Plant abiotic stress has become one of the key constraints to agricultural production and food security. Among them, drought, cold, and salinity stress are primary abiotic factors that impair plant growth and development and constrain their geographic distribution. These stresses often cause similar effects on plants, such as disrupting cellular osmotic balance, damaging cell membrane structures, and impairing antioxidant defense systems (Qu et al., 2019). To survive adverse environmental conditions, plants have evolved intricate signaling and gene regulatory pathways. These sophisticated mechanisms enable adaptation and mitigation against the detrimental impacts of abiotic stresses. Sugar metabolism, as one of these pathways, plays a crucial role in the process by which plants resist abiotic stress (Qin et al., 2018; Ma et al., 2019; Yoon et al., 2020). Sugars not only provide energy and carbon sources but also participate in signal transduction and the regulation of physiological processes. Although a large number of studies have shown that sugar metabolism is extensively involved in plant stress, relatively few studies have been conducted on how sugar mediates stress mechanisms.

Transcription factors, as key components of signal transduction, play the role of “molecular switches” in the transcriptional regulatory networks of abiotic stress responses. WRKY transcription factors (TFs), a unique class of proteins in higher plants, are widely involved in regulating various physiological and metabolic pathways. They are capable of highly specific recognition and binding to cis-acting elements called W-box on DNA sequences. This binding directly regulates the transcription levels of target genes, including self and other stress-related genes, and thus plays a key role in plant response to abiotic stresses. In addition, WRKY TFs can also bind to cis-acting elements in the promoter regions of sugar metabolism genes and regulate the expression of sugar metabolism-related genes (Sun et al., 2003; Govardhana and Kumudini, 2020; Goyal et al., 2020). Through regulation of the sugar metabolism pathway, they mediate responses to stress, thus improving plant tolerance to abiotic stresses and injury, and mitigating the damage inflicted by stress on plants (Wu et al., 2020).

Therefore, this paper mainly analyzed the structure and classification of WRKY transcription factors, summarized the research results and reviewed the regulatory mechanisms of WRKY transcription factors themselves in response to abiotic stresses as well as their involvement in abiotic stresses in plants through sugar metabolism pathways, with a view to providing a theoretical basis for the genetic improvement of plant stress tolerance, and providing a technological safeguard for the enhancement of agricultural production and the assurance of food safety.

WRKY TFs are among the largest families of transcription factors in higher plants and are designated as the “central regulators” of the abiotic stress response. The first WRKY TFs, SPF1, was originally identified and isolated from Ipomoea batatas (Ishiguro and Nakamura, 1994). Subsequent studies have characterized numerous WRKY TFs across diverse plant species, including. Arabidopsis (Glöckner et al., 2002), Oryza sativa (Kim et al., 2000), soybean (Schmutz et al., 2010), and Hordeum vulgare (Mangelsen et al., 2008). Comprehensive research has elucidated the extensive membership and multifaceted regulatory mechanisms characterizing the WRKY transcription factor family. By constructing complex signaling networks, WRKY TFs play a crucial role in plant growth, development, and stress responses (ülker and Somssich, 2004; Rushton et al., 2010).

WRKY TFs derive their nomenclature from the characteristic WRKY domain, defined by the highly conserved WRKYGQK motif (Wu et al., 2020). This family of proteins is characterized by the fact that all family members contain at least one WRKY structural domain consisting of about 60 highly conserved amino acids, the N-terminal end of which contains the highly conserved WRKYGQK heptapeptide sequence, and the C-terminal end of which has a zinc-finger motif of either the C₂H₂ or the C₂HC type (Wang et al., 2014b). WRKY TFs specifically recognize W-box cis-elements (A/TAACCA; C/TAACG/TG) in target gene promoters, thereby modulating transcription. Depending on the number of conserved WRKY domains and the type of zinc finger structure, WRKY transcription factors are usually divided into three families: family I contains two WRKY domains and two C₂H₂ zinc finger structures, family II contains one WRKY domain and one C₂H₂ zinc finger structure, and family III contains one WRKY domain and one C₂H₂ zinc finger structure. Family II is subdivided into five subfamilies: a, b, c, d, and e. Family II WRKY proteins are involved in the regulation of plant growth and development, such as senescence, seed dormancy, and germination; they are also involved in plant responses to drought, salt stress, and cold damage (Rushton et al., 2012). WRKYs cannot form homologous or heterodimers if they do not have LZ (leucine zipper) motifs (Narusaka et al., 2016). In addition to the above structural domains, WRKY transcription factor families have many other structures, such as kinase domains, glutamine rich regions, proline rich regions, nuclear localization signals, and so on. The existence of these structural domains makes it possible for these WRKY proteins to regulate the expression of target genes through the formation of homodimers or heterodimers by protein-protein interactions (Zhang and Wang, 2005; Agarwal et al., 2011) ( Figure 1 ).

In recent years, as climate change and extreme weather events have increased, the impact of abiotic stress on crop production has become more pronounced, resulting in slowed growth, deteriorating quality, and reduced yields (Hrmova and Hussain, 2021; Khoso et al., 2022). Consequently, over the course of long-term natural selection and evolutionary processes, plants have developed a complex and finely tuned regulatory network that enables them to detect and respond effectively to various environmental stresses (Su et al., 2023). Facing abiotic stress, WRKY TFs could dynamically modulate downstream gene expression, either enhancing transcriptional activation or imposing repression, directly regulating the expression of genes involved in stress response, or participate in other signaling pathways and regulatory networks to manage the stress response ( Figure 2 ). This activation of defense mechanisms helps enhance crop resilience against abiotic stress (Ma and Hu, 2024). Given that extensive and in-depth studies and reviews have already been conducted on WRKY TFs’ roles in responding to abiotic stress ( Table 1 ), this paper provides only a concise summary of the key findings.

Drought stress, as an essential abiotic stress, poses a serious threat to plant growth, development, and yield. Recent studies have identified multiple WRKY TFs as key regulators of drought tolerance. IgWRKY50 and IgWRKY32 in Iris germanica, which can enhance drought resistance in transgenic Arabidopsis by coordinated up-regulation of drought-responsive downstream genes (Zhang et al., 2022a). In Glycine max, GmWRKY17 directly binds to promoters of drought-inducible genes GmDREB1D and GmABA2, activating their transcription under water deficit (Yi and Yueping, 2023). SbWRKY30 in Sorghum bicolor directly activates the drought-response gene SbRD19, conferring improved growth and survival rates under drought stress (Yang et al., 2020).

Salt stress critically constrains plant growth and development, wherein WRKY transcription factors (TFs) execute pivotal regulatory roles. ZmWRKY104 in Zea mays overexpression enhances salt tolerance via positive regulation of ZmSOD4, reducing ROS accumulation, MDA content, and electrolyte leakage (Yan et al., 2022).In Gossypium hirsutum, GhWRKY34 confers salt tolerance by modulating selective Na⁺/K⁺ uptake and maintaining low Na⁺/K⁺ ratios in leaves/roots (Zhou et al., 2015).GmWRKY54 in Glycine max activates transcription in response to salt stress by binding to the W-box elements of the promoters of the DREB2A and STZ/ZAT10 genes, which are key transcription factors in the ABA-independent pathway that regulates osmoprotective substance synthesis, and STZ/ZAT10, which is involved in ROS scavenging and ion homeostasis maintenance (Zhou et al., 2008).

WRKY TFs also have a significant job in responding to heavy metal stresses. In Oryza sativa, OsWRKY74 regulates the expression of a set of downstream genes involved in phosphorus uptake, transport, and metabolism, collectively enhancing rice tolerance to phosphorus starvation (Dai et al., 2016). Similarly, OsWRKY72 negatively regulates lignin synthesis and accumulation by inhibiting the expression of OsGLP8-7 (germin-like protein), thereby reducing the ability of the cell wall to retain heavy metal ions and realizing the regulation of Cd/Cu toxicity (Shangguan et al., 2024). TaWRKY70 in Triticum aestivum reduces root Cd²⁺influx by re-pressing the expression of AtNRAMP5, AtHMA3, AtYSL3, and AtIRT1 heavy-metal transporter genes, which act as Cd transporters, while TaWRKY70 activates the expression of the TaCAT5 promoter by directly binding to its W-box motif to enhance catalase activity, reduce membrane lipid peroxidation, scavenge ROS, and confer resistance to Cd stress in transgenic Arabidopsis (Jia et al., 2021).

In addition, with global climate change in recent years, both high and low temperatures have become significant agricultural meteorological disasters, severely limiting normal plant and crop development. Heat stress triggers upregulation of WRKY25 and WRKY26 yet downregulates WRKY33 in Arabidopsis thaliana. Molecular evidence reveals that these three factors synergistically enhance thermotolerance by coordinating ethylene signaling activation with heat shock protein (HSP) pathways, leveraging functional crosstalk and complementary effects (Li et al., 2011). In Capsicum annuum, the transcription of CaWRKY40 is induced by Ralstonia solanacearum and high temperature. Heat stress induces an upregulation of CaWRKY40 expression, and its overexpression enhances heat stress tolerance, likely through the regulation of antioxidant systems and maintenance of cell membrane stability (Dang et al., 2013). Regarding low temperature, Zhang et al. (2022b) proposed a transcriptional regulatory cascade model involving OsWRKY63–OsWRKY76–OsDREB1B, where OsWRKY63 acts as a transcriptional repressor by inhibiting the expression of OsWRKY76, thereby suppressing the activation of OsDREB1B, which leads to reduced cold tolerance (Zhang et al., 2022b). The expression of VbWRKY32 was significantly increased in Verbena leaves under cold stress. Overexpression of the VbWRKY32 gene in Verbena and comparison of the expression profiles of cold-responsive genes between overexpressed and wild-type plants under cold stress revealed that VbWRKY32 acted as a positive regulator to enhance the cold resistance of plants by up-regulating the transcript levels of cold-responsive genes (Wang et al., 2020). In Camellia sinensis, CsWRKY6, CsWRKY31, CsWRKY48 were induced to be up-regulated under 4 °C cold treatment, indicating that they acted as positive regulators involved in the regulatory pathway of Camellia sinensis in response to cold (Wang et al., 2019). All these studies confirmed that WRKY TFs plays an essential role in defense against abiotic stresses.

Adversities such as low temperature, high temperature, drought, and salinity usually produce water stress in plants, and osmoregulation is one of the important physiological mechanisms for plants to resist such abiotic stresses. Plants through the regulation of various physiological metabolism in body accumulation of a wide range of organic or inorganic substances to increase the concentration of cell membranes, reduce the osmotic potential, and enhance the cellular water absorption or retention capacity. Sugars are an effective carbohydrate in plant response to abiotic stress, which not only keep the cellular osmotic balance, but also participate in the signaling molecules for the perception and conduction of adversity signals, and regulate the growth and development of plants and their ability to cope with adversity (Sun et al., 2015).

WRKY transcription factors are ubiquitously distributed across the plant kingdom and play pivotal roles in regulating plant growth, developmental programs, and stress-responsive mechanisms. In recent years, a growing body of research has focused on the mediation of abiotic stress by WRKY transcription factors through sugar metabolic pathways, with remarkable advancements achieved in research methodologies. Notwithstanding these progresses, this field still harbors significant prospects and unresolved research gaps that warrant systematic exploration.

First and foremost, future investigations should endeavor to elucidate in greater detail the specific molecular mechanisms underlying the interaction between WRKY transcription factors and sugar metabolic pathways. Although existing evidence has established that WRKY transcription factors modulate the expression of sugar metabolism-related genes, the intricate regulatory networks and precise target sites thereof remain incompletely characterized. To address this, future studies are expected to employ cutting-edge technical approaches, including gene-editing technologies (particularly multi-gene editing to circumvent functional redundancy) (Cao et al., 2025a), high-resolution protein-protein interaction analyses (such as in vivo co-immunoprecipitation, yeast two-hybrid library screening, and proximity labeling techniques) (Cao et al., 2024), and single-cell omics. These methodologies will facilitate the precise dissection of how WRKY proteins recognize and bind to the promoter regions of downstream sugar metabolism genes, as well as how their complexes with other transcription factors or coregulatory molecules exert fine-scale regulation over the activity of key enzymes, thereby influencing the dynamic homeostasis of critical sugar molecules.

Second, it is imperative to resolve the long-standing challenges of functional redundancy and specificity within the WRKY gene family. Comprising a large repertoire of members, the WRKY family often exhibits extensive functional redundancy or overlap, rendering traditional genetic approaches inadequate for accurately evaluating the contribution of individual members in sugar metabolism-stress response cascades. Moreover, distinct WRKY members may exhibit context-dependent functions under varying stress conditions, in different tissues/organs, or at specific developmental stages. Future research should integrate systems biology approaches with conditional gene-editing/inducible expression systems to meticulously dissect the specific roles of different WRKY members in regulating sugar metabolism under defined environmental and physiological contexts, along with the underlying molecular determinants.

Furthermore, more direct physiological and metabolic evidence is required to establish the causal relationship between WRKY-mediated sugar metabolism and enhanced stress tolerance. Current investigations predominantly focus on molecular-level analyses or terminal phenotypic observations, whereas the evidentiary chain for intermediate links remains fragmented. Specifically, following the regulation of specific sugar metabolism genes by WRKY, how do changes in sugar composition, concentration, spatiotemporal distribution, and cellular energy status directly impact key physiological processes, including stress signal perception, reactive oxygen species scavenging, osmotic adjustment, and maintenance of cell membrane integrity? Future studies should integrate metabolomics, enzyme activity assays, subcellular localization analyses, and live-cell imaging technologies to track, at high spatiotemporal resolution, how WRKY-mediated reprogramming of sugar metabolism translates into specific physiological and biochemical responses that underpin plant stress resilience.

In conclusion, the field of WRKY transcription factors mediating abiotic stress through sugar metabolic pathways presents substantial scope for advancement. Future research should prioritize the in-depth investigation of regulatory mechanisms, expansion of research frontiers, and comprehensive consideration of their roles across multiple metabolic networks, thereby fostering a holistic understanding of WRKY transcription factors in plant stress adaptation. Such endeavors are critical for the breeding of stress-tolerant crop varieties and the promotion of sustainable development in China’s forestry and agricultural sectors.