SPL3/4/5 Integrate Developmental Aging and Photoperiodic Signals into the FT-FD Module in Arabidopsis Flowering

Environmental sensitivity varies across developmental phases in flowering plants. In the juvenile phase, microRNA156 (miR156)-mediated repression of SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE (SPL) transcription factors renders Arabidopsis plants incompetent to floral inductive signals, including long-day (LD) photoperiod. During the vegetative phase transition, which accompanies a reduction of miR156 and a concomitant elevation of its targets, plants acquire reproductive competence such that LD signals promote flowering. However, it remains largely unknown how developmental signals are associated with photoperiodic flowering. Here, we show that SPL3, SPL4, and SPL5 (SPL3/4/5) potentiate the FLOWERING LOCUS T (FT)-FD module in photoperiodic flowering. SPL3/4/5 function as transcriptional activators through the interaction with FD, a basic leucine zipper transcription factor which plays a critical role in photoperiodic flowering. SPL3/4/5 can directly bind to the promoters of APETALA1, LEAFY, and FRUITFULL, thus mediating their activation by the FT-FD complex. Our findings demonstrate that SPL3/4/5 act synergistically with the FT-FD module to induce flowering under LDs, providing a long-sought molecular knob that links developmental aging and photoperiodic flowering.