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WRKY Transcription Factor Responses and Tolerance to Abiotic Stresses in Plants

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02 June 2024

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03 June 2024

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Abstract
Plants are subjected to abiotic stresses throughout their developmental period. Abiotic stresses include drought, salt, heat, cold, heavy metals, nutritional element and oxidative stresses. Improving plant response to various environmental stresses is critical for plant survival and perpetuation. The WRKY transcription factors have special structure (WRKY structural domains), which enable WRKY transcription factors to have different transcriptional regulatory functions. The WRKY transcription factors can not only regulate abiotic stresses response and plant growth and development by regulating phytohormone signalling pathways, but also promote or suppress the expression of downstream genes by binding to the W-box [TGACCA/TGACCT] in the promoters of their target genes. In addition, WRKY transcription factors not only interact with other families of transcription factors to regulate plant defence responses in abiotic stresses, but also self-regulate by recognizing and binding to W-boxes in their own target genes to regulate their defence responses to abiotic stresses. However, in recent years, research reviews on the regulatory roles of WRKY transcription factors in higher plants are scarce and shallow. In this review, we focus on the structure and classification of WRKY transcription factors, as well as the identification of their downstream target genes and molecular mechanisms involved in the response to abiotic stresses, which can improve the tolerance ability of plants in abiotic stress and we also look forward to their future research directions, with a view to providing theoretical support for the genetic improvement of crop abiotic stresses tolerance.
Keywords: 
WRKY transcription factor
;  
abiotic stress response and tolerance
;  
target gene
;  
plant growth and development
Subject: 
Biology and Life Sciences  -   Biochemistry and Molecular Biology

1. Introduction

Food is an indispensable and important resource in human life, and it carries people's survival and development. From planting to harvesting, from processing to consumption, food accompanies the historical process of mankind and profoundly affects the way of life and social structure of mankind. Food is the basic guarantee for human survival [1]. As one of the most important sources of food for human beings, grain provides the nutrition and energy needed by the human body and maintains its normal physiological functioning. Whether it is rice, wheat, corn or other grains, they are all important foods indispensable to human survival, providing humans with a wealth of carbohydrates, proteins and a variety of vitamins [2]. Finally, the food industry is also an important pillar of employment and economic development for human society. The production, processing and distribution of food involves a large number of practitioners and related industrial chains, creating enormous employment opportunities and economic benefits for society. The healthy development of the food industry is directly related to the prosperity and stability of national and regional economies [3]. In short, guaranteeing the stability of food production and supply, promoting the inheritance and innovation of food culture, and developing the food industry are all important guarantees for the sustained and stable development of human society [4].
Plants are subjected to a variety of stresses during growth and development, such as drought, temperature extremes, pests and diseases, etc., of which abiotic stresses are the major threats affecting the growth of food crops [5,6,7,8]. Currently, numerous studies have been conducted on the response of plants to abiotic stresses, for example, the response to cold temperature stress, drought stress, salt stress, heavy metal stress, etc [9,10,11,12]. The studies have been deepened to the level of molecular mechanisms, and the WRKY transcription factors, which are one of the largest families of transcription factors in plants, have gained great attention. Nowadays, a large number of WRKY transcription factor genes have been identified, and they are widely involved in the regulation of plant secondary metabolism, abiotic stress, growth and development [13,14,15]. Su et al. identified a WRKY group IIc transcription factor MdWRKY75, it is located in the nucleus. Overexpression of MdWRKY75 promoted anthocyanin accumulation in apple (Malus Domestica L.) 'Orin' callus. Anthocyanins play an important role in plant secondary metabolism, and MdWRKY75 stimulates anthocyanin accumulation mainly by binding to the promoter of the MYB transcription factor MdMYB1 [16]. Gentiana macrophylla is one of Chinese herbal medicines in which loganic acid and gentiopicroside, and kinds of iridoids or secoiridoids have been identified as major medicinal secondary metabolites. A total of 12 GmWRKYs were identified to be involved in the biosynthesis of secoiridoid, of which 8 genes GmWRKY1, GmWRKY6, GmWRKY12, GmWRKY17, GmWRKY33, GmWRKY34, GmWRKY38, and GmWRKY39 were found to regulate the synthesis of gentiopicroside and 4 genes were found to be involved GmWRKY7, GmWRKY14, GmWRKY26 and GmWRKY41 regulate strychnic acid synthesis [17]. Zhang et al. identified a WRKY transcription factor OsWRKY63 negatively regulates cold tolerance in Oryza sativa. Overexpression of OsWRKY63 lines were more sensitive to cold stress, and the knockout mutant line showed higher cold tolerance. OsWRKY63 was able to repress the expression of OsWRKY76, and the OsWRKY76-knockout mutant lines showed significantly lower cold tolerance and suppressed cold-induced expression of the five OsDREB1 genes [18]. Ma et al. found that the tomato WRKY transcription factor SlWRKY57 acts as a negative regulator in salt stress response by directly attenuating the transcription of salt-responsive genes (SlRD29B and SlDREB2) and an ion homeostasis genes (SlSOS1) [19]. Devaiah et al. found WRKY75 was located in the nucleus and was differentially induced in plants during phosphate (Pi) deficiency. When WRKY75 expression was inhibited, the expression of several genes involved in the Pi starvation response decreased, and lateral root length and number as well as the number of root hairs increased significantly [20]. Because of the important role of WRKY transcription factors in the regulation of abiotic stress and plant growth and development, it has become a popular gene family for plant stress breeding research.
This paper reviews the structural domains and classification of WRKY transcription factors, that transcriptional regulation downstream genes are involved in the response to abiotic stress. In the future, we can focus on studying WRKY transcription factors as a signal regulatory gene network in response to abiotic stress, and we also look forward to their future research directions, with a view to providing theoretical support for the genetic improvement of crop abiotic stresses tolerance.

1.1. Structural Domains and Classification of WRKY Transcription Factors

WRKY is a family of transcription factors unique to plants and defined as WRKY transcription factors because of their protein sequences contain a DNA binding domain with the highly conserved amino acid sequence WRKYGQK at the N-terminus of the domain [21]. However, in a few WRKY proteins, there are different types of mutations in the WRKYGQK amino acid sequence, mainly WRKYGEK, WRKYGMK, WRKYGKK, WSKYEQK or WIKYGEN (Figure 1). The WRKY transcription factors proteins are usually composed of 60 amino acids, and this sequence recognises the W-box [TGACCA/TGACCT] and some similar W-boxes containing the TGAC core structure in the homeopathic element, and specifically binds to them to regulate the downstream target genes [22,23]. The neighbouring sequences of the TGAC core structure determine the priority of WRKY transcription factor binding sites [24]. A large number of previous studies have shown that most of the promoters of genes related to abiotic stresses contain more than one W-box sequence, which explains the ability of the WRKY family of transcription factors to be widely involved in the regulation of the expression of many plant abiotic stress-related genes [25] (Table 2).
Typically, WRKY transcription factors contain at least one WRKY structural domain at the N-terminal end and an atypical zinc finger structure at the C-terminal end [26]. Based on the number of WRKY-binding domains and the characteristics of the zinc finger-like motifs, they can be classified into three groups: Group I contains two WRKY-binding domains with C2-H2 motifs (C-X4-5-CX22-23-H-X1-H); Group II contains one WRKY-binding domain with C2-H2 motifs. Group II can be generally divided into five subgroups (II a, II b, II c, II d and II e). Group III contains a WRKY-binding domain and a different zinc finger-like motif, C2-H-C (C-X7-C-X23-H-X1-C). Analyses based on phylogenetic data indicate that WRKY families in higher plants are more accurately classified into groups I, II a+II b, II c, II d+II e, and III, whereas [27,28] (Figure 2).
Table 1. The WRKYs genes total numbers in different plants.
Table 1. The WRKYs genes total numbers in different plants.
Gene name Species Total number Reference
AtWRKYs Arabidopsis thaliana 74 [29]
OsWRKYs Oryza sativa 100+ [30]
GmWRKYs Glycine max 197 [31]
HvWRKYs Hordeum vulgare 45 [32]
CsWRKYs Cucumis sativus 55 [33]
SlWRKYs Solanum lycopersicum 81 [34]
PgWRKYs Panax ginseng 118 [35]
VuWRKYs Vigna unguiculata 92 [36]
HvWRKYs Hordeum vulgare 86 [37]
IbWRKYs Ipomoea batatas 84 [38]
PhWRKYs Petunia hybrida 79 [39]
TkWRKYs Taraxacum kok-saghyz 72 [40]
SbWRKYs Scutellaria baicalensis 72 [41]
HuWRKYs Hylocereus undulatus 70 [42]
DcWRKYs Daucus carota 67 [43]
XsWRKYs Xanthoceras sorbifolium 65 [44]
KoWRKYs Kandelia obovata 64 [45]
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Figure 1. Conserved domains of WRKY family transcription factors in Glycine max, Arabidopsis thaliana and Oryza sativa. These asterisks “*”and red frame above the maps indicate the domain of conservative cysteine (C), cysteine (C), histidine (H) and cysteine (C), respectively.
Figure 1. Conserved domains of WRKY family transcription factors in Glycine max, Arabidopsis thaliana and Oryza sativa. These asterisks “*”and red frame above the maps indicate the domain of conservative cysteine (C), cysteine (C), histidine (H) and cysteine (C), respectively.
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Figure 2. Domain structure of different WRKY subfamilies in higher plants. The WRKY motif, the cysteines, and histidines that form the zinc finger are shown in boxes. The 4 β-strands are shown with dashed arrows.
Figure 2. Domain structure of different WRKY subfamilies in higher plants. The WRKY motif, the cysteines, and histidines that form the zinc finger are shown in boxes. The 4 β-strands are shown with dashed arrows.
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1.2. W-Box cis-Element in the Promoter Region of WRKY Downstream Genes

It has been shown that WRKY transcription factors can specifically bind to DNA through the cis-acting element W-box (5'-[TGACCA/TGACCT]-3') in the promoters of target genes to regulate the expression of related genes and affect plant in abiotic stresses, plant growth and development. The core sequence of the W-box is "TGAC", so the W-box can be used for the prediction of the target genes of WRKY transcription factors [21]. Different WRKY transcription factors bind different sequences near the W-box, which affects the selectivity and strength of WRKY transcription factor binding [46]. Mutations in the conserved sequence WRKYGQK in the WRKY structural domain or change any nucleotide in the W-box reduce the binding activity of WRKY transcription factor to DNA, whereas substitution of conserved cysteine (Cys) and histidine (His) residues in the C-terminal zinc finger structure removes their DNA-binding activity [47].

2. Response and Tolerance of WRKY Transcription Factor Family to Abiotic Stresses in Plant

Plants may encounter the effects of a wide range of abiotic stresses during growth and development, including drought, temperature extremes (high temperature and low temperature), salinity, heavy metal stresses and nutrient deficiencies. With climate change and increasing weather extremes, the impact of abiotic stresses on crops production is increasing, leading to growth retardation, quality deterioration and yield reduction [48,49]. Under abiotic stresses conditions, the WRKY transcription factors activate or suppress the transcription of downstream genes to regulate the expression of abiotic stress responsive genes or direct regulation of abiotic stress response gene expression, activate the defence mechanism against abiotic stresses in crops, and improve crops resilience to ensure grain yield under abiotic stresses [50,51].

2.1. Molecular Mechanisms of WRKY Transcription Factors Associated with Dought Stress

Drought is one of the major environmental factors affecting plant growth and development and crop yield (Figure 3). Many WRKY transcription factors genes have been identified to regulate drought tolerance in plants, and overexpression line or knockdown line of these WRKY genes has improved drought tolerance and even seed yield in Arabidopsis thaliana, Nicotiana tabacum, Glycine max, Oryza sativa, Triticum, Cotton [48,49,50]. It has been shown that WRKYs can improve plant tolerance to drought stress by reducing H2O2 content through the Reactive oxygen species (ROS) scavenging system. For example, overexpression of MdWRKY70L in Nicotiana tabacum reduced H2O2 and O2- accumulation and enhanced drought tolerance in transgenic plants [52]. Overexpression of the GmWRKY17 enhances drought tolerance in soybean, and it positively regulates drought tolerance in soybean by activating the expression of the drought-inducible gene GmDREB1D and the abscisic acid (ABA)-associated gene GmABA2 through combining their promoters [53]. Duan et al. found transcript abundance of MdWRKY56 was up-regulated under drought stress. MdWRKY56 overexpressed line exhibited lower electrolyte leakage, malondialdehyde (MDA) content and ROS accumulation, proline content and antioxidant enzyme activities [54]. Zhang et al. found ChaWRKY40 may enhance hazelnuts drought tolerance by positively regulating ChaP5CS gene expression to increase proline content. In the wild type, the expression of ChaWRKY40 and ChaP5CS increased with the increase of PEG-6000 concentration in the leaves and the gradual decrease of the relative water content of the leaves [55]. Wang et al. found the WRKY transcription factor EjWRKY17 was identified in Eriobotrya japonicaloqua, which was significantly up-regulated in leaves by melatonin treatment during drought stress. Overexpression of EjWRKY17 line was able to increase drought tolerance in plants, which had low water loss, limited electrolyte leakage, and lower levels of ROS and MDA compared to the wild type [56]. Huang et al. found MfWRKY40 promoted primordial root length elongation, increased water uptake, and reduced water loss under stress, and the antioxidant capacity of the overexpression lines was also significantly enhanced, as evidenced by higher chlorophyll content and antioxidant enzyme activities, and less malondialdehyde and ROS accumulation [57].
Drought is one of the major abiotic stresses that limit plant growth and development and reduce crop yield. Many members of the WRKY transcription factor family have been found to be able to respond to drought stress by binding downstream to the W-box element in the promoter region of drought stress-related genes and regulating the expression of the genes, which ultimately improves the ability of plants to cope with drought stress.

2.2. WRKY Transcription Factors Involved in Response to Temperature Stress

Temperature is considered the major abiotic stress for plants. Extreme high or low temperatures can lead to severe effects on plants, resulting in plant mortality and extensive agricultural economic losses. It is therefore important to increase the tolerance of plant cells to drastic changes in temperature and is necessary to protect food production. WRKY transcription factors help plants to resist temperature changes by regulating the expression of genes involved in temperature stress, and they also respond to extreme temperatures by regulating the expression of genes involved in ABA response [58,59,60].

2.2.1. WRKY Transcription Factors and High Temperature Stress

When the temperature exceeds the maximum upper limit of the temperature to which the plant can adapt, it has an injurious effect on the plant and stunts its growth and development. High can also weaken photosynthesis and enhance respiration, causing plants to over-consume their own energy and causing them to die from long-term starvation. High temperatures can also disrupt the water balance of plants, leading to the accumulation of harmful metabolites in the body. Therefore, high temperature is very important for the normal growth and development of plants. Nowadays, more and more researchers are focusing on high temperature stress in the their study [61,62]. He et al. found the WRKY transcription factor TaWRKY1 and TaWRKY33 was identified in Triticum aestivum L. Overexpression of TaWRKY33 lines showed enhanced heat stress tolerance. TaWRKY1 was slightly up-regulated by high temperature and ABA and down-regulated by low temperature. TaWRKY33 was involved in the response to high and low temperatures. Overexpression of TaWRKY1 and TaWRKY33 activated several stress-related downstream genes and promoted root growth in Arabidopsis under various stresses [63]. Wang et al. identified a WRKY family transcription factor SlWRKY3 that was induced and up-regulated under heat stress, whereas a knockout strain of wrky3 resulted in reduced heat stress tolerance. Overexpression of SlWRKY3 accumulated less ROS, whereas wrky3 knockout lines accumulated more ROS under heat stress. They concluded that SlWRKY3 activated the expression of a range of abiotic stress-responsive genes involved in ROS scavenging [64]. Wu et al. performed transcriptome analysis of lily (Lilium longiflorum) and identified the a WRKY family transcription factor gene LlWRKY22, which was activated for expression at high temperatures, and overexpression of LlWRKY22 in Lilium longiflorum increased heat tolerance and activated the expression of heat-related LlDREB2B genes, which play a positive role in the regulation of heat tolerance [65]. Balfagón et al. found that the WRKY family transcription factor AtWRKY48 was able to negatively control Arabidopsis acclimation to a combination of high light and heat stress, and that AtWRKY48 gene expression was declined by jasmonic acid (JA) under this condition [66].

2.2.1. WRKY Transcription Factors and Low Temperature Stress

Temperature is one of the main environmental factors affecting the normal growth of plants and is necessary to ensure normal growth of plants, too low a temperature can cause stress to plants, affecting the growth and development of plants. With the change of global climate, low temperature has become one of the agrometeorological disasters, when the temperature drops to the lowest limit that plants can tolerate, it will cause crop growth obstacles, damage to the fruiting organs, and ultimately lead to the inability of normal growth and fruiting, which will result in a substantial reduction in crop yields. Therefore, the study of the molecular mechanism of plant response to low temperature stress is of great scientific significance to improve the cold tolerance of crops [67,68]. Mi et al. identified a WRKY family transcription factor CsWRKY21 in tea tree, which CsWRKY21 was induced by low temperatures and expressed 6 times more compared to the control [69]. Yu et al. identified 42 PgWRKY genes of seven subclasses in the genome of Platycodon grandiflorus. Among them, the expression of PgWRKY26 increased significantly after 6 h of cold stress [70]. Wang et al. identified a cold-inducible WRKY gene, PmWRKY57 was cloned in P. mume. Overexpressing PmWRKY57 line increased cold tolerance in Arabidopsis. Under cold treatment, the transgenic lines had significantly lower malondialdehyde content and significantly higher superoxide dismutase activity, peroxidase activity, and proline content in leaves than wild-type plants. The expression levels of cold-responsive genes such as AtCOR6.6, AtCOR47, AtKIN1, and AtRCI2A were up-regulated in transgenic Arabidopsis thaliana leaves compared with the wild type [71]. Liu et al. isolated an uncharacterized WRKY family transcription factor VvWRKY28, in Beichun (V. vinifera x V.amurensis). Cold treatments can induce high expression of VvWRKY28. Overexpression of VvWRKY28 lines improved tolerance to low temperature in Arabidopsis. Among them, MDA content decreased, chlorophyll and proline content increased, and superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT) activities increased in overexpression of VvWRKY28 lines. In addition, WRKY28 can be associated with the regulation of the expression of downstream genes associated under cold stress (RAB18, COR15A, ERD10, PIF4, COR47 and ICS1) [72]. Wang et al. identified a new WRKY family transcription factor SlWRKY50 in Solanum lycopersicum. SlWRKY50 responds to cold stimuli and plays a key role in JA biosynthesis. Overexpression of SlWRKY50 lines increased cold resistance in tomato, and leading to higher levels of Fv/Fm, antioxidative enzymes, allene oxide synthase expression, and JA accumulation [73].

2.3. WRKY Transcription Factors in Response to Salt Stress

When the salt concentration in the soil is too high, it leads to dehydration of plant cells, affecting and nutrient absorption, thus inhibiting normal root growth. Salt is also capable of causing ionic toxicity in plants, leading to an ionic imbalance in the plant, affecting the osmotic pressure balance inside and outside the root cells, leading to cell swelling or shrinkage, and in severe cases, cell death. Salt therefore plays an important role in plant growth and development [74,75,76]. Huang et al. isolated a WRKY family transcription factor OsWRKY50, overexpression OsWRKY50 lines enhanced salt stress tolerance in plants. OsWRKY50 transcription was repressed under salt stress conditions but activated after ABA treatment. OsWRKY50 was able to bind to the promoter of OsNCED5 and repress its transcription [77]. Huang et al. identified a new WRKY family transcription factor OsWRKY54. Salt stress resulted in rapid induction of OsWRKY54 expression in roots. The wrky54 mutant led to greater sodium accumulation in shoots and enhanced the sensitivity of rice plants to salt stress. OsWRKY54 regulates the expression of OsHKT1;5, this is an essential gene related to salt tolerance, OsWRKY54 regulates the expression of OsHKT1;5 by directly binding to the W-box motif in its promoter [78]. Fang et al. found a new transcription factor gene ZmWRKY86 in Zea mays L., whose expression was up-regulated by salt stress. The wrky86 mutant enhanced plant tolerance to salt stress, with higher viability, catalase activity, and K+ content, and lower malondialdehyde accumulation and Na+ content under salt stress conditions [79]. Ma et al. found WRKY57 is able to negatively regulate plant salt stress response in tomato by directly attenuating the transcription of salt-responsive genes SlRD29B and SlDREB2 and ion homeostasis gene SlSOS1 [80]. Yu et al. found TaWRKY17 expression was up-regulated by salt, drought, hydrogen peroxide (H2O2), and ABA treatments in wheat. Overexpression of TaWRKY17 in Arabidopsis thaliana and wheat resulted in a significant increase in plant salt stress tolerance. Among the overexpression TaWRKY17 plants, SOD, POD and CAT activities were elevated, whereas H2O2 and MDA accumulation were reduced [81].

2.4. Role of WRKY Transcription Factors in Plant Response to Heavy Metals Stress

Heavy metal levels in plants that exceed thresholds can affect produce quality and food safety. Heavy metals can also inhibit the growth of plants, resulting in short plants, loss of green leaves, poor root development and other phenomena. Heavy metals can interfere with the normal physiological and metabolic processes of plants, affecting photosynthesis and respiration, leading to poor nutrient uptake and ultimately causing the death of plants and affecting plants yields. If heavy metals accumulate excessively in food crops, human consumption of such excess crops will cause great harm to human health. Therefore, heavy metals are essential for human food security [82,83,84,85]. Gu et al. identified that the WRKY transcription factor gene ZmWRKY64 is enhanced in maize roots and leaves under cadmium stress, and that knocking down the expression of ZmWRKY64 leads to excessive cadmium accumulation in leaf and root cells, resulting in a cadmium-sensitive phenotype. ZmSRG7 is a key gene that regulates ROS homeostasis under abiotic stress, and ZmWRKY64 directly enhances the transcription of this gene, thereby regulating maize tolerance in response to cadmium stress [86]. Jia et al. identified a WRKY transcription factor TaWRKY70, that regulates tolerance to the heavy metal cadmium in wheat. Cadmium accumulated in overexpressing TaWRKY70 Arabidopsis roots but not in leaf tissues. When TaWRKY70 was expressed, the net influx of Cd2+ into Arabidopsis roots was reduced. Overexpression of TaWRKY70 showed lower electrolyte leakage in Arabidopsis thaliana, malondialdehyde, and hydrogen peroxide contents than the wild type, and higher antioxidant enzyme activities than the wild type. TaWRKY70 directly binds to and regulates the expression of TaCAT5 promoter, which in turn regulates the tolerance of plants to cadmium stress [87]. Xian et al. identified a WRKY transcription factor gene GmWRKY172 expression was significantly up-regulated under cadmium stress, overexpressing GmWRKY172 lines exhibited enhanced cadmium tolerance and reduced cadmium content in shoots. Under cadmium stress, transgenic soybean accumulated less MDA and H2O2, had higher flavonoids, lignin content and POD activity than wild type [88]. Under cadmium stress, the overexpression StWRKY6 strain had significantly higher soil and plant analyzer development values and reactive oxygen scavenging enzyme content than the wild type. The ability of cadmium to induce StWRKY6 transcription factors up-regulated the expression of a number of potential genes, including those involved in cadmium chelation APR2, DFRA, plant defences VSP2, PDF1.4, toxic substance efflux ABCG1, light morphology development BBX20 and auxin signal SAUR64/67. He et al. demonstrated that these genes coordinate the regulation of cadmium tolerance in StWRKY6 overexpressing lines [89]. A new WRKY transcription factor GmWRKY142 positively regulating cadmium stress was identified by cai et al. GmWRKY142 was highly expressed in roots and the expression of the gene was significantly up-regulated under cadmium stress, and overexpression of GmWRKY142 in Arabidopsis and soybean hairy roots significantly enhanced cadmium tolerance. ATCDT1, GmCDT1-1, and GmCDT1-2, encoding cadmium tolerance 1, were induced in the overexpression GmWRKY142 lines [90].

2.5. WRKY Transcription Factors Involved in Plant Response to Nutritional Element Stress

Nitrogen (N) is one of the most important nutrients in the growth and development of plants, and is a component of organic compounds such as proteins, chlorophyll, nucleic acids and various biological enzymes. Plants mainly obtain inorganic nitrogen nutrients in the form of nitrate nitrogen (NO3-) and ammonium nitrogen (NH4+) in the soil through the root system. The inorganic nitrogen in the soil that can be used directly by plants is very little, and inorganic nitrogen is easy to leach and volatilise, but also be fixed by the organic matter in the soil, so the effective nitrogen in the soil is far from enough for the normal growth of plants [91,92,93]. Javed et al. found four genes ShWRKY13-2, ShWRKY39-1, ShWRKY49-3 and ShWRKY125-3 exhibited significant up-regulation in resistance to leaf scald LCP85-384 in two Saccharum spp varieties triggered by Xanthomonas albilineans (Xa). In particular, ShWRKY22-1, ShWRKY49-3 and ShWRKY52-1 acted as negative regulators in both Saccharum spp varieties in response to a range of N injection doses [94]. To assess whether nitrogen form affects the synthesis of the high-value terpene metabolite steviol glycosides (SGs) in stevia (Stevia rebaudiana), Sun et al. utilised stevia plants to the same nitrogen level with NO3- or NH4+ and they found that nitrogen form had no significant effect on stevia leaf biomass or total nitrogen content, but that NO3- increased the leaf SGs content. Combined transcriptome analysis identified 397 genes that were differentially expressed (DEGs) between NO3- and NH4+ treatments. It was concluded that NO3- could promote leaf SG synthesis through the NO3--MYB/WRKY-GGPPS/CPS module [95]. Betalain is a water-soluble nitrogenous pigment, Zhang et al. identified a novel WRKY transcription factor HmoWRKY40 in Hylocereus monacanthus. Betalain content and HmoWRKY40 expression increased rapidly during dragon fruit colouring, and silencing of the HmoWRKY40 gene led to significant reductions in betacyanin content. HmoWRKY40 binds to the promoter of HmoCYP76AD1 and activates its expression, thereby regulating betalain biosynthesis in Hylocereus monacanthus fruit [96].
Phosphorus (P) is one of the essential nutrients for plant growth and development, and phosphorus deficiency will lead to morphological and physiological changes in plants. Phosphorus deficiency has an effect on photosynthesis, respiration and biosynthetic processes in plants. Phosphorus is also an integral part of plant cells and is closely linked to all plant life activities, playing a vital role in plant growth and development [97,98,99,100]. Wang et al. identified a WRKY family of transcription factors OsWRKY108 and OsWRKY21 in rice, and overexpression of these two genes resulted in up-regulation of Pi transporter protein genes, thereby enhancing Pi accumulation [101]. Wang et al. identified the FtWRKY29 transcription factor in Fagopyrum tataricum Gaertn, FtWRKY29 regulates the ability to tolerate phosphorus deficiency. Overexpression of FtWRKY29 in Arabidopsis produced transgenic lines that increased phosphorus uptake and regulated anthocyanin accumulation and were less sensitive to low phosphorus-induced stress. Low-phosphorus-responsive genes PHT1;1, PHT1;4, and PHO1 were significantly up-regulated in these lines [102]. Liu et al. found that the GmWRKY46 gene is involved in the regulation of phosphorus deficiency tolerance in soybean. The expression of GmWRKY46 was significantly higher in low phosphorus-sensitive than in phosphorus-tolerant soybean varieties, and the gene was strongly induced by phosphorus deficiency. The expression patterns of many P-responsive genes, for example GmPht1;1, GmPht1;4, GmPTF1, GmACP1, GmPAP21, and GmExpansin-A7 were altered in overexpression of the GmWRKY46 lines and in GmWRKY46-silenced lines [103]. Zhang et al. found overexpression of OsWRKY21 or OsWRKY108 caused an increase in Pi accumulation due to elevated expression of phytophosphate transporter protein 1 (PHT1). Oswrky21 and Oswrky108 double mutants showed decreased Pi accumulation and OsPHT1;1 expression in a Pi-dependent manner. Their results demonstrate that rice WRKY transcription factors function redundantly to promote Pi uptake by activating OsPHT1;1 expression under Pi-sufficient conditions [104]. Knockdown of OsWRKY10 results in increased Pi uptake and accumulation under conditions of Pi sufficiency. OsPHT1;2 results in increased Pi accumulation in oswrky10. OsWRKY10 is a transcriptional repressor, induced by Pi transcription, and it is up-regulated by a subset of the PHT1 gene upon its mutation. During Pi starvation, OsWRKY10 protein is degraded via the 26S proteasome. Their results demonstrate that the OsWRKY10-OsPHT1;2 module inhibits Pi uptake only in the presence of Pi sufficient [105].

2.6. WRKY Transcription Factors and Oxidative Stress

Oxidative stress is one of the most severe stresses caused by various other stresses. There are 4 main types of reactive oxygen species in plants: singlet oxygen (1O2), superoxide (O2−), hydroxyl radical (OH) and hydrogen peroxide H2O2 . Induction of ROS accumulation in Arabidopsis with salt stress or by treating plants with H2O2 or methyl viologen (MV) induces the expression of multiple genes encoding WRKY family transcription factors [106,107,108,109]. Jia et al. identified a WRKY family of transcription factors GhWRKY68 promoter-driven β-glucuronidase activity is enhanced after exposure to drought, salt, ABA and H2O2. GhWRKY68 overexpression lines showed reduced resistance to drought and salt, and reduced tolerance to oxidative stress, which was associated with accumulation of ROS, reduced enzyme activity, increased MDA content and altered expression of ROS-related genes [110]. Sun et al. found AtWRKY53 overexpression lines were highly sensitive to drought stress compared to Col-0 plants. Activated expression of AtWRKY53 inhibited stomatal closure by reducing the H2O2 content of guard cells. AtWRKY53 could bind directly to the qua-quine starch (QQS, AT3G30720) gene promoter sequence and leading to enhanced starch metabolism [111].

3. Conclusion and Prospects

Due to the continuous changes in the global climate environment, plants often suffer from different forms of biotic and abiotic stress during their growth and development. In order to cope with these adverse conditions, plants have developed a complete coping system in the process of evolution. Plant adversities are dealt with through protein regulation of the expression level of downstream genes or interactions between proteins. Because transcription factors contain different gene binding sites, they can often regulate the expression of multiple downstream genes. Therefore, focusing on the functions of transcription factors has become a major issue in crops. As a large class of important transcription factors in plants, WRKY transcription factors genes play a key role throughout a plant's life cycle. With the continuous development of gene editing and third-generation sequencing technology, many researchers have verified the functions of WRKY family members in different types of plants, and found and proved that WRKY genes play a key role in plant growth and development, biotic and abiotic stresses [112,113,114,115,116]. In order to investigate the phylogeny and evolutionary relationships of WRKY family genes in different species, we constructed phylogenetic trees of the amino acid sequences of some WRKY family transcription factors in Glycine max, Arabidopsis thaliana and Oryza sativa using MEGA 11.0 software [117]. Among them, we found that GmWRKY58 and GmWRKY76 were highly related, GmWRKY46 and GmWRKY43 were highly related, AtWRKY39 and OsGmWRKY87 were highly related, and OsWRKY73 and OsGmWRKY97 were highly related, which indicated that the WRKY family of transcription factors were highly related in various species have close affinities between them, and it is possible that WRKY family transcription factors have similar functions in different species (Figure 4).
Future research on WRKY transcription factors can start from the following aspects, such as the use of CRISPR/Cas9 technology to knock out the WRKY family transcription factor genes and overexpression of genes and other technologies, to cultivate new varieties of resilient and excellent crops, and to promote the sustainable development of agriculture. To further investigate the upstream and downstream regulators and target genes of WRKY family transcription factor genes by using existing technologies, to analyse their regulatory networks in response to adversity stress, and to elucidate the molecular mechanisms of WRKY and plant response to abiotic stresses.
Nowadays, scientists mainly focus on the response of WRKY transcription factors to common abiotic stresses such as drought, cold, salt, heavy metals (Table 2). While the molecular mechanisms of WRKY transcription factors in response to chemical agent stresses are less reported. In today's increasingly developed industry, chemical pollutants such as car exhaust, haze and pesticides are extremely harmful to crops. The main component of automobile exhaust and haze is sulfide, and SO2 in the atmosphere generates SO3 under the action of sunlight, water vapour and drifting dust and so on. Firstly, while SO3 falls to the ground in the form of rainfall and drenches the plants, damaging the waxy protective layer of the epidermis of the plant leaves and impairing the normal transpiration and gas exchange process. Secondly, acid rain also destroys a class of alkaline nutrients such as potassium, calcium and phosphorus in the soil, leading to withering and death of plants that cannot absorb nutrients in soils with insufficient fertility. Excessive use of pesticides will inhibit the growth and development of plants, resulting in short plants, small leaf area and yellowing of leaf colour. The toxicity of pesticides can also lead to cell membrane rupture, cytoplasmic leakage and ultimately affect the normal growth and development of plants. Today, people are more and more concerned about crop security, if we pay more attention to focus on the molecular mechanism of WRKY transcription factors and chemical reagents in the future, this will provide a guarantee for crop security.
In summary, the WRKY family of transcription factors is critical for plant growth and development as well as regulation in plant response to abiotic stresses. In the future, we will pay more attention to the mechanism by which WRKY transcription factors can regulate downstream target genes in response to abiotic stresses, which can provide more theoretical basis for the improvement of food production and safety.
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Figure 4. Phylogenetic tree WRKYs family genes in Glycine max, Arabidopsis thaliana and Oryza sativa. Phylogenetic tree of WRKY transcription factors proteins in selected angiosperms. The WRKY family gene sequences of Glycine max, Arabidopsis thaliana and Oryza sativa were retrieved using the China National Rice Data Center (https://www.ricedata.cn/) and NCBI (https://www.ncbi.nlm.nih.gov/). The phylogenetic tree was constructed using MEGA version 11.0 with the bootstrap method based on full amino acid sequences. Numbers next to the branches show the percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates).
Figure 4. Phylogenetic tree WRKYs family genes in Glycine max, Arabidopsis thaliana and Oryza sativa. Phylogenetic tree of WRKY transcription factors proteins in selected angiosperms. The WRKY family gene sequences of Glycine max, Arabidopsis thaliana and Oryza sativa were retrieved using the China National Rice Data Center (https://www.ricedata.cn/) and NCBI (https://www.ncbi.nlm.nih.gov/). The phylogenetic tree was constructed using MEGA version 11.0 with the bootstrap method based on full amino acid sequences. Numbers next to the branches show the percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates).
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Table 2. Abiotic stress responsive the WRKY transcription factors in plants.
Table 2. Abiotic stress responsive the WRKY transcription factors in plants.
Abiotic Stress Type WRKY transcription factors Species Expression patternBREAK Reference
Heat AtWRKY39 Arabidopsis thaliana L. Increase [118]
Boron AtWRKY47 Arabidopsis thaliana L. Decrease [119]
Cadmium AtWRKY13 Arabidopsis thaliana L. Increase [120]
Salt AtWRKY28 Arabidopsis thaliana L. Increase [121]
Salt AtWRKY33 Arabidopsis thaliana L. Increase [122]
Salt AtWRKY46 Arabidopsis thaliana L. Increase [123]
Salt, drought GmWRKY12 Glycine max L. Increase [124]
Salt, drought GmWRKY16 Glycine max L. Increase [125]
Salt GmWRKY20 Glycine max L. Increase [126]
Salt, drought GmWRKY27 Glycine max L. Increase [127]
Salt, drought GmWRKY54 Glycine max L. Increase [128]
Salt GmWRKY144, 165 Glycine max L. Increase [129]
Salt ZmWRKY17 Zea mays L. Decrease [130]
Salt ZmWRKY86 Zea mays L. Decrease [79]
Drought ZmWRKY104 Zea mays L. Increase [131]
Salt OsWRKY50 Oryza sativa Increase [77]
Cold OsWRKY63 Oryza sativa Decrease [18]
Cold OsWRKY76 Oryza sativa Increase [132]
Salt OsWRKY42 Oryza sativa Increase [133]
Drought OsWRKY55 Oryza sativa Decrease [134]
Drought OsWRKY5 Oryza sativa Decrease [135]
Drought OsWRKY97 Oryza sativa Increase [136]
Aluminum OsWRKY22 Oryza sativa Decrease [137]
Salt, drought OsWRKY87 Oryza sativa Increase [138]

Author Contributions

All the authors contributed to the present form of the manuscript. Z.M. collected the data and drafted the manuscript; Z.M., L.H., and W.J. edited the manuscript; Z.M. and L.H. created the figures and tables; Z.M. and W.J. supervised; Z.M. and L.H. and W.J. finalised and approved the final version of the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 32201695). Open Access funding provided by the Max Planck Society.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no competing interests.

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Preprints 108162 g003
Figure 3. Impacts of drought stress in plants. Overexpression of WRKY transcription factor genes in plants can can reduce a ROS production, stomatal closure, down regulation of noncyclic protein, leaf traits are suppressed and ion toxicity and nutrient imbalance. This allows plants to improve their water retention capacity to cope with plant survival rate under drought stress.
Figure 3. Impacts of drought stress in plants. Overexpression of WRKY transcription factor genes in plants can can reduce a ROS production, stomatal closure, down regulation of noncyclic protein, leaf traits are suppressed and ion toxicity and nutrient imbalance. This allows plants to improve their water retention capacity to cope with plant survival rate under drought stress.
Preprints 108162 g003
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