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Function and Mechanism of WRKY Transcription Factors in Abiotic Stress Responses of Plants

Weixing Li, Siyu Pang, Zhaogeng Lu and 1 more

Plants · 2020 · Review · CC BY

doi:10.3390/plants9111515

Abstract

The WRKY gene family is a plant-specific transcription factor (TF) group, playing important roles in many different response pathways of diverse abiotic stresses (drought, saline, alkali, temperature, and ultraviolet radiation, and so forth). In recent years, many studies have explored the role and mechanism of WRKY family members from model plants to agricultural crops and other species. Abiotic stress adversely affects the growth and development of plants. Thus, a review of WRKY with stress responses is important to increase our understanding of abiotic stress responses in plants. Here, we summarize the structural characteristics and regulatory mechanism of WRKY transcription factors and their responses to abiotic stress. We also discuss current issues and future perspectives of WRKY transcription factor research.

Full text

From PubMed Central, U.S. National Library of Medicine, as current on Oct 20, 2026. Paragraph numbers are ours, so an answer can point at one.

1. Introduction

As a fixed-growth organism, plants are exposed to a variety of environmental conditions and may encounter many abiotic stresses, for example, drought, waterlogging, heat, cold, salinity, and Ultraviolet-B (UV-B) radiation. To adapt and counteract the effects of such abiotic stresses, plants have evolved several molecular mechanisms involving signal transduction and gene expression. Transcription factors (TFs) are important regulators involved in the process of signal transduction and gene expression regulation under environmental stresses. TFs can be combined with cis-acting elements to regulate the transcriptional efficiency of target genes by inhibiting or enhancing their transcription. Accordingly, plants may show corresponding responses to external stresses via TFs regulating target genes. Although some TF families (MYB, bZIP, AP2/EREBP, NAC) are associated with adversity, WRKY is the most extensively studied TF family in plant stress responses.

The WRKY family is a unique TF superfamily of higher plants and algae, which play important roles in many life processes, particularly in response against biotic and abiotic stress. In 1994, the SWEET POTATO FACTOR1 (SPF1) gene of the WRKY family was first found in Impoea batatas. Later, ABF1 and ABF2 were found in wild Avena sativa, and showed regulatory roles in seed germination. A previous study successively cloned WRKY1, WRKY2, and WRKY3 from Petroselinum crispum, named the WRKY TF, and proved for the first time that WRKY protein can regulate plant responses to pathogens. With an increase in available published genomes, many members of the WRKY TF family have been identified in various species, including 104 from Populus, 37 from Physcomitrella patens, 45 from Hordeum vulgare, 55 from Cucumis sativus, 74 from Arabidopsis thaliana, 83 from Pinus monticola, 81 from Solanum lycopersicum, and 102 from Oryza sativa. WRKY TFs exist as gene families in plants, and the number of WRKY TFs varies among species. In plants exposed to abiotic stresses (salt, drought, temperature, and so forth), WRKY family members play important roles in diverse stress responses. In addition, these TFs affect the growth and development of plants. Therefore, WRKY TFs have attracted broad attention. Although some reviews on WRKY TFs are available, in this review we focus on the structural characteristics and regulatory mechanisms of WRKY TFs and summarize recent progress in understanding the roles of WRKY TFs during exposure to abiotic stresses such as drought, temperature, salt, and UV radiation.

2. Structural Characteristics of WRKY TFs

The WRKY structure consists of two parts: the N-terminal DNA binding domain and the C-terminal zinc-finger structure. The DNA binding domain sequence of WRKY is based on the heptapeptide WRKYGQK (Figure 1), but there are some differences, such as WRKYGQK, WRKYGKK, WRKYGMK, WSKYGQK, WKRYGQK, WVKYGQK, and WKKYGQK. Zinc-finger structures mainly include C2H2 type and C2HC type, whereas some exist in the form of CX29HXH and CX7CX24HXC (Figure 1). According to the number of WRKY domains and the structure of their zinc-finger motifs, WRKY can be divided into groups I, II, and III (Figure 1). Group I usually contains two WRKY domains and one C2H2 zinc-finger structure. Those in group II and group III contain only one WRKY domain. The difference is that the zinc-finger structure in group II is C2H2 and that in group III is C2HC (Figure 1). According to the phylogenetic relationship of the amino acid sequence of the primary structure, group II can be further divided into subgroups a–e. Evolutionary analyses have shown that the WRKY of group II is not generally a single source, mainly including five categories I, IIa + IIb, IIc, IId + IIe, and III. In addition, some WRKY proteins contain a glutamate enrichment domain, a proline enrichment domain, and a leucine zipper structure.

3. Regulatory Mechanism of WRKY TFs

WRKY family members have diverse regulatory mechanisms. Briefly, WRKY protein can be effectively combined with W-box elements to activate or inhibit the transcription of downstream target genes. Moreover, it can also bind other acting elements to form protein complexes, which enhances the activity of transcription binding.

WRKY TFs can effectively activate the expression of downstream genes by binding conserved W-box cis-acting elements in the downstream gene promoter region. There are abundant W-box elements in the self-promoter of most WRKY TFs. Therefore, these WRKY TFs can bind with their own promoters to achieve self-regulation or cross-regulation networks by combining with other WRKY TFs. For example, CaWRKY6 of Capsicum frutescens can activate CaWRKY40 and make the plant more tolerant to high temperature and humidity. Glycine max GmWRKY27 not only inhibits the activity of downstream GmNAC29 promoter by independent inhibition, but also cooperatively interacts with GmMYB174 to inhibit the expression of GmNAC29, thereby increasing drought and salt stress resistances. Moreover, chromatin immunoprecipitation (ChIP) studies have shown that when Petroselinum crispum is infected by pathogenic bacteria, PcWRKY1 promoter can effectively bind to itself and the W-box of PcWRKY3 promoter, and transcriptional activation can be achieved through self-negative feedback regulation and cross-regulation with other WRKY proteins. In addition, WRKY TFs can interact with non-W-box elements. For example, Oryza sativa OsWRKY13 can interact with PRE4 (TGCGCTT) elements. Hordeum vulgare HvWRKY46 and Nicotiana tabacum NtWRKY12 can effectively combine with the sucrose response element SURE. These results indicate that there are multiple binding modes between WRKY TFs and structural genes. Different binding patterns and preferences of binding sites allow for the regulation of downstream target genes, providing WRKY TFs with versatile functions in the plant transcriptional regulation network.

4. WRKY TF Involved in Abiotic Stress Responses

When plants sense stress, the corresponding signaling is activated and transferred to the cell interior. Reactive oxygen species (ROS) and Ca2+ ions are usually exchanged as the signal transduction in the cell. Protein kinases such as MPKs are subsequently activated to regulate the activities of related TFs. Consequently, the plant presents a stress response. In response to abiotic stresses, some WRKY TFs can be rapidly differentially expressed, promoting signal transduction and regulating the expression of related genes. The expression patterns and functional identifications of WRKYs in most studies are generally based on transcriptome analyses, real-time fluorescence quantitative PCR, gene chip analyses, and genetic transformation. Hence, WRKY genes can function effectively in most abiotic stress responses or tolerances in various plants (Table 1, Figure 2).

4.1. WRKY TFs and Drought Stress

Drought has a major impact on plant growth and development, resulting in a significant decrease in grain and other types of crop yield. Under drought stress, drought-tolerant plants can accumulate oligosaccharides through sucrose metabolism to improve drought resistance. For example, when Arabidopsis is subjected to drought stress, the expression of AtWRKY53 combined with the Qua-Quine Starch (QQS) promoter sequence is rapidly induced, hydrogen peroxide content is reduced, and the glucose metabolism pathway is significantly enhanced, thereby regulating stomatal opening and ultimately affecting drought tolerance. In Boea hygrometrica, BhWRKY1 effectively regulates the expression of the BhGolS1 gene, and the overexpression of BhGolS1 and BhWRKY1 induces the accumulation of raffinose family oligosaccharides (RFOs) in transgenic Nicotiana tabacum, thus improving the ability of seedlings to resist drought.

WRKY protein can directly regulate the expression of drought-resistant genes. For example, in sorghum, SbWRKY30 regulates the drought stress response gene SbRD19 by binding with W-box elements of the SbRD19 promoter, and protects plant cells from the damage of reactive oxygen species by improving ROS scavenging capability, enhancing drought tolerance. TaWRKY2 of wheat can bind to STZ and downstream drought-resistant gene RD29B promoter, with a positive regulatory effect on the expression of RD29B. DREB2A regulates the expression of dehydration stress-related genes, while TaWRKY19 can bind to DREB2A promoter, ultimately activating the expression of RD29A, RD29B, and Cor6.6 in transgenic Arabidopsis plants. Similarly, Arabidopsis AtWRKY57 positively regulates the expression of RD29A and NCED3 genes by binding their W-box elements in the promoter regions. In addition, WRKY protein can act on other TFs to play regulatory roles in drought tolerance. For example, TcWRKY53 of Thlaspi arvense significantly inhibits the expression of NtERF5 and NterEBp-1 of the AP2/ERF TF family, thus improving plant resistance to drought stress.

WRKY TFs also regulate plant tolerance through abscisic acid (ABA) and ROS-related signaling pathways. During drought stress, higher ABA levels were accumulated in plants, and leaf stomata were closed to reduce transpiration rate, thus regulating water balance in plants. ABA accumulation in cells, integrated with a variety of stress signals, regulates the expression of downstream genes, consequently sensing and responding to the adverse environment. Arabidopsis AtWRKY63 has a specific effect on ABA-mediated stomatal closure and other signal transduction pathways, thus affecting the drought response. GhWRKY21 regulates ABA-mediated cotton drought tolerance by promoting the expression of GhHAB. Overexpression of BdWRKY36 in tobacco reduces the accumulation of ROS, activated NtLEA5, NtNCED1, and NtDREB3 in the ABA biosynthetic pathway, and significantly enhances the drought resistance of plants. In Solanum lycopersicum, SlWRKY81 increases the drought tolerance of plants by inhibiting the accumulation of H2O2, playing a negative regulation role of stomatal closure.

4.2. WRKY TFs and Salt Stress

Salt stress is an important abiotic stress affecting crop productivity, particularly in arid and semiarid regions. WRKY TFs play essential roles in regulating the response to salt stress. To date, a total of 47 WRKY genes have been found to be expressed under salt stress in the wheat genome. STZ is a protein related to ZPT2, which acts as a transcriptional inhibitor to downregulate the deactivation of other transcription factors. GmWRKY54 of Glycine max inhibits STZ expression and responds to salt stress by positively regulating the DREB2A-mediated pathway. FcWRKY70 promotes the upregulation of arginine decarboxylase (ADC) expression, which is heterologously expressed in tobacco, and the content of lemon putrescine is significantly increased, thus enhancing the salt tolerance of plants. The IbWRKY47 gene positively regulates stress resistance-related genes and significantly improves the salt tolerance of Ipomoea batatas. MiR156/SPL modulates salt tolerance by upregulation of Malus domestica salt tolerance gene MdWRKY100. In Sorghum bicolor, SbWRKY50 could directly bind to the upstream promoter of SOS1 and HKT1 and participate in plant salt response by controlling ion homeostasis. In addition, some WRKY genes function as negative regulation factors involved in salt stress resistance. Arabidopsis RPD3-like histone deacetylase HDA9 inhibits salt stress tolerance by regulating the DNA binding and transcriptional activity of WRKY53. Chrysanthemum CmWRKY17 overexpressed in Arabidopsis allows the plants to be more sensitive to salt stress. The expression level of stress resistance-related genes in transgenic Arabidopsis is lower than that in wild-type plants, indicating that CmWRKY17 may be involved in negatively regulating the salt stress response in Chrysanthemum. The expression of GhWRKY68 is strongly induced in upland cotton and decreases salt tolerance. In contrast, a high expression level of GhWRKY25 enhances the salt tolerance of upland cotton, while transgenic tobacco shows a relatively weaker tolerance to drought stress, indicating that the regulatory effects of different WRKY TFs involved in drought response are different.

Plants can also respond to saline–alkali stress through ABA, H2O2, and other signal pathways. In Glycine max, the negative regulatory factor ABI1 in the ABA pathway may be the downstream target gene of GmWRKY13. Genetic transformation experiments in Arabidopsis have shown that overexpression of GmWRKY13 significantly increases the expression of ABI1, but plants show a low tolerance to salt stress. Overexpression of ZmWRKY17 has an inhibitory effect on the sensitivity of exogenous ABA treatment, resulting in a relatively lower tolerance to high levels of salinity. Under salt-induced H2O2 and cytosolic Ca2+ stimulation, the activity of antioxidant enzymes increases, thus improving the tolerance to high-salinity environments. ABA-induced WRKY gene expression is largely related to salt stress. Exogenous application of ABA and NaCl also induce AtWRKY25 and AtWRKY33 in Arabidopsis, OsWRKY72 in rice, GbWRKY1 in Verbena bonariensis, and VpWRKY1/2 and VpWRKY3 in grape.

4.3. WRKY TFs and Temperature Stress

Both low- and high-temperature stress can reduce crop yield and quality in plants. WRKY TFs play a role in the stress response through different signal transduction pathways. For example, in Verbena bonariensis, VbWRKY32 as a positive regulator, upregulates the transcriptional level of cold response genes, which increases the antioxidant activity, maintains membrane stability, and enhances osmotic regulation ability, thereby improving the survival ability under cold stress. The BcWRKY46 gene of Brassica campestris is strongly induced by low temperature and ABA, activating related genes in the ABA signaling pathway to improve the low-temperature tolerance of plants. CBF TFs regulate the expression of COR, and the overexpressed transgenic lines of CBF1, CBF2, and CBF3 show stronger cold resistance. AtWRKY34 has a negative regulatory effect on the CBF-mediated cold response pathway; it is specifically expressed in mature pollen grains after exposure to low temperatures, resulting in resistance to low temperatures. In addition, plants respond to temperature changes by coordinating organ development in an adverse environment. At low temperatures, rice MADS-Box TF OsMADS57 and its interacting protein OsTB1 synergistically activate the transcriptional regulation of OsWRKY94, preventing tillering by inhibiting transcription of the organ development gene D14.

Due to global climate change, high-temperature stress has attracted significant attention. There is evidence that, to a certain extent, high temperatures will lead to biochemical changes in plants. Thermal stimulation can activate Ca2+ channels to maintain a higher intracellular Ca2+ concentration, thereby activating calmodulin protein expression and inducing thermal-shock protein transcriptional expression. In Arabidopsis, AtWRKY54 significantly responds to heat shock whereas basic leucine zipper factors (bZIPs) respond to prolonged warming. Overexpression of AtWRKY39 can make plants more heat-sensitive. AtWRKY39 is highly homologous to AtWRKY7, and both of them can effectively bind calmodulin in plants, indicating a similar function. In addition, AtWRKY25, AtWRKY26, and AtWRKY33 can improve tolerance to high-temperature stress in transgenic Arabidopsis by regulating the Hsp101 and Zat10 genes. Plants subjected to heat stress can also activate the oxidative stress response through ethylene. Under high-temperature stress, the expressions of AtWRKY25, AtWRKY26, and AtWRKY33 in Arabidopsis are induced by ethylene, the feedback factor EIN2 is transcriptionally regulated, and the effective activation of ethylene signal transduction contribute to relatively stronger heat resistance. In Oryza sativa, HSP101 promoter can activate the expression of the OsWRKY11 gene. Under heat treatment, the leaves wilted more slowly and the green part of the plant was less damaged, which makes it more heat-resistant. In addition, some noncoding RNAs, such as miR396, play a role in the response to heat stress by regulating its target WRKY6.

4.4. WRKY TFs and Other Abiotic Stresses

WRKY TFs are also involved in oxidative stress, mechanical damage, UV radiation, and other abiotic stresses (Figure 3). FcWRKY40 overexpression can significantly enhance the resistance of transgenic tobacco to oxidative stress. When Arabidopsis is treated with ROS, the expressions of AtWRKY30, AtWRKY40, AtWRKY75, AtWRKY6, AtWRKY26, and AtWRKY45 are significantly upregulated. After mechanical injury, the expression levels of AtWRKY11, AtWRKY15, AtWRKY22, AtWRKY33, AtWRKY40, AtWRKY53 and AtWRKY6 are upregulated. Similarly, NaWRKY3 is strongly expressed in tobacco. By contrast, the sensitivity of transgenic plants is increased when NaWRKY3 is knocked out. In two previous studies, UV-B radiation treatment induced three WRKY genes in Arabidopsis and the OsWRKY89 gene in rice, resulting in a thick waxy substance on the leaf surface and improved tolerance to heat.

In addition, a single WRKY TF can play multiple roles in different stress responses via various signal pathways and regulatory networks. For example, TaWRKY44 expression in tobacco can improve resistance to drought, salt stress, and osmotic stress, while PgWRKY62 and PgWRKY33 in Pennisetum glaucum respond to salt and drought simultaneously. BhWRKY1 protein in Boea hygrometrica binds to the promoter of BhGolS1 and is associated with both low-temperature resistance and drought tolerance. IbWRKY2 can interact with IbVQ4, and drought and salt treatment can induce the expression of IbVQ4, thus improving the tolerance of plants to drought and salt stress. MdWRKY30 overexpression enhances tolerance to salt and osmotic stress in transgenic apple callus through transcriptional regulation of stress-related genes. PagWRKY75 negatively regulates the tolerance of 84 K poplar (Populus alba × P. glandulosa) to salt and osmotic stress by reducing the scavenging capacity of ROS and the accumulation of proline, thus actively regulates the rate of leaf water loss.

5. Conclusions and Perspectives

As one of the largest TF families, WRKY plays an important and indispensable role in normal life activities of plants. Over the years, it has been shown that WRKY TFs not only participate in plant growth and development, but also show complex regulatory mechanisms and networks involved in external abiotic stresses. A large number of WRKYs have been functionally characterized in model plants, providing abundant functional references for other plants. Given that crops usually face various stresses and WRKYs play important roles in stress responses, further in-depth studies on WRKY genes in more crops are required. As increasing plant genomes have been sequenced, particularly of economically important crops, the genome-wide identification of WRKY genes will facilitate screening for stress resistance-related functional genes in plants. Moreover, previous studies of WRKY gene functions were largely dependent on transcriptomics and functional predictions, whereas more applications of genetic verification combined with new technologies are accelerating the research progress of WRKY’s novel functions. In addition, characterization of the downstream genes regulated by WRKY TFs or WRKY TF self-regulation will help clarify the regulatory network of abiotic stress responses. Furthermore, noncoding RNAs and epigenetic modifications involved in the regulation of WRKY TFs should be explored in future studies. Ultimately, using WRKY TFs to screen for stress-resistant plant cultivars and improve plant stress resistance will significantly benefit agricultural crop yield and quality in the context of aggravated climate change.

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    Not in our library10.1007/s00709-015-0885-3

  45. 45.

    Jia H., Wang C., Wang F., Liu S., Li G., Guo X. GhWRKY68 reduces resistance to salt and drought in transgenic Nicotiana benthamiana. PLoS ONE. 2015;10:e0120646.

    Not in our library10.1371/journal.pone.0120646

  46. 46.

    Wang M., Vannozzi A., Wang G., Liang Y.-H., Tornielli G.B., Zenoni S., Cavallini E., Pezzotti M., Cheng Z.-M. Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Hortic. Res. 2014;1:14016.

    Not in our library10.1038/hortres.2014.16

  47. 47.

    Dang F.F., Wang Y.N., Yu L., Eulgem T., Lai Y., Liu Z.Q., Wang X., Qiu A.L., Zhang T.X., Lin J., et al. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant Cell Environ. 2013;36:757-774.

    Not in our library10.1111/pce.12011

  48. 48.

    Sun J., Hu W., Zhou R., Wang L., Wang X., Wang Q., Feng Z.-J., Yu H., Qiu D., He G., et al. The Brachypodium distachyon BdWRKY36 gene confers tolerance to drought stress in transgenic tobacco plants. Plant Cell Rep. 2014;34:23-35.

    Not in our library10.1007/s00299-014-1684-6

  49. 49.

    Gong X., Zhang J., Hu J., Wang W., Wu H., Zhang Q., Liu J.-H. FcWRKY70, a WRKY protein of Fortunella crassifolia, functions in drought tolerance and modulates putrescine synthesis by regulating arginine decarboxylase gene. Plant Cell Environ. 2015;38:2248-2262.

    Not in our library10.1111/pce.12539

  50. 50.

    Wu X., Shiroto Y., Kishitani S., Ito Y., Toriyama K. Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep. 2009;28:21-30.

    Not in our library10.1007/s00299-008-0614-x

  51. 51.

    Song Y., Chen L., Zhang L., Yu D. Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis. J. Biosci. 2010;35:459-471.

    Not in our library10.1007/s12038-010-0051-1

  52. 52.
    OsWRKY74 , a WRKY transcription factor, modulates tolerance to phosphate starvation in rice · 2015
    No notice
  53. 53.
    WRKY76 is a rice transcriptional repressor playing opposite roles in blast disease resistance and cold stress tolerance · 2013
    No notice
  54. 54.

    Wang H., Hao J., Chen X., Hao Z., Wang X., Lou Y., Peng Y., Guo Z. Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol. Biol. 2007;65:799-815.

    Not in our library10.1007/s11103-007-9244-x

  55. 55.

    Zhou Q.-Y., Tian A.-G., Zou H.-F., Xie Z.-M., Lei G., Huang J., Wang C.-M., Wang H.-W., Zhang J.-S., Chen S.-Y. Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol. J. 2008;6:486-503.

    Not in our library10.1111/j.1467-7652.2008.00336.x

  56. 56.

    Yan H., Jia H., Chen X., Hao L., An H., Guo X. The cotton WRKY transcription factor GhWRKY17 functions in drought and salt stress in transgenic Nicotiana benthamiana through ABA signaling and the modulation of reactive oxygen species production. Plant Cell Physiol. 2014;55:2060-2076.

    Not in our library10.1093/pcp/pcu133

  57. 57.

    Cai R., Dai W., Zhang C., Wang Y., Wu M., Zhao Y., Ma Q., Xiang Y., Cheng B. The maize WRKY transcription factor ZmWRKY17 negatively regulates salt stress tolerance in transgenic Arabidopsis plants. Planta. 2017;246:1215-1231.

    Not in our library10.1007/s00425-017-2766-9

  58. 58.

    Niu C.-F., Wei W., Zhou Q.-Y., Tian A.-G., Hao Y.-J., Zhang W., Ma B., Lin Q., Zhang Z.-B., Zhang J.-S., et al. Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in transgenic Arabidopsis plants. Plant Cell Environ. 2012;35:1156-1170.

    Not in our library10.1111/j.1365-3040.2012.02480.x

  59. 59.

    Wang F., Hou X., Tang J., Wang Z., Wang S., Jiang F., Li Y. A novel cold-inducible gene from Pak-choi (Brassica campestris ssp. chinensis), BcWRKY46, enhances the cold, salt and dehydration stress tolerance in transgenic tobacco. Mol. Biol. Rep. 2011;39:4553-4564.

    Not in our library10.1007/s11033-011-1245-9

  60. 60.

    Wang Z., Zhu Y., Wang L., Liu X., Liu Y., Phillips J., Deng X. A WRKY transcription factor participates in dehydration tolerance in Boea hygrometrica by binding to the W-box elements of the galactinol synthase (BhGolS1) promoter. Planta. 2009;230:1155-1166.

    Not in our library10.1007/s00425-009-1014-3

  61. 61.

    Li H., Xu Y., Xiao Y., Zhu Z., Xie X., Zhao H., Wang Y. Expression and functional analysis of two genes encoding transcription factors, VpWRKY1 and VpWRKY2, isolated from Chinese wild Vitis pseudoreticulata. Planta. 2010;232:1325-1337.

    Not in our library10.1007/s00425-010-1258-y

  62. 62.

    Zhu Z., Shi J., Cao J., He M., Wang Y. VpWRKY3, a biotic and abiotic stress-related transcription factor from the Chinese wild Vitis pseudoreticulata. Plant Cell Rep. 2012;31:2109-2120.

    Not in our library10.1007/s00299-012-1321-1

  63. 63.

    Wei W., Zhang Y., Han L., Guan Z., Chai T. A novel WRKY transcriptional factor from Thlaspi caerulescens negatively regulates the osmotic stress tolerance of transgenic tobacco. Plant Cell Rep. 2008;27:795-803.

    Not in our library10.1007/s00299-007-0499-0

  64. 64.

    Skibbe M., Qu N., Galis I., Baldwin I.T. Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell. 2008;20:1984-2000.

    Not in our library10.1105/tpc.108.058594

  65. 65.

    Yang G., Zhang W., Liu Z., Yi-Maer A.Y., Zhai M., Xu Z. Both JrWRKY2 and JrWRKY7 of Juglans regia mediate responses to abiotic stresses and abscisic acid through formation of homodimers and interaction. Plant Biol. 2017;19:268-278.

    Not in our library10.1111/plb.12524

  66. 66.

    Yang Z., Chi X., Guo F., Jin X., Luo H., Hawar A., Chen Y., Feng K., Wang B., Qi J., et al. SbWRKY30 enhances the drought tolerance of plants and regulates a drought stress-responsive gene, SbRD19, in sorghum. J. Plant Physiol. 2020;246:153142.

    Not in our library10.1016/j.jplph.2020.153142

  67. 67.

    Song Y., Li J., Sui Y., Han G., Zhang Y., Guo S., Sui N. The sweet sorghum SbWRKY50 is negatively involved in salt response by regulating ion homeostasis. Plant Mol. Biol. 2020;102:603-614.

    Not in our library10.1007/s11103-020-00966-4

  68. 68.

    Qin Z., Hou F., Li A., Dong S., Wang Q., Zhang L. Transcriptome-wide identification of WRKY transcription factor and their expression profiles under salt stress in sweetpotato (Ipomoea batatas L.). Plant Biotechnol. Rep. 2020;14:599-611.

    Not in our library10.1007/s11816-020-00635-4

  69. 69.

    Zhu H., Zhou Y., Zhai H., He S., Zhao N., Liu Q. A novel sweetpotato WRKY transcription factor, IbWRKY2, positively regulates drought and salt tolerance in transgenic. Arabidopsis. 2020;10:506.

    Not in our library10.3390/biom10040506

  70. 70.

    Dong Q., Zheng W., Duan D., Huang D., Wang Q., Liu C., Li C., Gong X., Li C., Mao K., et al. MdWRKY30, a group IIa WRKY gene from apple, confers tolerance to salinity and osmotic stresses in transgenic apple callus and Arabidopsis seedlings. Plant Sci. 2020;299:110611.

    Not in our library10.1016/j.plantsci.2020.110611

  71. 71.
    The miR156/SPL module regulates apple salt stress tolerance by activating MdWRKY100 expression · 2020
    No notice
  72. 72.

    Ahammed G.J., Li X., Yang Y., Liu C., Zhou G., Wan H., Cheng Y. Tomato WRKY81 acts as a negative regulator for drought tolerance by modulating guard cell H2O2–mediated stomatal closure. Environ. Exp. Bot. 2020;171:103960.

    Not in our library10.1016/j.envexpbot.2019.103960

  73. 73.

    Luo X., Li C., He X., Zhang X., Zhu L.-F. ABA signaling is negatively regulated by GbWRKY1 through JAZ1 and ABI1 to affect salt and drought tolerance. Plant Cell Rep. 2019;39:181-194.

    Not in our library10.1007/s00299-019-02480-4

  74. 74.

    Wang M.-Q., Huang Q.-X., Lin P., Zeng Q.-H., Li Y., Liu Q.-L., Zhang L., Pan Y.-Z., Jiang B.-B., Zhang F. The overexpression of a transcription factor gene VbWRKY32 enhances the cold tolerance in Verbena bonariensis. Front. Plant Sci. 2020;10:1746.

    Not in our library10.3389/fpls.2019.01746

  75. 75.

    Chanwala J., Satpati S., Dixit A., Parida A., Giri M.K., Dey N. Genome-wide identification and expression analysis of WRKY transcription factors in pearl millet (Pennisetum glaucum) under dehydration and salinity stress. BMC Genom. 2020;21:1-16.

    Not in our library10.1186/s12864-020-6622-0

  76. 76.

    Zhao K., Zhang D., Lv K., Zhang X., Cheng Z., Li R., Zhou B., Jiang T. Functional characterization of poplar WRKY75 in salt and osmotic tolerance. Plant Sci. 2019;289:110259.

    Not in our library10.1016/j.plantsci.2019.110259

  77. 77.

    Anjum S.A., Xie X.-Y., Wang L.-C., Saleem M.F., Man C., Lei W. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agr. Res. 2011;6:2026-2032.

    Not in our library10.5897/ajar10.027

  78. 78.

    Sakuma Y., Maruyama K., Osakabe Y., Qin F., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell. 2006;18:1292-1309.

    Not in our library10.1105/tpc.105.035881

  79. 79.

    Hassan S., Lethin J., Blomberg R., Mousavi H., Aronsson H. In silico based screening of WRKY genes for identifying functional genes regulated by WRKY under salt stress. Comput. Biol. Chem. 2019;83:107131.

    Not in our library10.1016/j.compbiolchem.2019.107131

  80. 80.

    Linxiao W., Song A., Gao C., Wang L., Wang Y., Sun J., Jiang J., Chen F., Chen S. Chrysanthemum WRKY gene CmWRKY17 negatively regulates salt stress tolerance in transgenic chrysanthemum and Arabidopsis plants. Plant Cell Rep. 2015;34:1365-1378.

    Not in our library10.1007/s00299-015-1793-x

  81. 81.

    Shen Z., Yao J., Sun J., Chang L., Wang S., Ding M., Qian Z., Zhang H., Zhao N., Sa G., et al. Populus euphratica HSF binds the promoter of WRKY1 to enhance salt tolerance. Plant Sci. 2015;235:89-100.

    Not in our library10.1016/j.plantsci.2015.03.006

  82. 82.

    Jaglo-Ottosen K.R. Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science. 1998;280:104-106.

    Not in our library10.1126/science.280.5360.104

  83. 83.
    Os MADS 57 together with Os TB 1 coordinates transcription of its target Os WRKY 94 and D14 to switch its organogenesis to defense for cold adaptation in rice · 2018
    No notice
  84. 84.
    The effect of experimental warming on leaf functional traits, leaf structure and leaf biochemistry in <it>Arabidopsis thaliana</it> · 2011
    Not checked
  85. 85.

    Liu H.-T., Li G.-L., Chang H., Sun D.-Y., Zhou R.-G., Li B. Calmodulin-binding protein phosphatase PP7 is involved in thermotolerance in Arabidopsis. Plant Cell Environ. 2007;30:156-164.

    Not in our library10.1111/j.1365-3040.2006.01613.x

  86. 86.

    Larkindale J., Huang B. Effects of abscisic acid, salicylic acid, ethylene and hydrogen peroxide in thermotolerance and recovery for creeping bentgrass. Plant Growth Regul. 2005;47:17-28.

    Not in our library10.1007/s10725-005-1536-z

  87. 87.

    Zhao J., He Q., Chen G., Wang L., Jin B. Regulation of non-coding RNAs in heat stress responses of plants. Front. Plant Sci. 2016;7:1213.

    Not in our library10.3389/fpls.2016.01213

  88. 88.

    Gong X.-Q., Hu J.-B., Liu J.-H. Cloning and characterization of FcWRKY40, A WRKY transcription factor from Fortunella crassifolia linked to oxidative stress tolerance. Plant Cell Tissue Organ Cult. PCTOC. 2014;119:197-210.

    Not in our library10.1007/s11240-014-0526-0

  89. 89.

    Cheong Y.H., Chang H.-S., Gupta R., Wang X., Zhu T., Luan S. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 2002;129:661-677.

    Not in our library10.1104/pp.002857

  90. 90.

    Robatzek S., Somssich I.E. A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. Plant J. 2001;28:123-133.

    Not in our library10.1046/j.1365-313x.2001.01131.x

  91. 91.

    Kilian J., Whitehead D., Horak J., Wanke D., Weinl S., Batistic O., D’Angelo C., Bornberg-Bauer E., Kudla J., Harter K. The AtGenExpress global stress expression data set: Protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. Plant J. 2007;50:347-363.

    Not in our library10.1111/j.1365-313x.2007.03052.x

  92. 92.

    Han Y., Zhang X., Wang Y., Ming F. The suppression of WRKY44 by GIGANTEA-miR172 pathway is involved in drought response of Arabidopsis thaliana. PLoS ONE. 2013;8:e73541.

    Not in our library10.1371/journal.pone.0073541

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