Seasonal bud dormancy in perennial woody plants is a crucial and intricate process that is vital for the survival and development of plants. Over the past few decades, significant advancements have been made in understanding many features of bud dormancy, particularly in model species, where certain molecular mechanisms underlying this process have been elucidated. We provide an overview of recent molecular progress in understanding bud dormancy in trees, with a specific emphasis on the integration of common signaling and molecular mechanisms identified across different tree species. Additionally, we address some challenges that have emerged from our current understanding of bud dormancy and offer insights for future studies.

Summary: The seasonally synchronized annual growth cycle that is regulated mainly by photoperiod and temperature cues is a crucial adaptive strategy for perennial plants in boreal and temperate ecosystems. Phytochrome B (phyB), as a light and thermal sensor, has been extensively studied in Arabidopsis. However, the specific mechanisms for how the phytochrome photoreceptors control the phenology in tree species remain poorly understood. We characterized the functions of PHYB genes and their downstream PHYTOCHROME INTERACTING FACTOR (PIF) targets in the regulation of shade avoidance and seasonal growth in hybrid aspen trees. We show that while phyB1 and phyB2, as phyB in other plants, act as suppressors of shoot elongation during vegetative growth, they act as promoters of tree seasonal growth. Furthermore, while the Populus homologs of both PIF4 and PIF8 are involved in the shade avoidance syndrome (SAS), only PIF8 plays a major role as a suppressor of seasonal growth. Our data suggest that the PHYB‐PIF8 regulon controls seasonal growth through the regulation of FT and CENL1 expression while a genome‐wide transcriptome analysis suggests how, in Populus trees, phyB coordinately regulates SAS responses and seasonal growth cessation.

Photoperiod is a crucial environmental cue for phenological responses, including growth cessation and winter dormancy in perennial woody plants. Two regulatory modules within the photoperiod pathway explain bud dormancy induction in poplar (Populus spp.): the circadian oscillator LATE ELONGATED HYPOCOTYL 2 (LHY2) and GIGANTEA-like genes (GIs) both regulate the key target for winter dormancy induction FLOWERING LOCUS T2 (FT2). However, modification of LHY2 and GIs cannot completely prevent growth cessation and bud set under short-day conditions, indicating that additional regulatory modules are likely involved. We identified PtoHY5a, an orthologs of the photomorphogenesis regulatory factor ELONGATED HYPOCOTYL 5 (HY5) in poplar (Populus tomentosa), that directly activates PtoFT2 expression and represses the circadian oscillation of LHY2, indirectly activating PtoFT2 expression. Thus, PtoHY5a suppresses short day-induced growth cessation and bud set. Accordingly, PtoHY5a knockout facilitates dormancy induction. PtoHY5a also inhibits bud-break in poplar by controlling gibberellic acid (GA) levels in apical buds. Additionally, PtoHY5a regulates the photoperiodic control of seasonal growth downstream of phytochrome PHYB2. Thus, PtoHY5a modulates seasonal growth in poplar by regulating the PtoPHYB2–PtoHY5a–PtoFT2 module to determine the onset of winter dormancy, and by fine-tuning GA levels to control bud-break.

In temperate and boreal regions, perennial plants adapt their annual growth cycle to the change of seasons. In natural forests, juvenile seedlings usually display longer growth seasons compared to adult trees to ensure their establishment and survival under canopy shade. However, how trees adjust their annual growth according to their age is not known. In this study, we show that age-dependent seasonal growth cessation is genetically controlled and found that the miR156-SPL3/5 module, a key regulon of vegetative phase change (VPC), also triggers age-dependent growth cessation in Populus trees. We show that miR156 promotes shoot elongation during vegetative growth, and its targets SPL3/5s function in the same pathway but as repressors. We find that the miR156-SPL3/5s regulon controls growth cessation in both leaves and shoot apices and through multiple pathways, but with a different mechanism compared to how the miR156-SPL regulon controls VPC in annual plants. Taken together, our results reveal an age-dependent genetic network in mediating seasonal growth cessation, a key phenological process in the climate adaptation of perennial trees.

Flower initiation is a phenological developmental process strictly regulated in all flowering plants. Studies in Arabidopsis thaliana, a model plant organism in plant biology and genetics, and major cereal crops have provided fundamental knowledge and understanding of the underlying molecular mechanisms and regulation in annuals. However, this flowering process and underly molecular mechanisms in perennials are much more complicated than those in annuals and remain to be poorly understood, and documented. In recent years, the availability of more and more perennial plant genomes and advances in biotechnology have allowed the identification and characterization of flowering-associated gene orthologs in perennials. In this review, we compared and summarized the recent progress in regulation of flowering time in perennial trees, with an emphasis on the perennial-specific regulatory mechanisms. Besides, pleiotropic effects on tree growth habits such as juvenility, seasonal activity–dormancy growth, and the applications of tree flowering phenology are discussed.