Terminal Shoot Maturity Orchestrates LcSPL–LcFT1 Signaling to Dictate Low-Temperature Floral Induction in Litchi (Litchi chinensis Sonn.)

In perennial fruit trees, erratic floral initiation and alternate bearing represent major horticultural challenges, yet how vegetative shoot maturity conditions low-temperature responsiveness remains poorly understood. Here, using litchi (Litchi chinensis Sonn.) as a model, we deciphered the physiological and molecular framework governing maturity-dependent floral induction under winter chilling. Mature terminal shoots exhibited exceptional flowering competence and superior inflorescence morphology, whereas immature expanding shoots failed to initiate pure panicles. Dynamic metabolic profiling revealed that shoot maturation established a high-energy status characterized by elevated sucrose accumulation and sustained transcription of trehalose-6-phosphate synthase genes (LcTPS1/3/4). At the transcriptional level, specific members of LcSPL1, LcSPL3, and LcSPL10 were strongly upregulated in mature shoots, reaching peak expression at the “whitish millet” stage, marking morphological flower bud differentiation. Functional characterization in Arabidopsis thaliana confirmed that ectopic expression of LcSPL1/3/10 significantly accelerated flowering time and reduced rosette leaf number. Mechanistically, dual-luciferase reporter assays demonstrated that LcSPL1, LcSPL3, and LcSPL10 transcriptionally activated the promoter of the florigen gene LcFT1, with LcSPL1 exerting the strongest transactivation, whereas the immature shoot-enriched LcSPL9 repressed LcFT1 expression. Concurrently, mature leaves exhibited a dramatic surge in LcFT1 transcript levels alongside persistent suppression of the floral repressor LcTFL1. Together, our findings demonstrate that shoot maturity confers floral competence through an integrated T6P metabolism and LcSPL1/3/10–LcFT1 transcriptional cascade. This study provides crucial theoretical insights and potential targets for flowering-related regulation in perennial woody crops.