The ubiquitin ligase SINA3 and the transcription factor WOX14 regulate tomato growth and development

Abstract

Abstract In this study, we demonstrated that a regulatory module consisting of the SEVEN IN ABSENTIA (SINA) ubiquitin ligase SINA3 and the WUSCHEL homeobox-containing (WOX) transcription factor WOX14 fine-tunes tomato (Solanum lycopersicum) growth and development. Overexpression of SINA3 in tomato (SINA3-OX) resulted in dwarfism due to shortened internodes with smaller cells. SINA3 regulates WOX14 levels through ubiquitin-independent proteasome-mediated degradation, wherein SINA3 acts as a linker between WOX14 and the proteasome subunits REGULATORY PARTICLE NON-ATPASEs 9 and 13 (RPN9 and RPN13). Moreover, WOX14 knockout plants (WOX14-KO) exhibited dwarfism comparable to that of SINA3-OX plants. Genetic analyses showed that SINA3 controls vegetative growth by regulating WOX14 accumulation. Notably, WOX14 directly binds to the promoters of GA biosynthesis genes and activates their expression, thereby enhancing GA levels. Knockout of the GA biosynthesis gene GA3ox1 (GA3ox1-KO) caused growth retardation in tomato, similar to SINA3-OX and WOX14-KO transgenic plants. Bioactive GA levels were lower in SINA3-OX and WOX14-KO plants compared to the controls, and exogenous bioactive GA application partially restored their vegetative growth. This finding suggests that the SINA3–WOX14 module regulates vegetative growth in both GA-dependent and -independent manners. In addition, the SINA3–WOX14 module regulates GA-mediated reproductive growth and development, including fruit growth, seed set, seed growth, and maturation.