Short-day-induced expression of PtTFL2 triggers growth–defense tradeoffs during Pinus tabuliformis dormancy

Conifers have developed intricate dormancy strategies to cope with extreme climates in winter. Among various environmental cues, shortened photoperiods in the fall induce conifers to enter dormancy, leading to growth cessation, bud set, and enhanced freezing tolerance. However, the molecular mechanisms of short-day-induced dormancy are not fully understood. In this study, we treated Pinus tabuliformis seedlings with different photoperiods and confirmed that short days rapidly induced and promoted dormancy. Transcriptomic analysis of photoperiod and annual cycle conditions revealed that the expression of TFL1-like (PtTFL2) was highly associated with various biological processes associated with dormancy. Heterologous overexpression studies showed that PtTFL2 promoted dormancy in poplar and delayed vegetative growth and enhanced freezing tolerance in both poplar and Arabidopsis thaliana. The transcription factor co-expression network centered on PtTFL2 identified for the co-transcription factors PtNF-YC18 and PtNAC67. PtTFL2 physically interacted with PtNF-YC18 to synergistically regulate both vegetative growth and growth cessation during dormancy. Additionally, PtTFL2 interacted with PtNAC67 to directly activate PtDHN2 expression, enhancing freezing tolerance during dormancy. Our findings highlight the role of PtTFL2 in conifer dormancy rapidly induced by short days and outline a regulatory network centered on PtTFL2 wherein two modules (PtTFL2-PtNF-YC18 and PtTFL2-PtNAC67) trigger growth-defense tradeoffs in the onset of winter dormancy.