An annual gene expression atlas of tree peony identifies regulators of low-temperature-associated flowering

Plant development relies on the coordinated expression of gene modules across developmental stages, shaping diverse organs and tissues. Woody perennials are highly responsive to seasonal cues and often enter dormancy in winter. Tree peony (Paeonia suffruticosa), renowned as the 'king of flowers', possesses significant ornamental, medicinal, and edible value, yet the regulatory mechanisms governing its seasonal flowering remain largely unknown. Here, we constructed a monthly transcriptomic atlas of tree peony flower buds over a complete annual cycle, generating a resource spanning key developmental phases from vegetative growth to dormancy and blooming. Weighted gene co-expression network analysis identified multiple gene modules with month- or season-specific enrichment patterns. We found that the transition from vegetative to reproductive growth and subsequent blooming are distinctly but coordinately regulated at the transcriptional level. Critically, we identified and functionally characterized PsLIF (LOW-TEMPERATURE-INDUCED FACTOR), a transcription factor whose expression is specifically induced during cold acclimation. We demonstrate that PsLIF overexpression in Arabidopsis resulted in an early flowering phenotype following cold treatment. Furthermore, we found that PsLIF directly binds to the promoter of the florigen gene PsFT (FLOWERING LOCUS T) and activates its expression, thereby supporting its role in promoting flowering under low-temperature conditions. This annual transcriptome atlas not only provides a valuable resource for dissecting seasonal development in tree peony but also offers insights applicable to other perennial woody plants. Furthermore, the discovery of the PsLIF-PsFT regulatory module reveals a novel molecular mechanism underlying low-temperature-induced flowering in perennials, providing a perspective for investigating recurrent flowering from a genome-wide view.