FvGI–FvCO–FvFT1 pathway activates FvTFL1 in long days to repress flowering in woodland strawberry ( Fragaria vesca )

Photoperiod is a stable seasonal signal. Although photoperiodic flowering is well understood in short-day (SD) and long-day (LD) annual plants, the regulatory mechanisms in perennials remain elusive. In a perennial woodland strawberry (Fragaria vesca), flowering is induced in SDs in autumn and plants flower following spring, while in plants with mutated FvTERMINAL FLOWER1 (FvTFL1), LDs induce flowering. We investigated photoperiodic flowering of F. vesca through phenotypic and molecular characterization of transgenic lines and their crosses. We studied natural variation in flowering time and gene expression in European accessions and explored their correlations with climatic, geographical and genetic origins. We showed that FvGIGANTEA (FvGI) activates FvFLOWERING LOCUS T1 (FvFT1) via FvCONSTANS (FvCO) in LDs resulting in early flowering in fvtfl1 mutant. In natural accessions, FvFT1 activates FvTFL1 to repress flowering, and decreasing expression of FvFT1 and FvTFL1 towards colder climates in the east and north correlates with earlier flowering. We define a photoperiodic flowering pathway controlling floral transition of perennial F. vesca in autumn that differs from known mechanisms in annual and perennial plants. Our findings open new avenues to understand how perennial plants cope with changing seasons across climatic and geographical ranges.