Perennial plants in boreal and temperate regions have developed adaptive growth strategies that enable them to cycle annually between growth and dormancy, protecting shoot apical meristems from adverse environmental conditions [1]. A key trait of perennials is their capacity to remain dormant, during which the meristem temporarily becomes unresponsive to growth-promoting signals until dormancy is lifted [2]. Throughout the life cycle of perennial plants, buds progress through distinct dormancy stages: paradormancy, endodormancy, and ecodormancy [3]. Notably, the transition from endodormancy to ecodormancy is crucial for subsequent bud break and flowering under favorable spring conditions [4]. Understanding the mechanisms governing bud dormancy transition (BDT) is essential for addressing significant agricultural challenges, particularly issues like failed bud break and blooming of perennials growing in the subtropical zone [5,6,7,8].

MADS-box transcription factors are distinguished by the MADS domain, a highly conserved region located at the N-terminal of the protein [9]. The MADS-box gene family, comprising type I and type II (MIKC-type) genes, is crucial for plant growth and development, with MIKC-type genes serving as key regulators of bud dormancy and flowering [10,11]. MIKC-type genes are further categorized into two subgroups, MIKC^C and MIKC*, based on sequence variations in the intervening region [12]. In Arabidopsis thaliana, MIKC^C genes are grouped into 12 phylogenetic clades, including AP1/FUL, SOC1, AG, SVP, AGL15 (AGL18), AP3/PI, SEP, AGL6, FLC, BS, AGL12, and AGL17 [13,14]. The analysis of increasing transcriptome data indicates that MIKC genes are modulated by environmental signals and play a pivotal role in regulating bud dormancy [15,16]. Among these MIKC genes, the Dormancy-associated MADS-box (DAM) gene, a homolog of the Arabidopsis SHORT VEGETATIVE PHASE (SVP) gene, was first identified in a non-dormant evergrowing peach (Prunus persica) mutant [17] and later recognized as a master regulator of dormancy induction and maintenance in perennial species, such as peach [18], leafy spurge (Euphorbia esula) [19], pear (Pyrus pyrifolia) [20], and apricot (Prunus mume) [21].

In contrast to the DAM gene, another MIKC homolog, Arabidopsis SUPPRESSOR OF OVEREXPRESSION OF CO1 (SOC1), has been shown to facilitate bud dormancy release and bud break in tree peony (Paeonia suffruticosa) [22] and kiwifruit (Actinidia chinensis) [23]. In hybrid aspen (Populus tremula x Populus tremuloides), the APETALA1 (AP1) gene regulates seasonal growth cessation via the CONSTANS (CO)/FLOWERING LOCUS T (FT) module [24]. Additionally, a newly identified MIKC gene, the low-temperature-induced MADS-box (LIM1) gene, has been shown to activate the gibberellic acid (GA) pathway, facilitating dormancy release by reducing callose accumulation and reopening plasmodesmata [25]. MIKC genes are also involved in responding to various stresses. In Arabidopsis, AGL16 negatively regulates drought resistance by affecting stomatal density and movement [26]. AGL21 is responsive to various environmental stresses, with its overexpression resulting in increased sensitivity to abscisic acid, salt, and osmotic stresses [27]. Moreover, MIKC genes are also crucial for regulating flower development and flowering time [14]. In tomato (Solanum lycopersicum), the overexpression of the MIKC gene Tomato MADS 8 (TM8) led to abnormal stamens and poorly viable pollen [28]. In Arabidopsis, key MIKC genes such as SOC1 [29], FLOWERING LOCUS C (FLC) [30], AGAMOUS-LIKE 18 (AGL18) [31], AGL24 [32], and SVP [33] have been identified as crucial regulators of flowering time. Nevertheless, the mechanisms by which MIKC genes regulate bud dormancy in herbaceous perennials remain poorly understood.

Herbaceous peony (Paeonia lactiflora Pall.), belonging to the Paeoniaceae family, is a versatile ornamental and oil crop cultivated worldwide, known for its vibrant flowers and promising oilseed production [34,35]. The overwintering buds of herbaceous peony are generated from underground parts in autumn and enter endodormancy under a short daylength and low temperatures [36]. Sufficient low temperatures are needed in winter to complete the transition from endodormancy to ecodormancy [8]. However, global warming has resulted in increasingly frequent warm winters, reducing the accumulation of chilling temperatures necessary for the dormancy transition of herbaceous peony [36,37]. This disruption hampers subsequent growth and development, ultimately leading to reduced crop yields, particularly in southern China [37,38]. Current research has predominantly focused on understanding the processes of bud dormancy in woody plants, while the mechanisms governing these processes in herbaceous peony remain largely unexplored [39]. Although our previous studies on physiological responses and gene expression have identified several MIKC gene homologs, such as SVP, SOC1, and AP1, whose expression correlates with dormancy transitions [36,40], a comprehensive exploration of MIKC gene involvement in regulating bud dormancy in herbaceous peony is still lacking.