Introduction

Plants are sessile and highly sensitive to changing climatic conditions. Owing to climate change and the threat of global warming, it has been estimated that abiotic stresses such as drought, salinity, freezing, and extreme temperature fluctuations will affect commercial agricultural production by up to 50% by the end of this century (FAO 2015). Abiotic stresses can reduce horticultural crop production and cause yield losses ranging from 50% to 70% (Francini and Sebastiani et al. 2019). Salinity affects almost 20%–30% of arable soils (Thorne et al. 2020). Heat and drought severely impact plant growth and reproductivity due to reactive oxygen species (ROS) imbalance, cell damage, and protein degradation (Devireddy et al. 2021; Wang and Zhu 2022; Khan et al. 2022a). Plants have evolved various adaptive strategies to cope with long-term abiotic stresses through regulatory mechanisms. In this scenario, producing high-yield horticultural crop varieties requires an improved understanding of gene regulatory functions involving development and abiotic stress response.

Stress-tolerant plants display a vast network of regulatory mechanisms, including reprogramming the expression of various genes at the transcriptional and post-transcriptional levels. These regulations are essential for plants to restore cell homeostasis during recovery. Transcription factors (TFs) are prime players at the transcriptional and post-transcriptional levels (Kumar et al. 2021). Many important TFs, such as NAC, WRKY, bZIP, NF-Y, and ERF, have been identified through genome-wide studies (Wu et al. 2015; Banerjee and Roychoudhury 2017; Yang et al. 2018; Zhang et al. 2023). These TFs are involved in the responses of plants to abiotic stress and stress-specific transcriptional patterns linked to upstream signaling through TFs. Specific stresses such as drought, cold, and salinity can also induce common transcriptional responses (Ma and Bohnert 2007). For example, the Arabidopsis thaliana NFYA5 (nuclear factor Y) was strongly influenced by drought-induced stress using the abscisic acid (ABA)-dependent pathway. NFYA5 contains a miR169 binding site (CCAAT), which targets the translational repression of mRNAs; miR169 was downregulated by drought-induced stress in an ABA-dependent manner. NFYA5 regulated drought-induced stress at the transcriptional and post-transcriptional levels and induced drought tolerance (Li et al. 2008).

WUSCHEL-related homeobox (WOX) TFs also play an essential role in the transcriptional and post-transcriptional regulation of genes involved in the developmental processes in plants. In rice, OsWOX3B and OsSPL10 regulated the expression pattern of HEARY LEAF6 (HL6); OsWOX3B and OsSPL10 interact and subsequently impact the transcription of HL6, which is essential for developing trichomes (Liao et al. 2023). Trichomes play a positive role in providing resistance against biotic and abiotic stresses (Liao et al. 2023). Additionally, OsWOX3B and HL6 modulated the expression of various genes involved in auxin (indole acetic acid; IAA) biosynthesis and signaling, including AUXIN RESPONSE FACTOR 4 (OsARF4), PIN-FORMED1a (OsPIN1a), and Tryptophan aminotransferases 5 (OsYUCCA5). HL6 binds to the promoter of OsYUCCA5 and the OsWOX3B-HL6 interaction enhances the binding property (Sun et al. 2017). Current research on plant WOX TFs has focused on developmental regulation.

WOXs are differentially expressed under abiotic stresses in horticultural crops such as tomato (Solanum lycopersicum), citrus (Citrus sinensis), apple (Malus domestica), and banana (Musa acuminata) (Li et al. 2021; Khan et al. 2021; Chaudhary et al. 2022; Lv et al. 2023). For example, tomato SlWOXs showed robust, differential expression patterns under cold, NaCl, and drought predicting a significant role in abiotic stress response (Li et al. 2021). Overexpression of MdWOX13-1 in apple calli increased ROS scavenging and weight (Lv et al. 2023). MdWOX13-1 directly bound to the promoter of MdSOD and enhanced ROS scavenging in response to drought (Lv et al. 2023). Various gene regulatory mechanisms are involved in the fight for survival and play a significant role in the changes in horticultural plants during abiotic stresses.

Previous reviews have illustrated the responses of plants for survival under abiotic stresses (Estravis-Barcala et al. 2020; Saijo and Loo 2020; Khan et al. 2023a, b). Some abiotic stress-responsive families of TFs, such as WRKY, NAC, AP2/ERF, and MYB, are ideal candidates for genome editing and genetic improvement to enhance resistance against abiotic stresses (Wang et al. 2016). Thus, understanding the underlying molecular mechanisms in horticultural crop production is essential. The mechanism through which WOXs perform their functional roles, including interaction with partners to target promoters, is still not precise. Hence, this review focuses on the regulatory pathways behind the association of the WOX family and resistance abiotic stresses and development in horticultural plants. This can further demonstrate the functional identification of gene regulatory mechanisms to customize the genetic improvement in crops, providing a central platform for future research.

Identification and classification of WOX TFs

WOXs belong to the homeodomain (HD) family of TFs (Xu et al. 2019). They are divided into 14 subfamilies, including PINTOX, NDX (NODULIN homeobox), KNOX (KNOTTED like homeobox), BELL (BELL like homeodomain), WOX (WUSCHEL related homeobox), SAWADEE homeodomain, HD-ZIP I-IV (homeodomain leucine zipper), ZF-HD (zinc finger homeodomain), DDT (homeodomain-DDT), LD (luminidependens homeodomain), and PHD (plant homeodomain with a finger domain) (Jain et al. 2008; Mukherjee et al. 2009; Bürglin and Affolter 2016; Xu et al. 2019). HDs bind with DNA as monomers with high affinity mediated via interactions through the helix-turn-helix (HTH) structure. The HD in the N-terminal of WOXs is conserved in plants (Sun et al. 2023; Zhang et al. 2023; Galibina et al. 2023; Xu et al. 2023; Yang et al. 2023; Tang et al. 2023; Riccucci et al. 2023). The other regions of WOXs are highly divergent in their sequences. The C-termini of WOXs comprise a distinct WUS box motif “TLXLFP”, where X can be any amino acid that locates the C-terminal to the HDs and ERF-linked amphiphilic repression (EAR)-like motif “SLELRLN” (Park et al. 2005; van der Graaff et al. 2009; Zhang et al. 2010; Chen et al. 2023; Youngstrom et al. 2022). The WUS-box is specific to the WUS clade members and functions as an activator and contains a C-terminal EAR domain that involves transcriptional repression (van der Graaff et al. 2009; Mukherjee et al. 2009; Lin et al. 2013). EAR-motif interacts with TOPLESS (TPL)/TPL-related (TPR) corepressor to repress the transcription of auxin-responsive genes (Szemenyei et al. 2008). This family was identified in various horticultural plants and fruit-bearing trees (Table 1) (Khan et al. 2021; Xu et al. 2022; Chaudhary et al. 2022). Using phylogenetic analysis and evolutionary relationships, the WOX family is grouped into three clades: ancient, WUS/modern, and intermediate (Rahman et al. 2017; Alvarez et al. 2018; Chang et al. 2019; Tang et al. 2020; Daude et al. 2020; Khan et al. 2021; Feng et al. 2021; XU et al. 2022; Galibina et al. 2023; Xu et al. 2023; Yang et al. 2023; Tang et al. 2023; Riccucci et al. 2023) (Fig. 1). The ancient clade represents conserved WOXs found in the genomes of algae to angiosperms which includes three genes, WOX10, 13, and 14 in Arabidopsis. WOX8/WOX9 and WOX11/12 from the intermediate clade are involved in developmental processes such as embryogenesis and regeneration into Arabidopsis. The WOXs in the modern clade contain HD and WUS motifs, which are essential for normal functioning. They include WUS, WOX5, and WOX7, which contain the EAR-motif domain with specific repressor activity (Feng et al. 2021; Li et al. 2022; Yang et al. 2022; Sun et al. 2023; Zhang et al. 2023).

Table 1 The number of WOXs identified in plants and fruit trees
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Fig. 1
figure 1

A midrooted phylogenetic tree of the WUSCHEL-related homeobox (WOX) transcription factor family using various classified plant species such as Arabidopsis, strawberry (Fragaria vesca), sweet orange (Citrus sinensis), rice (Oryza sativa L.), and wheat (Triticum aestivum L.) (Khan et al. 2021; Yang et al. 2022; Li et al. 2020) was constructed using Clustal Omega (www.ebi.ac.uk/Tools/msa/clustalo/). The tree was drawn using Interactive Tree of Life (IToL) v. 6 (https://itol.embl.de/). Scale bars correspond to 0.1 substitutions

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In Arabidopsis, 15 WOXs that synergistically participate in the regulatory mechanisms of various developmental processes, such as stem cell proliferation and maintenance, shoot apical meristem (SAM), and root apical meristem (RAM) development, and organ formation (Haecker et al. 2004; van der Graaff et al. 2009). Recently, 127 WOXs have been identified in eleven cucurbit crops such as snake gourd (Trichosanthes anguina), monk fruit (Siraitia grosvenorii), chayote (Sechium edule), wax gourd (Benincasa hispida), sponge gourd (Luffa cylindrica), bottle gourd (Lagenaria siceraria), bitter gourd (Momordica charantia), pumpkin (Cucurbita maxima), melon (Cucumis melo), watermelon (Citrullus lanatus), and cucumber (Cucumis sativus) (Li et al. 2023). WOXs have also been identified in the genomes of other horticultural plants and woody perennials (Table 1). An overview of WOXs involved in plant growth and development in model plants is presented in Fig. 2.

Fig. 2
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A graphic representation of the role of the WUSCHEL-related homeobox (WOX) transcription factor family in plant development

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WOX TFs are crucial for plant development

Classically, developmental biology studies have mainly focused on Arabidopsis as a model plant. However, much progress has been made in analyzing the functions of various WOXs in different horticultural plants and woody perennials (Table 2). Generally, the WOX family plays a crucial role in shoot apical meristem (SAM) development, floral meristem identity, stem cell maintenance, flower organ formation, lateral root (LR) formation, cell differentiation, somatic embryogenesis, and somatic embryo development (Klimaszewska et al. 2011; Tvorogova et al. 2021; Willoughby and Nimchuk 2021). The WOX family regulates developmental processes-related regulatory mechanisms and is well-documented in model plants (Fig. 2). The combined activities of WOXs regulated tissue proliferation and embryogenic development in Arabidopsis (Wu et al. 2007). AtWUS was involved in stem cell and floral meristem identities and regulated SAM maintenance (Laux et al. 1996; Mayer et al. 1998). The AtWUS homolog in pineapple (Ananas comosus L.) AcoWUS is highly conserved functionally and significantly regulates female gametophyte development. Moreover, WUS positively regulated somatic embryogenesis in coffee (Coffee canephora) (Arroyo-Herrera et al. 2008) and dedifferentiation during somatic embryogenesis in coconut (Cocos nucifera) (Khan et al. 2023a, b). C.sinensis CsWUS stimulates stem cell proliferation in Carrizo citrange, whereas it regulates floral organ development in tobacco (Zhang et al. 2020; Khan et al. 2021). CsWUS-silencing in lemons induced thorn development and upregulated the expression of thorn identity-related genes (Khan et al. 2021). A recent study revealed that radish (Raphanus sativus) RsWUS plays an important role in shoot development. The RESPONSE REGULATOR 18–1 (RsRR18-1) encoded protein binds to the RsWUSb promoter and activates its expression. RsRR18-1-WUSb modulated shoot development in radish through the cytokinin (CK) signaling pathway (Hu et al. 2024). The Loquat (Eriobotrya japonica) EjWUSa when overexpressed in Arabidopsis promoted early flowering (Yu et al. 2022). AtWOX1 regulated meristem and leaf blade development via the modulation of CLAVATA3 (CLV3) expression (Vandenbussche 2021). Loss of function wox1 mutation reduced leaf blade in Petunia and Arabidopsis (Vandenbussche et al. 2009). PpWOX1 controlled cell division during the early stage of fruit development in pears (Pyrus pyrifolia) (Jiang et al. 2018). CsWOX1 regulated early reproductive development in cucumber and directly interacted with SPOROCYTELESS (CsSPL). CsWOX1 stimulated sporogenesis through the CsSPL-based signaling pathway and modulated IAA signaling in cucumber (Niu et al. 2018). AtWOX2 marked the apical cell line during embryo development and is highly expressed in the egg cell and zygote (Haecker et al. 2004). AtWOX4 regulated cell division in vascular tissues, and OsWOX4 regulated early leaf development in rice (Etchells et al. 2013; Yasui et al. 2018). In grapevine (Vitis vinifera), VvWOX4 regulated stem cells (Ru et al. 2011). In blueberry (Vaccinium corymbosum L.), the expression of VcWOX4b was enhanced in the shoots and roots compared to other VcWOXs. Further, VcWOX4b-overexpression in tobacco inhibited adventitious root formation by modifying vascular cell division and differentiation. VcWOX4b regulated CK- and IAA- stimulated primary xylem cell differentiation by inhibiting adventitious root (AR) formation (Gao et al. 2021). JrWOX5, 9, and 11 play an essential role in AR formation and determining root architecture in walnut (Juglans regia L.) (Chang et al. 2019; Chang et al. 2022). Apple (M. domestica) MdWOX4 and MdWOX4-2 are essential for AR and shoot development (Xu et al. 2022; Dong et al. 2022). AtWOX5 is involved in RAM development; wox5 mutation is involved in the reduction of LR development, enlargement and differentiation of columella cells, and the quiescent center (QC) (Sarkar et al. 2007). AtWOX6 regulated the differentiation of megaspore mother cells and proliferation of internal integument and floral primordial cells (Park et al. 2005). AtWOX7 is involved in initiating LR growth (Kong et al. 2016). AtWOX8 and 9 are involved in embryogenic development and maintain the basal and apical embryo lineages (Wu et al. 2007). Loss of function in AtWOX8 and 9 causes abnormal cell division in the apical and basal domains of Arabidopsis plants (Breuninger et al. 2008). Similarly, grapevine VvWOX9, VvWOX2, and VvWUS are also involved in somatic embryogenesis (Gambino et al. 2011). The cucumber CsWOX9 regulated the formation of branches, rosette leaves, and shorter siliques in Arabidopsis (Gu et al. 2020). In Lily (Lilium lancifolium), overexpression of LlWOX9 and 11 in stem segments promoted, whereas silencing them inhibited bulbil formation; CK-type B-response regulators bound to the promoters of LlWOX9 and 11 and upregulated their expression (He et al. 2022). In MdWOX11-overexpressing (OE) transgenic plants, AR formation was inhibited; further analysis revealed that the endogenous levels of CK, IAA, and ABA were upregulated in MdWOX11-RNAi than in MdWOX11-OE transgenic plants (Mao et al. 2022).

Table 2 The substantial role of the WOX genes in woody perennials and fruiting trees
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In Arabidopsis, AtWOX11 and 12 induced de novo root organogenesis and LR formation (Baesso et al. 2018; Liu et al. 2014), while AtWOX13 was involved in fruit development and regulated replum (Romera‐Branchat et al. 2013). However, OsWOX13 in rice was involved in abiotic stress tolerance and early flowering (Minh-Thu et al. 2018). AtWOX14 stimulated the development of conductive tissues and regulated flowering. Loss of function wox14 mutation led to dwarfism and delayed flowering. AtWOX14/4 regulated the proliferation of cells in the vascular tissue (Denis et al. 2017), demonstrating that WOX TFs had species-specific functional and developmental roles. This reason strongly favors the idea that plant development biology in common would be beneficial by acting on multimodal approaches.

Regulatory mechanisms of WOX TFs in response to abiotic stresses

Abiotic stresses impede the development and growth of plants. As WOXs are involved in multiple aspects of plant development and stress responses, an in-depth research is necessary. Moreover, numerous hormones responsive motifs, ABRE abscisic acid-responsive motif, CGTCA-methyl jasmonate responsive motif, ERE-ethylene responsive motif, gibberellic acid responsive motifs (P-box, GARE-motif, and TATC-box) were identified in the promoters of WOXs. Auxin-responsive factors (ARFs) and the AUX/IAA-ARF pathway controlled the expression of WOXs by binding to Auxin Response Elements (AuxREs) in the WOX promoters (Ulmasov et al. 1997; Tiwari et al. 2003; Guan et al. 2017). CK triggered WUS expression via binding to the type-B ARABIDOPSIS RESPONSE REGULATORs (B-ARRs) to the B-ARR element in the WUS promoters (Wang et al. 2017). WOX1 is involved in IAA signaling, biosynthesis, and transport. WOX1 positively regulated AUX1 and PIN1, whereas it negatively regulated TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA)/YUCCA5 (YUC5) and Tryptophan aminotransferase related 2 (TAR2) (Nakata et al. 2018). B-ARRs (ARR10) bound to the B-ARR motif in the promoters of WOX11 and 12 (Zubo et al. 2017). Abiotic/biotic stress-responsive cis-regulatory elements (TC-rich repeats, LTR, and MBS) were also found in the WOX promoters (Chaudhary et al. 2022; Wang et al. 2019; Li et al. 2021; Khan et al. 2021; Akbulut et al. 2022). Thus, WOXs TFs are active in abiotic stress response in plants.

Expression and regulatory role of WOX TFs in response to salinity

The differential expression pattern of WOXs in response to abiotic stresses has been reported in many plants (Wang et al. 2019; Li et al. 2020, 2022; Khan et al. 2021; Chaudhary et al. 2022). Banana (M. acuminata) is a highly salt-sensitive crop, and MaWOXs are essential in the development and abiotic stress response. MaWOX11 induced tolerance against drought in transgenic rice plants (Cheng et al. 2016). The expression of MaWOX1, 3, and 9a was markedly enhanced under drought. Furthermore, those of MaWOX3, 8a, and 11b were higher under 12 h of salinity treatment, while those of MaWOX were lower under cold-induced stress (Chaudhary et al. 2022). Expression patterns of SlWOX3a, 3b, 4, 5, and 13 significantly changed under 1 h of treatment with NaCl, indicating that they may mediate NaCl-induced stress in tomato plants (Li et al. 2021).

JrWOX11 expression was unexpectedly induced after NaCl, ABA, and PEG treatments, indicating that it was highly responsive to salt- and osmotic-state-related stress. Overexpression of JrWOX11 enhanced AR formation in walnuts (J. regia L.) and abiotic stress tolerance in 84 K poplar (Chang et al. 2022). OsWOX11 bound to the cis-regulatory “TTAATGG/C” motif and directly activated the transcription of OsLOB16, OsASR3, and OsFRDL1. WOX11 functioned intricately with stress-related genes, such as OsWRKY24, OsTCP21, OsMTN3, OsERF922, and OsPP2C8 (Jiang et al. 2017). Moreover, the AP2/ERF-type gene ETHYLENE RESPONSE FACTOR 3 (ERF3) was expressed during crown root development and interacted with WOX11. Both ERF3 and WOX11 target the CK signaling-related type type-A ARABIDOPSIS RESPONSE REGULATORS (A-RR2) gene. CK and IAA regulated WOX11 expression, and ERF3 regulated the expression of CK- and auxin-related genes. ERF3 directly targeted RR2 through the ERF binding site “GCCGCC” in its promoter and positively regulated its expression during root development (Zhao et al. 2015; Jiang et al. 2017). Moreover, WOX11 was induced upon exogenous treatment with CK and directly inhibited the expression of RR2. The expression of CK-responsive genes elevated in the crown root tips of wox11 mutants and WOX11 played an essential role in modulating the CK-based signaling and stress response (Jiang et al. 2017).

PagWOX11/12a regulated the genes involved in redox processes; PagWOX11/12a binds to the promoter of PagCYP736A12 and regulates its expression (Fig. 3). PagWOX11/12a-overexpression lines of poplar showed increased salt tolerance via ROS scavenging by directly regulating PagCYP736A12 (Wang et al. 2021). SMALL AUXIN UP RNA36 (SAUR36) related to the early auxin-inducible gene family encodes an auxin-responsive protein involved in AR formation in poplar via auxin signaling under salt stress. Moreover, PagWOX11/12a bound to the WOX-binding motif “TTAATGG” located in the promoter of SAUR36, regulating its transcription, which increased during salt-induced stress (Liu et al. 2022). Overexpression or RNAi of PagWOX11/12a-PagSAUR36 revealed that this module was essential for AR development during salt-induced stress via the IAA pathway (Liu et al. 2022). Further, identifying the regulatory mechanisms and target genes of the abiotic stress-responsive WOXs may unravel novel signaling pathways and help better understand the molecular mechanisms involved in response to abiotic stress.

Fig. 3
figure 3

Effect of WUSCHEL-related homeobox (WOX) transcription factors in abiotic stress tolerance in trees. OsWOX11, Oryza sativa L. WOX; PagERF, Populus alba × P. glandulosa ETHYLENE RESPONSE FACTOR 3; MdWOX, Malus domestica WOX; CsRAP2.12 (Cs1g16690), Citrus sinensis AP2/ERF; CLV, CLAVATA3; OsLOB16, Os LATERAL ORGAN BOUNDRY 16; OsASR3, abiotic stress responsive rice 3; OsFRDL1, Os FERRIC REDUCTASE DEFECTIVE LIKE 1; PagCY736A12, cytochrome P450 CYP736A12; SAUR36, SMALL AUXIN UP RNA 36; OsDREB1A, dehydration-responsive element-binding protein 1A; MdMnSOD, Malus domestica manganese superoxide dismutase; CsWUS, WUSCHEL; CK, cytokinin

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Expression and regulatory role of WOX TFs in response to drought

During floral inductive water deficit conditions in sweet orange (Citrus. sinensis), CsWUS, CsWOX6, and CsWOX11 were not expressed; CsWOX1, 3, 4, and 5 were slightly expressed at the beginning of water deficit (Khan et al. 2021); and CsWOX13 was upregulated (Khan et al. 2022a). In tomato, SlWOX1, 3a, 3b, 4, 5, and 9 were upregulated under drought treatment for 3 h (Li et al. 2021).

In tea plants, CsWOX13, 14, and 15 were positively upregulated under drought- and cold-induced stress (Wang et al. 2019). The AP2/ERF family member, CsRAP2.12 (Cs1g16690), encodes a TF that binds to the “GGCGGCC” cis-element in the promoter of CsWUS to regulate its expression. CsRAP2.12 was also upregulated in sweet oranges under floral inductive water deficit conditions (Khan et al. 2021). WOX12, a close homolog of WOX11, is the primary regulator of AR formation in plants (Tvorogova et al. 2021). Very little is known about the identity of the downstream target genes of WOX TFs, as only a few studies have addressed the issue. For example, in Poplar, PagWOX11/12a was involved in drought tolerance by regulating root development; PagERF35 bound to the drosophila DNA replication-related element (DRE) motif (TATCGATA) in the promoter of PagWOX11/12a and regulated its expression; and drought induced a higher expression of PagWOX11/12a and PagERF35 (Wang et al. 2020). Identifying the downstream targets of WOXs would be highly useful as it would help reveal the specific role of WOXs in the gene regulatory mechanism involved in abiotic stress tolerance in plants.

The WOXs overlap in abiotic stress responses and plant development markedly. Thus, overexpression in plants may offer various benefits. MdWOX13-1-encoded protein directly binds with the “TTAATGG” element in the MdMnSOD promoter, increasing drought tolerance by scavenging ROS. The activities of the antioxidant enzymes SOD, POD, and CAT enhanced in transgenic apple calli than in the wild type (WT). Overexpression of MdWOX13-1 increased calli weight and promoted ROS scavenging, providing resistance against drought-induced stress (Lv et al. 2023). OsWOX13 improved drought tolerance and promoted early flowering in rice (Minh-Thu et al. 2018). OsWOX13 directly bound to the cis-regulatory “ATTGATTG” motif. The promoters of drought-responsive-TF encoding genes, such as OsDREB1A and 1F, contained the “ATTGATTG” motif. In rice, the relative expression of OsDREB1A and OsDREB1F was positively upregulated during drought in OsWOX13-overexpressing plants, thereby enhancing drought tolerance. OsWOX13 also promoted early flowering by activating OsMADS16 and Hd3a. The promoters of these genes consisted of the “ATTGATTG” motif, indicating that OsWOX13 is involved in drought tolerance and floral induction (Minh-Thu et al. 2018).

Expression and regulatory role of WOX TFs in response to freezing and heat-induced stress

WOXs also regulate the response of plants to temperature fluctuations. WOXs were upregulated under heat-induced stress in pineapple (A. comosus L.). AcoWOX13 was highly expressed at 24 h of heat treatment (Rahman et al. 2017). High expression of osmotically responsive genes 9 (HOS9) encodes an HD-TF and shares a highly similar motif with Arabidopsis WUS and PRESSED FLOWER (PRS). Arabidopsis hos9-1 mutants revealed an improved expression of cold-responsive genes. Cold susceptibility of hos9-1 mutants revealed a disruption of functions in those genes post-transcriptionally targeted by HOS9 or other than those targeted by C-repeat dehydration-responsive element binding factor (CBF)-encoding genes. CBFs control the hos9-1 mutation. HOS9 plays a significant role in cold tolerance by regulating the kind of genes but is not a part of the CBF pathway (Zhu et al. 2004). In paper mulberry, the expression of five WOXs that may be essential in cambial development was significantly induced after cold exposure (Peng et al. 2015). The OsWOX11-target genes and a NAC-TF-encoding gene (OMTN3) were associated with cold tolerance (Fang et al. 2014). OsTCP21 and OsERF922 were negative modulators of cold and salinity response in plants (Liu et al. 2012). Recent studies have proposed WOXs as promising candidate genes for manipulating abiotic stress tolerance in plants that can be used for genetic improvement.

The expression patterns and regulatory role of WOX TFs in response to heavy metal-induced stress

Cd is a toxic heavy metal that is highly soluble in water.

Cd is absorbed by the roots and translocated to the aerial parts of plants via xylem loading, leading to physiological, biochemical, and genetic damage (Song et al. 2017). The PsnWOX family plays a crucial role in CdCl2-induced stress. The expression of PsnWOX13a and PsnWOX13b in Populus × xiaohei T.S. Hwang et Liang was positively regulated during the early stage of CdCl2 treatment (Li et al. 2022). WUS, CLV3, and WOX5 were involved in stem cell maintenance and control of SAM and RAM development in plants. Cd inhibited primary and regulated lateral root growth in Arabidopsis. A short treatment with Cd (100–150 µM) for 24 h altered the RAM and SAM. Cd-induced coexpression of WUS and WOX5 and accumulation of CK played a significant role in SAM and RAM activity (Leonardo et al. 2021). Further, the role of stress-responsive WOXs and their regulation must be identified to understand the signaling pathway involved in abiotic stress tolerance.

Conclusions

The response of plants to various abiotic and biotic stresses critically depends on the transcriptional regulation of stress-responsive genes. In the last few years, significant progress has been made in identifying the TFs involved in the expression of genes relevant to stress in horticultural plants. To date, several members of the WOX family of TFs have been identified and functionally studied in plants. Increasing genome sequencing in plants and data availability has provided a basis for genome-wide identification, screening, and expression analysis of genes involved in abiotic stresses. WOX homologs have species-specific functions in plants. However, the studies regarding the functional characterization of WOXs using genetic transformations and in vitro regeneration in trees are limited. Previous studies have relied on the coexpression patterns of WOXs, which may affect the accurate determination of gene function. WOXs are involved in the transcriptional activation of stress-related genes. The regulation of their interactions and the identification of new partners require further investigation. Only a few overexpression and genetic mutation studies of specific genes have explored the variety of WOXs in different plant species. Significant evidence indicates the convergence of WOXs during abiotic stress tolerance in plants. WOXs play crucial roles in abiotic stress responses and are potent targets for modifying abiotic stress tolerance in horticultural plants.

CRISPR/Cas9 technology is a valuable tool for genetic improvement in woody perennials (Khan et al. 2022b), and targeted sequence insertion or deletion can modify the expression patterns of TFs. A functional comparison of the WOX orthologs in diverse plant species and its application in constructing WOX mutants by CRISPR/Cas9-based genome editing will help achieve sustainable production goals. Notably, gene editing in horticultural crops could encompass abiotic stress resilience and increased yield for food security. Here, we propose that WOXs synchronize the link between stress and metabolic regulation; the stresses included in this review involve WOXs as significant actors. However, the precise molecular process and equilibrium between defense and growth are mostly unclear. During an abiotic stress response, the WOXs and their target genes may lead to identifying novel signaling pathways. Finally, it dissects the functional role of WOXs in developing stress-resilient crops that can significantly improve agriculture crop production under the climate change framework.