Grapevine (Vitis) is a vital fruit crop with global cultivation [1], prized for its diverse applications. These include the production of wine, table fruit, jam, juice, dried varieties, vinegar, grape seed extract, and grape seed oil [2]. However, grape production faces a significant challenge from cold stress, particularly the late spring cold. This stress adversely affects the grapevine growth, development, yield, and quality. Recently, China and other countries, such as France, North America, and Australia, have experienced more frequent late spring cold events due to global climate change [[3], [4], [5], [6], [7], [8], [9]], posing an ongoing risk to grape production. Therefore, identifying cold-resistance genes and unraveling the regulatory mechanisms that govern grapevine responses to cold stress are critical research priorities for ensuring the healthy development of the grape and wine industry.

When plants are exposed to cold stress, a series of injuries ensue, including increased cell membrane permeability, disruption of cell structure stability, damage to enzyme activity on the cell membrane, and inhibition of photosynthesis and metabolism [[10], [11], [12]]. Moreover, cold stress induces the production of reactive oxygen species (ROS) in plants, such as hydroxyl radicals (HO−), superoxide ions (O2−), and hydrogen peroxide (H2O2) [13,14]. Excessive ROS accumulation leads to oxidative stress, causing damage to DNA, RNA, proteins, and membranes [15]. To counteract these adverse effects, plants have developed intricate adaptive mechanisms [16,17]. This includes a sophisticated homeostasis system, incorporating the enzymatic defense system [18,19] and the accumulation of osmolytes, such as proline [20]. These mechanisms contribute to maintain intracellular ROS homeostasis, allowing adaption to cold stresses. Peroxiredoxins (Prxs), a family of antioxidant enzymes that reduce hydrogen or organic peroxides, play essential roles in regulating ROS balance under biotic and abiotic stresses [21,22]. In plants, the 2-Cys Prx (BAS1), as the subgroup of peroxiredoxins, has been demonstrated to play a key role in the redox regulation [23,24] and participates in defense against oxidative [[25], [26], [27]], salt [28,29], cold [30], and high temperature stresses [31].

Additionally, transcription factors (TFs) are widely recognized for their essential roles in improving cold tolerance. These TFs are rapidly activated in response to cold stress, initiating downstream signal regulation networks that mediate plant responses to cold stress [[32], [33], [34], [35], [36]]. Among these TFs, C-repeat binding proteins (CBFs) and cold-responsive (COR) genes constitute the most well-understood regulatory cascade. However, some studies indicate that CBFs only regulate a small percentage of COR genes [37,38], suggesting the involvement of other TFs in the COR gene regulation. Presently, numerous TFs in plants have been identified as key players in responding to cold stress, including MYB [39], WRKY [40], NAC [41], and bHLH [42].

As one of the largest groups of regulatory factors in plants, the APETALA2/ETHYLENE-RESPONSIVE FACTORS (AP2/ERFs) TF family, possessing one or two conserved AP2 domains, can be categorized into four subfamilies: AP2 (APETALA2), ERF (ethylene response factor), DREB (dehydration responsive element binding), and RAV (related to ABI3/VP1) [43]. The ERF subfamily, boasting the most members, regulates downstream targets by directly binding the GCC-box (GCCGCC) cis-acting element within their promoters [43]. Extensive evidence supports the involvement of ERFs in the plant's response to cold stress. In Arabidopsis, the overexpression of ERFs, such as AtDREB1, AtERF105, AtERF102, and AtERF103, significantly enhances cold tolerance [[44], [45], [46]]. Similarly, in apples, ERFs such as MdERF1B, MdERF113, and MdERF11 participate in the response to cold stress [[47], [48], [49]]. This pattern extends to other plants, with examples including PtrERF9, PtrERF108, and PtrERF109 in orange [[50], [51], [52]], SlERF·B3 and SlERF·B8 in tomato [53,54], MaERF10 and MaERF110 in banana [55,56], and VaERF57, VvERF63, VaERF92, and VviERF105 in grapevine [33,[57], [58], [59]]. However, numerous plant ERF genes still remain unexplored suggests a relatively unknown role in cold resistance. Moreover, the regulatory network and target genes of ERFs in response to cold stress are in the early stages of exploration, particularly in grapevine, where knowledge is notably lacking.

In a prior study, we conducted a transcriptome analysis on cold-treated grapevine seedlings, identifying 80 cold-induced TFs, including 32 ERF genes. Among them, VIT_03s0063g00460 encoded an ERF protein (VvERF117), which significantly upregulated post-cold treatment [60]. However, the function and potential regulatory mechanism of VvERF117 remain unclear. In this study, we investigated the role of VvERF117 in cold tolerance through overexpression and RNA interference (RNAi). The results demonstrated that VvERF117 overexpression increased cold tolerance in Arabidopsis and grape calli by increasing proline content, antioxidant enzyme activity (superoxide dismutase (SOD), peroxidase (POD), catalase (CAT), and ascorbate peroxidase (APX)), and VvCBF transcription while decreasing ROS accumulation. Conversely, silencing VvERF117 had the opposite effect. Finally, we employed yeast one-hybrid (Y1H) and dual luciferase (LUC) assays to examine the transcriptional regulation of cold-responsive genes by VvERF117.