R.R., Z.C., T.Y., H.Z., Y.T., S.H. and L.S. performed the genotyping of the tomato germplasm. Q.Z., C.S., H.Z. and H.J. performed the plant transformations. T.Y. and C.-B.L. helped grow the plants. D.F. and E.v.d.K. reviewed and edited the manuscript. With input from all authors, C.L., L.D. and Q.Z. wrote the manuscript. All authors read and approved the content of the manuscript.

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Correspondence to Chuanyou Li.

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Extended data

Extended Data Fig. 1 fs8.1-mediated shape change leads to increased fruit firmness.

a, Fruit and ovary shape index measurements via Tomato Analyzer version 4.0 and ImageJ (NIH). The fruit and ovary shape indexes are defined as the ratios of the maximum height length (L) to maximum width (W) of a fruit or an ovary. b,c, Fruit shape indexes (b) and CR (c) of different fresh-market and processing tomatoes. In b, n = 16, 12, 9, 11, 11, 12, 9, 13, 13, 13, 6 fruits from left to right. In c, n = 12, 14, 11, 10, 11, 10, 15, 18, 16, 18, 14 fruits from left to right. d, Fruit shape indexes of LA0716, M82 and NILs (n = 8, 8, 11, 8, 11 fruits from left to right). e, Ripe fruits of LA1589 and Rio Grande. Bar = 1 cm. f, Fruit shape index of LA1589 and Rio Grande (n = 13 fruits). g, Ripe fruits of fs8.1 NILs in the background of Rio Grande. Bar = 1 cm. h, Fruit shape indexes of fs8.1 NILs in the background of Rio Grande (n = 7 fruits). i, CR of fs8.1 NILs in the background of Rio Grande. n = 17 (for NIL-FS8.1) and 31 (for NIL-fs8.1) fruits. j, Sequence analysis showing the Solyc08g061910A857T mutation in different fresh-market or processing tomato accessions. Bars represent the means ± SD. The significance of the difference was evaluated by two-tailed Student’s t tests, the exact P value is indicated on the graph.

Source data

Extended Data Fig. 2 Genetic validation of the FS8.1 candidate gene.

a, Generation of fs8.1 mutants in the IL8-1-1 background. The sgRNA targets and protospacer adjacent motifs (PAMs) are highlighted in red and bold fonts, respectively. The blue dashes indicate deletions, and the numbers indicate the numbers of nucleotides involved. b‒f, Histological and cellular observations of anthesis ovaries of IL8-1-1 and fs8.1 mutants. The cell number and cell size were measured along the red, blue and yellow lines indicated in Fig. 1a. IOWL, inner ovary wall length; OWT, ovary wall thickness; CL, columella length. In b, n = 10, 11, 11, 10, 11, 10 ovaries from left to right. In c, n = 9, 10, 11, 10, 10, 10 ovaries from left to right. In d, n = 10, 12, 11, 10, 11, 10 ovaries from left to right. In e, n = 11, 8, 9 ovaries from left to right. In f, n = 12 ovaries. g, Fruit weight of IL8-1-1 and fs8.1 mutants (n = 22, 27, 12, 13 fruits from left to right). h, RT‒qPCR results showing Solyc08g061910 expression in 9 DBA ovaries of the indicated genotypes (n = 3 independent biological replicates). i‒m, Histological and cellular observations of the anthesis ovaries of M82 and Comp lines. The cell number and cell size were measured along the red, blue and yellow lines indicated in Fig. 1a. IOWL, inner ovary wall length; OWT, ovary wall thickness; CL, columella length. In i, n = 8, 10, 11, 10, 13, 13 ovaries from left to right. In j, n = 9, 11, 11, 11, 14, 13 ovaries from left to right. In k, n = 9, 10, 9, 10, 13, 13 ovaries from left to right. In l, n = 12, 16, 16 ovaries from left to right. In m, n = 10, 12, 12 ovaries from left to right. Bars represent the means ± SD. The significance of the difference was evaluated by two-tailed Student’s t tests, the exact P value is indicated on the graph.

Source data

Extended Data Fig. 3 FS8.1 encodes a GT-2-like protein that lacks the duplicate trihelix domains.

a, Protein sequence alignment of SlGT-16, SlGT-34, FS8.1 and fs8.1. The gray boxes indicate the conserved domains. b, Phylogenetic tree of trihelical transcription factors in tomato and Arabidopsis. The phylogenetic tree was constructed by the neighbor-joining method using MEGA version 7.0. The five clades composing the trihelix family are indicated by different colors. The FS8.1 gene is highlighted in the red box. c, Structures of SlGT-16, FS8.1 and fs8.1 predicted by AlphaFold. N, N-terminus; C, C-terminus; TD1, trihelix domain 1; TD2, trihelix domain 2; HD, α-helical domain. AlphaFold produces a per-residue confidence score (pLDDT) between 0 and 100. Some regions below 50 pLDDT may be unstructured in isolation. Accession numbers are from the SGN and TAIR database. The phylogenetic tree was constructed by the neighbor-joining method using MEGA version 7.0.

Extended Data Fig. 4 Phylogenetic analyses of FS8.1 and SlGT-16.

a,b, Phylogenetic analyses of FS8.1 orthologs (a) and SlGT-16 orthologs (b). Accession numbers are from the SGN, CuGenDB, TAIR, Phytozome and NCBI databases.

Extended Data Fig. 5 FS8.1 differentially regulates cell cycle-related genes.

a, RT‒qPCR results showing the expression levels of FS8.1, SlKRP2 and SlGT-16 in various tissues of AC plants (n = 3 independent biological replicates). MG, mature green; B, breaker; B + 4/7, 4/7 days after the breaker stage. b, Photograph of flowers at the indicated developmental stages. Bar = 5 mm. c, Expression profiles of cell cycle-related genes regulated by FS8.1. The FC (log10 scale) of the average expression of each gene is shown. d, Phylogenetic tree of tomato KRPs and their Arabidopsis orthologs based on protein sequences. The phylogenetic tree was constructed by the neighbor-joining method using MEGA version 7.0. The scale bar indicates the average number of amino acid substitutions per site. e, Generation of slkrp1 slkrp2 slkrp4 triple mutants in the IL8-1-1 background. The sgRNA targets and PAM are highlighted in red and bold font, respectively. The blue dashes and letters indicate deletions and insertions, respectively, and the numbers indicate the numbers of nucleotides involved (+, insertion; -, deletion). f, Fruit shape indexes of IL8-1-1, slkrp2 mutants (n = 14 fruits). g, RT‒qPCR results showing SlKRP2 expression in the anthesis ovaries of the indicated genotypes (n = 3 independent biological replicates). Bars represent the means ± SD. The significance of the difference was evaluated by two-tailed Student’s t tests, the exact P value is indicated on the graph.

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Extended Data Fig. 6 SlGT-16 and SlGT-34 redundantly regulate SlKRP2 expression and fruit shape formation.

a, LCI assays designed to determine interactions between FS8.1 and five canonical GT-2 factors (n = 10, 10, 10, 10, 9, 10 independent biological replicates from left to right). Tobacco cells coexpressing FS8.1-nLUC and cLUC were used as negative controls. b, RT‒qPCR results showing SlGT-16 expression in the ovaries of the indicated genotypes at anthesis (n = 3 independent biological replicates). c, Generation of single and double mutants of SlGT-16 and SlGT-34 in different backgrounds. The sgRNA targets and PAMs are highlighted in red and bold font, respectively. The blue dashes and letters indicate deletions and insertions, respectively, and numbers indicate the numbers of nucleotides involved (+, insertion; -, deletion). d, Ripe fruits of AC, slgt-16, slgt-34 and slgt-16 slgt-34 mutants. Bar = 1 cm. e, Fruit shape indexes of AC, slgt-16, slgt-34 and slgt-16 slgt-34 mutants (n = 16, 17, 16, 14, 13, 16, 17 fruits from left to right). f, RT‒qPCR results showing SlKRP2 expression in the ovaries of the indicated genotypes at anthesis (n = 3 independent biological replicates). Bars represent the means ± SD. The significance of the difference was evaluated by two-tailed Student’s t tests, the exact P value is indicated on the graph.

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Extended Data Fig. 7 Editing of FS8.1 enhances fruit firmness without compromising nutrition.

a, Generation of fs8.1 single mutants and fs8.1 sp double mutants in different backgrounds. The sgRNA targets and PAM are highlighted in red and bold font, respectively. The blue dashes and letters indicate deletions and insertions, respectively, and the numbers indicate the numbers of nucleotides involved (+, insertion; -, deletion). b, Ripe fruits of AC and fs8.1 mutants. Bar = 1 cm. c, d, Fruit shape indexes (c) and fruit CR (d) of AC and fs8.1 mutants. n = 16 (for c) and 12 (for d) fruits. e, Fruit weight of AC and fs8.1 mutants (n = 25, 21, 18 fruits from left to right). f‒k, Contents of fruit quality-related metabolites. In f, g, i‒k, n = 4 independent biological replicates. In h, n = 3 independent biological replicates. Bars represent the means ± SD. The significance of the difference was evaluated by two-tailed Student’s t tests, the exact P value is indicated on the graph.

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Zhu, Q., Deng, L., Chen, J. et al. Redesigning the tomato fruit shape for mechanized production. Nat. Plants 9, 1659–1674 (2023). https://doi.org/10.1038/s41477-023-01522-w

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