Genome-wide characterization of the tomato GASA family identifies SlGASA1 as a repressor of fruit ripening

Abstract

Gibberellins (GAs) play crucial roles in a wide range of developmental processes and stress responses in plants. However, the roles of GA-responsive genes in tomato (Solanum lycopersicum) fruit development remain largely unknown. Here, we identify 17 GASA (Gibberellic Acid-Stimulated Arabidopsis) family genes in tomato. These genes encode proteins with a cleavable signal peptide at their N terminus and a conserved GASA domain at their C terminus. The expression levels of all tomato GASA family genes were responsive to exogenous GA treatment, but adding ethylene eliminated this effect. Comprehensive expression profiling of SlGASA family genes showed that SlGASA1 follows a ripening-associated expression pattern, with low expression levels during fruit ripening, suggesting it plays a negative role in regulating ripening. Overexpressing SlGASA1 using a ripening-specific promoter delayed the onset of fruit ripening, whereas SlGASA1-knockdown fruits displayed accelerated ripening. Consistent with their delayed ripening, SlGASA1-overexpressing fruits showed significantly reduced ethylene production and carotenoid contents compared to the wild type. Moreover, ripening-related genes were downregulated in SlGASA1-overexpressing fruits but upregulated in SlGASA1-knockdown fruits compared to the wild type. Yeast two-hybrid, co-immunoprecipitation, transactivation, and DNA pull-down assays indicated that SlGASA1 interacts with the key ripening regulator FRUITFULL1 and represses its activation of the ethylene biosynthesis genes ACS2 and ACO1. Our findings shed new light on the role and mode of action of a GA-responsive gene in tomato fruit ripening.

Acknowledgements

This research was supported by the National Natural Science Foundation of China (32172643 and 32172271), the Applied Basic Research Category of Science and Technology Program of Sichuan Province (2021YFQ0071; 2022YFSY0059), and the Technology Innovation and Application Development Program of Chongqing (cstc2021jscx-cylhX0001). This project was also supported by the Fundamental Research Funds for the Central Universities (SCU2021D006).

Author contributions

M.L. planned and designed the research; D.S., Z.Y., Y.L., and Y.Z. performed the experiments; K.L., Y.Z., Y.W., H.., X.Z., and H.C. analysed data; M.L. and H.D. wrote the manuscript, and D.G. helped improve the manuscript..

Data availability

The authors confirm that all the experimental data are available and accessible via the main text and/or the supplemental data.

Conflict of interests

The authors declare no conflict of interest.

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