Releasing a sugar brake generates sweeter tomato without yield penalty

Jinzhe Zhang, Hongjun Lyu, Jie Chen, Xue Cao, Ran Du, Liang Ma, Nan Wang, Zhiguo Zhu, Jianglei Rao, Jie Wang, Kui Zhong, Yaqing Lyu, Yanling Wang, Tao Lin, Yao Zhou, Yongfeng Zhou, Guangtao Zhu, Zhangjun Fei, Harry Klee & Sanwen Huang

Nature volume 635, pages 647–656 (2024). Published: 13 November 2024

Abstract

In tomato, sugar content is highly correlated with consumer preferences, with most consumers preferring sweeter fruit1^,2^,3^,4. However, the sugar content of commercial varieties is generally low, as it is inversely correlated with fruit size, and growers prioritize yield over flavour quality5^,6^,7. Here we identified two genes, tomato (Solanum lycopersicum) calcium-dependent protein kinase 27 (SlCDPK27; also known as SlCPK27) and its paralogue SlCDPK26, that control fruit sugar content. They act as sugar brakes by phosphorylating a sucrose synthase, which promotes degradation of the sucrose synthase. Gene-edited SlCDPK27 and SlCDPK26 knockouts increased glucose and fructose contents by up to 30%, enhancing perceived sweetness without fruit weight or yield penalty. Although there are fewer, lighter seeds in the mutants, they exhibit normal germination. Together, these findings provide insight into the regulatory mechanisms controlling fruit sugar accumulation in tomato and offer opportunities to increase sugar content in large-fruited cultivars without sacrificing size and yield.

See https://www.nature.com/articles/s41586-024-08186-2

Figure 1: Identification and characterization of SlCDPK27.

a, Manhattan plot of SNPs associated with total SSC. The y axis shows the −log scale of P values, which was determined using a mixed linear model with a binomial test, implemented in EMMAX. The dotted line denotes the threshold for statistical significance: 1.0 × 10⁻⁶ for GWAS. b, Linkage disequilibrium plot for SNPs in the 190-kb interval surrounding the leading SNP. Black bars, genes. Asterisk, position of the leading SNP. The colour key (white to red) represents linkage disequilibrium values (D′). c, Correlation between SlCDPK27 expression levels and total SSCs in tomato. The Pearson correlation coefficient (R) and its corresponding P value, which was calculated from a two-sided test, are indicated at the top. d, Haplotypes of SlCDPK27 among tomato natural variations. In the box plots, the boxes represent the interquartile range, the line in the middle of each box represents the median, the whiskers represent the interquartile range and the dots represent outlier points; n indicates the number of accessions belonging to each haplotype. P values were derived by one-way analysis of variance. e, Allele distribution of the 12-bp insertion in PIM, CER and BIG groups. n indicates the number of accessions in each group.