Enhanced brassinosteroid signaling via the overexpression of SlBRI1 positively regulates the chilling stress tolerance of tomato

Abstract

Brassinosteroids (BRs) regulate plant development and response to stress. BRASSINOSTEROID INSENSITIVE 1 (BRI1) is a BR receptor that activates BR signaling. Although the function of the tomato BR receptor SlBRI1 in regulating growth and drought resistance has been examined, that of SlBRI1 in cold tolerance is unclear. This study indicated that the expression of SlBRI1 in tomato was rapidly induced and reached its highest level at 3 h under chilling treatment and then decreased. The overexpression of SlBRI1 displayed low relative electrolyte leakage, malondialdehyde content, and reactive oxygen species (ROS) accumulation under chilling stress. The proline content and activities of superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) in SlBRI1OE plants were higher than those in the wild-type (WT) plants after chilling stress. The transcript abundances of five cold-responsive genes were higher in SlBRI1OE plants than in WT plants during chilling stress. RNA sequence analysis showed that the expression of the majority of genes encoding photosystem I and II were downregulated. The degree of suppression in SlBRI1OE plants was weaker than that in WT plants. Additionally, the Pn and Fv/Fm of SlBRI1OE plants were significantly higher than those of WT plants under chilling stress. We identified several genes encoding key enzymes in BRs; indole acetic acid (IAA), gibberellin (GA), and abscisic acid (ABA) biosynthesis or signaling were upregulated or downregulated during chilling stress. Chilling stress decreased the BRs and GA3 content, and increased IAA and ABA content. The contents were lower or higher in SlBRI1OE than in WT plants. Furthermore, chilling stress regulated the expression levels of 43 transcription factors. The expression of seven cold-regulated protein genes was higher or lower in SlBRI1OE plants than in WT plants under chilling stress. These results suggest that SlBRI1 positively regulates chilling tolerance mainly through ICE1–CBF–COR pathway in tomato.