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 (<i>Solanum lycopersicum</i>) fruit development remain largely unknown. Here, we identify 17 <i>GASA</i> (<i>Gibberellic Acid-Stimulated Arabidopsis</i>) 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 <i>GASA</i> family genes were responsive to exogenous GA treatment, but adding ethylene eliminated this effect. Comprehensive expression profiling of <i>SlGASA</i> family genes showed that <i>SlGASA1</i> follows a ripening-associated expression pattern, with low expression levels during fruit ripening, suggesting it plays a negative role in regulating ripening. Overexpressing <i>SlGASA1</i> using a ripening-specific promoter delayed the onset of fruit ripening, whereas <i>SlGASA1</i>-knockdown fruits displayed accelerated ripening. Consistent with their delayed ripening, <i>SlGASA1</i>-overexpressing fruits showed significantly reduced ethylene production and carotenoid contents compared to the wild type. Moreover, ripening-related genes were downregulated in <i>SlGASA1</i>-overexpressing fruits but upregulated in <i>SlGASA1</i>-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 <i>ACS2</i> and <i>ACO1</i>. Our findings shed new light on the role and mode of action of a GA-responsive gene in tomato fruit ripening.