CsHEC1 integrates brassinosteroid and auxin pathways to regulate hypocotyl elongation in cucumber

Hypocotyl length is a core indicator for seedling quality that directly affects vegetative growth and crop final yield. Despite intensive studies have been investigated the mutual promotion effect of auxin and brassinosteroids (BRs) in shaping hypocotyl elongation in Arabidopsis, the regulatory relationship between auxin and BR during hypocotyl development in horticultural crops remains largely unknown. In this study, we investigated the function of HECATE1 (CsHEC1) in cucumber seedlings and found that CsHEC1 positively regulates hypocotyl elongation. CsHEC1 can directly activate the expression of auxin biosynthesis YUCCA8 (CsYUC8), thereby promoting auxin biosynthesis. Exogenous application of the 1-Naphthaleneacetic acid (NAA) to Cshec1 mutants could mostly rescue the short-hypocotyl phenotype. Mutation of BRASSINOSTEROID INSENSITIVE 2 (BIN2), a negative regulator in the BR signaling pathway, resulted in long-hypocotyl phenotype upon 24-epibrassinolide (24-eBL) treatment in cucumber. However, the promoting effect of 24-eBL on hypocotyl elongation was abolished in Cshec1 mutants. Biochemical analyses demonstrated that CsBIN2 can interact with and phosphorylate CsHEC1, which consequently triggers the degradation of CsHEC1 and thus impairs the activation of CsYUC8. The hypocotyl length of Csbin2 Cshec1 double mutant resemble that of Cshec1 single mutant, indicating that CsBIN2 acts upstream of CsHEC1. In summary, our data suggested that CsHEC1 integrated BR signaling and auxin biosynthesis to regulate cucumber hypocotyl elongation, thus providing a valuable target for high-quality seedling breeding in cucumber.