Abstract
Main conclusion
This review article explores the intricate role, regulation, and signaling mechanisms of WRKY TFs in response to biotic stress, particularly emphasizing their pivotal role in the trophism of plant-pathogen interactions.
Abstract
Transcription factors (TFs) play a vital role in governing both plant defense and development by controlling the expression of various downstream target genes. Early studies have shown the differential expression of certain WRKY transcription factors by microbial infections. Several transcriptome-wide studies later demonstrated that diverse sets of WRKYs are significantly activated in the early stages of viral, bacterial, and fungal infections. Furthermore, functional investigations indicated that overexpression or silencing of certain WRKY genes in plants can drastically alter disease symptoms as well as pathogen multiplication rates. Hence the new aspects of pathogen-triggered WRKY TFs mediated regulation of plant defense can be explored. The already recognized roles of WRKYs include transcriptional regulation of defense-related genes, modulation of hormonal signaling, and participation in signal transduction pathways. Some WRKYs have been shown to directly bind to pathogen effectors, acting as decoys or resistance proteins. Notably, the signaling molecules like salicylic acid, jasmonic acid, and ethylene which are associated with plant defense significantly increase the expression of several WRKYs. Moreover, induction of WRKY genes or heightened WRKY activities is also observed during ISR triggered by the beneficial microbes which protect the plants from subsequent pathogen infection. To understand the contribution of WRKY TFs towards disease resistance and their exact metabolic functions in infected plants, further studies are required. This review article explores the intrinsic transcriptional regulation, signaling mechanisms, and hormonal crosstalk governed by WRKY TFs in plant disease defense response, particularly emphasizing their specific role against different biotrophic, hemibiotrophic, and necrotrophic pathogen infections.
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References
Aamir M, Singh VK, Dubey MK, Kashyap SP, Zehra A, Upadhyay RS, Singh S (2018) Structural and functional dissection of differentially expressed tomato WRKY transcripts in host defense response against the vascular wilt pathogen (Fusarium oxysporum f. sp. lycopersici). PLoS ONE 13(4):e0193922. https://doi.org/10.1371/journal.pone.0193922
Abbruscato P, Nepusz T, Mizzi L, Del Corvo M, Morandini P, Fumasoni I, Michel C, Paccanaro A, Guiderdoni E, Schaffrath U, Morel JB, Piffanelli P, Faivre-Rampant O (2012) OsWRKY22, a monocot WRKY gene, plays a role in the resistance response to blast. Mol Plant Pathol 13(8):828–841. https://doi.org/10.1111/j.1364-3703.2012.00795.x
Abd-Ellatif S, Ibrahim AA, Safhi FA, Abdel Razik ES, Kabeil SSA, Aloufi S, Alyamani AA, Basuoni MM, SM AL, Elshafie HS, (2022) Green synthesized of Thymus vulgaris Chitosan nanoparticles induce relative WRKY-genes expression in Solanum lycopersicum against Fusarium solani, the causal agent of root rot disease. Plants (basel) 11(22):3129. https://doi.org/10.3390/plants11223129
Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y, Yaeno T, Shirasu K, Yoshioka H (2015) WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. Plant Cell 27(9):2645–2663. https://doi.org/10.1105/tpc.15.00213
Agrios GN (2008) Transmission of plant diseases by insects. Encyclopedia of entomology. 3853–3885
Ahuja I, Rohloff J, Bones AM (2011) Defence mechanisms of Brassicaceae: implications for plant-insect interactions and potential for integrated pest management. Sustain Agric 2:623–670
Alfieri M, Vaccaro MC, Cappetta E, Ambrosone A, De Tommasi N, Leone A (2018) Coactivation of MEP-biosynthetic genes and accumulation of abietane diterpenes in Salvia sclarea by heterologous expression of WRKY and MYC2 transcription factors. Sci Rep 8(1):11009
Alvarez SE, Harikumar KB, Hait NC, Allegood J, Strub GM, Kim EY, Maceyka M, Jiang H, Luo C, Kordula T (2010) Sphingosine-1-phosphate is a missing cofactor for the E3 ubiquitin ligase TRAF2. Nature 465(7301):1084–1088
Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NH, Zhu S, Qiu JL, Micheelsen P, Rocher A, Petersen M, Newman MA, Bjorn Nielsen H, Hirt H, Somssich I, Mattsson O, Mundy J (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. EMBO J 24(14):2579–2589. https://doi.org/10.1038/sj.emboj.7600737
Asai S, Ohta K, Yoshioka H (2008) MAPK signaling regulates nitric oxide and NADPH oxidase-dependent oxidative bursts in Nicotiana benthamiana. Plant Cell 20(5):1390–1406. https://doi.org/10.1105/tpc.107.055855
Atamian HS, Eulgem T, Kaloshian I (2012) SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta 235:299–309
Bahrini I, Sugisawa M, Kikuchi R, Ogawa T, Kawahigashi H, Ban T, Handa H (2011) Characterization of a wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants. Breed Sci 61:121–129
Bai H, Si H, Zang J, Pang X, Yu L, Cao H, Xing J, Zhang K, Dong J (2021) Comparative proteomic analysis of the defense response to Gibberella stalk rot in maize and reveals that ZmWRKY83 is involved in plant disease resistance. Front Plant Sci 12:694973
Barna B, Fodor J, Harrach BD, Pogany M, Kiraly Z (2012) The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiol Biochem 59:37–43. https://doi.org/10.1016/j.plaphy.2012.01.014
Bhattarai KK, Atamian HS, Kaloshian I, Eulgem T (2010) WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant J 63(2):229–240. https://doi.org/10.1111/j.1365-313X.2010.04232.x
Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol 159(1):266–285
Booth BD, Murphy SD, Swanton CJ (2004) Invasive ecology of weeds in agricultural systems. Weed biology and management. Springer, The Netherland, pp 29–45. https://doi.org/10.1007/978-94-017-0552-3_2
Brotman Y, Landau U, Cuadros-Inostroza A, Tohge T, Fernie AR, Chet I, Viterbo A, Willmitzer L (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog 9(3):e1003221. https://doi.org/10.1371/journal.ppat.1003221
Cai M, Qiu D, Yuan T, Ding X, Li H, Duan L, Xu C, Li X, Wang S (2008) Identification of novel pathogen-responsive cis-elements and their binding proteins in the promoter of OsWRKY13, a gene regulating rice disease resistance. Plant Cell Environ 31(1):86–96. https://doi.org/10.1111/j.1365-3040.2007.01739.x
Cai Y, Chen X, Xie K, Xing Q, Wu Y, Li J, Du C, Sun Z, Guo Z (2014) Dlf1, a WRKY transcription factor, is involved in the control of flowering time and plant height in rice. PLoS ONE 9(7):e102529. https://doi.org/10.1371/journal.pone.0102529
Cai H, Yang S, Yan Y, Xiao Z, Cheng J, Wu J, Qiu A, Lai Y, Mou S, Guan D, Huang R, He S (2015) CaWRKY6 transcriptionally activates CaWRKY40, regulates Ralstonia solanacearum resistance, and confers high-temperature and high-humidity tolerance in pepper. J Exp Bot 66(11):3163–3174. https://doi.org/10.1093/jxb/erv125
Chanwala J, Satpati S, Dixit A, Parida A, Giri MK, Dey N (2020) Genome-wide identification and expression analysis of WRKY transcription factors in pearl millet (Pennisetum glaucum) under dehydration and salinity stress. BMC Genomics 21(1):231. https://doi.org/10.1186/s12864-020-6622-0
Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129(2):706–716. https://doi.org/10.1104/pp.001057
Chen YF, Li LQ, Xu Q, Kong YH, Wang H, Wu WH (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21(11):3554–3566. https://doi.org/10.1105/tpc.108.064980
Chen L, Song Y, Li S, Zhang L, Zou C, Yu D (2012) The role of WRKY transcription factors in plant abiotic stresses. Biochim Biophys Acta 2:120–128. https://doi.org/10.1016/j.bbagrm.2011.09.002
Chen L, Zhang L, Li D, Wang F, Yu D (2013a) WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proc Natl Acad Sci 110(21):1963–1971
Chen X, Liu J, Lin G, Wang A, Wang Z, Lu G (2013b) Overexpression of AtWRKY28 and AtWRKY75 in Arabidopsis enhances resistance to oxalic acid and Sclerotinia sclerotiorum. Plant Cell Rep 32(10):1589–1599. https://doi.org/10.1007/s00299-013-1469-3
Chen X, Li C, Wang H, Guo Z (2019) WRKY transcription factors: evolution, binding, and action. Phytopathol Res 1(1):13. https://doi.org/10.1186/s42483-019-0022-x
Chen T, Li Y, Xie L, Hao X, Liu H, Qin W, Wang C, Yan X, Wu-Zhang K, Yao X (2021) AaWRKY17, a positive regulator of artemisinin biosynthesis, is involved in resistance to Pseudomonas syringae in Artemisia annua. Hortic Res 8:217
Cheng H, Liu H, Deng Y, Xiao J, Li X, Wang S (2015) The WRKY45-2 WRKY13 WRKY42 transcriptional regulatory cascade is required for rice resistance to fungal pathogen. Plant Physiol 167(3):1087–1099. https://doi.org/10.1104/pp.114.256016
Chinnapandi B, Bucki P, Braun Miyara S (2017) SlWRKY45, nematode-responsive tomato WRKY gene, enhances susceptibility to the root knot nematode. M Javanica Infect Plant Signal Behav 12(12):e1356530. https://doi.org/10.1080/15592324.2017.1356530
Chujo T, Takai R, Akimoto-Tomiyama C, Ando S, Minami E, Nagamura Y, Kaku H, Shibuya N, Yasuda M, Nakashita H, Umemura K, Okada A, Okada K, Nojiri H, Yamane H (2007) Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. Biochim Biophys Acta 1769(7–8):497–505. https://doi.org/10.1016/j.bbaexp.2007.04.006
Chujo T, Miyamoto K, Shimogawa T, Shimizu T, Otake Y, Yokotani N, Nishizawa Y, Shibuya N, Nojiri H, Yamane H, Minami E, Okada K (2013) OsWRKY28, a PAMP-responsive transrepressor, negatively regulates innate immune responses in rice against rice blast fungus. Plant Mol Biol 82(1–2):23–37. https://doi.org/10.1007/s11103-013-0032-5
Chujo T, Miyamoto K, Ogawa S, Masuda Y, Shimizu T, Kishi-Kaboshi M, Takahashi A, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K (2014) Overexpression of phosphomimic mutated OsWRKY53 leads to enhanced blast resistance in rice. PLoS ONE 9(6):e98737. https://doi.org/10.1371/journal.pone.0098737
Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68(1–2):81–92. https://doi.org/10.1007/s11103-008-9353-1
Contreras-Cornejo HA, Macias-Rodriguez L, Cortes-Penagos C, Lopez-Bucio J (2009) Trichoderma virens, a plant beneficial fungus, enhances biomass production and promotes lateral root growth through an auxin-dependent mechanism in Arabidopsis. Plant Physiol 149(3):1579–1592. https://doi.org/10.1104/pp.108.130369
Cristina MS, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649
Cui H, Tsuda K, Parker JE (2015) Effector-triggered immunity: from pathogen perception to robust defense. Annu Rev Plant Biol 66:487–511. https://doi.org/10.1146/annurev-arplant-050213-040012
Dabi M, Agarwal P, Agarwal PK (2020) Overexpression of JcWRKY2 confers increased resistance towards Macrophomina phaseolina in transgenic tobacco. 3 Biotech 10(11):490. https://doi.org/10.1007/s13205-020-02490-0
Dang FF, Wang YN, Yu L, Eulgem T, Lai Y, Liu ZQ, Wang X, Qiu AL, Zhang TX, Lin J, Chen YS, Guan DY, Cai HY, Mou SL, He SL (2013) 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 36(4):757–774. https://doi.org/10.1111/pce.12011
Davis RJ (1993) The mitogen-activated protein kinase signal transduction pathway. J Biol Chem 268(20):14553–14556
De Vos M, Van Oosten VR, Van Poecke RM, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CM (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18(9):923–937. https://doi.org/10.1094/MPMI-18-0923
Dey S, Wenig M, Langen G, Sharma S, Kugler KG, Knappe C, Hause B, Bichlmeier M, Babaeizad V, Imani J, Janzik I, Stempfl T, Huckelhoven R, Kogel KH, Mayer KF, Vlot AC (2014) Bacteria-triggered systemic immunity in barley is associated with WRKY and ETHYLENE RESPONSIVE FACTORs but not with salicylic acid. Plant Physiol 166(4):2133–2151. https://doi.org/10.1104/pp.114.249276
Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51(1):21–37. https://doi.org/10.1023/a:1020780022549
Dou L, Zhang X, Pang C, Song M, Wei H, Fan S, Yu S (2014) Genome-wide analysis of the WRKY gene family in cotton. Mol Genet Genomics 289(6):1103–1121. https://doi.org/10.1007/s00438-014-0872-y
Duan Y, Jiang Y, Ye S, Karim A, Ling Z, He Y, Yang S, Luo K (2015) PtrWRKY73, a salicylic acid-inducible poplar WRKY transcription factor, is involved in disease resistance in Arabidopsis thaliana. Plant Cell Rep 34(5):831–841. https://doi.org/10.1007/s00299-015-1745-5
Dutta A, Choudhary P, Caruana J, Raina R (2017) JMJ 27, an Arabidopsis H3K9 histone demethylase, modulates defense against Pseudomonas syringae and flowering time. Plant J 91(6):1015–1028
Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206. https://doi.org/10.1016/s1360-1385(00)01600-9
Fan C, Yao H, Qiu Z, Ma H, Zeng B (2018) Genome-wide analysis of Eucalyptus grandis WRKY genes family and their expression profiling in response to hormone and abiotic stress treatment. Gene 678:38–48
Freeborough W, Gentle N, Rey MEC (2021) WRKY transcription factors in cassava contribute to regulation of tolerance and susceptibility to cassava mosaic disease through stress responses. Viruses 13(9):1820. https://doi.org/10.3390/v13091820
Fu R, Zhang M, Zhao Y, He X, Ding C, Wang S, Feng Y, Song X, Li P, Wang B (2017) Identification of salt tolerance-related microRNAs and their targets in maize (Zea mays L.) using high-throughput sequencing and degradome analysis. Front Plant Sci 8:864
Fu J, Liu Q, Wang C, Liang J, Liu L, Wang Q (2018) ZmWRKY79 positively regulates maize phytoalexin biosynthetic gene expression and is involved in stress response. J Exp Bot 69(3):497–510
Gallou A, Declerck S, Cranenbrouck S (2012) Transcriptional regulation of defence genes and involvement of the WRKY transcription factor in arbuscular mycorrhizal potato root colonization. Funct Integr Genomics 12(1):183–198. https://doi.org/10.1007/s10142-011-0241-4
Gao QM, Venugopal S, Navarre D, Kachroo A (2011) Low oleic acid-derived repression of jasmonic acid-inducible defense responses requires the WRKY50 and WRKY51 proteins. Plant Physiol 155(1):464–476. https://doi.org/10.1104/pp.110.166876
Gao R, Liu P, Yong Y, Wong SM (2016) Genome-wide transcriptomic analysis reveals correlation between higher WRKY61 expression and reduced symptom severity in Turnip crinkle virus infected Arabidopsis thaliana. Sci Rep 6:24604. https://doi.org/10.1038/srep24604
Gao YF, Liu JK, Yang FM, Zhang GY, Wang D, Zhang L, Ou YB, Yao YA (2020) The WRKY transcription factor WRKY8 promotes resistance to pathogen infection and mediates drought and salt stress tolerance in Solanum lycopersicum. Physiol Plant 168(1):98–117. https://doi.org/10.1111/ppl.12978
Giacomelli JI, Weigel D, Chan RL, Manavella PA (2012) Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol 195(4):766–773. https://doi.org/10.1111/j.1469-8137.2012.04259.x
Goel R, Pandey A, Trivedi PK, Asif MH (2016) Genome-wide analysis of the musa WRKY gene family: evolution and differential expression during development and stress. Front Plant Sci 7:299. https://doi.org/10.3389/fpls.2016.00299
Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148(1):358–368. https://doi.org/10.1104/pp.108.119131
Grunewald W, De Smet I, Lewis DR, Löfke C, Jansen L, Goeminne G, Vanden Bossche R, Karimi M, De Rybel B, Vanholme B (2012a) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proc Natl Acad Sci 109(5):1554–1559
Grunewald W, De Smet I, Lewis DR, Löfke C, Jansen L, Goeminne G, Vanden Bossche R, Karimi M, De Rybel B, Vanholme B, Teichmann T, Boerjan W, Van Montagu MCE, Gheysen G, Muday GK, Friml J, Beeckman T (2012b) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proc Natl Acad Sci 109(5):1554–1559. https://doi.org/10.1073/pnas.1121134109
Guillaumie S, Mzid R, Méchin V, Léon C, Hichri I, Destrac-Irvine A, Trossat-Magnin C, Delrot S, Lauvergeat V (2010) The grapevine transcription factor WRKY2 influences the lignin pathway and xylem development in tobacco. Plant Mol Biol 72(1):215–234. https://doi.org/10.1007/s11103-009-9563-1
Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297. https://doi.org/10.1016/j.plantsci.2011.12.003
Hu Z, Wang R, Zheng M, Liu X, Meng F, Wu H, Yao Y, Xin M, Peng H, Ni Z (2018) Ta WRKY 51 promotes lateral root formation through negative regulation of ethylene biosynthesis in wheat (Triticum aestivum L.). Plant J 96(2):372–388
Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genomics 287(6):495–513. https://doi.org/10.1007/s00438-012-0696-6
Huh SU, Choi LM, Lee GJ, Kim YJ, Paek KH (2012) Capsicum annuum WRKY transcription factor d (CaWRKYd) regulates hypersensitive response and defense response upon Tobacco mosaic virus infection. Plant Sci 197:50–58. https://doi.org/10.1016/j.plantsci.2012.08.013
Humphreys JM, Hemm MR, Chapple C (1999) New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450-dependent monooxygenase. Proc Natl Acad Sci 96(18):10045–10050. https://doi.org/10.1073/pnas.96.18.10045
Hwang SH, Kwon SI, Jang JY, Fang IL, Lee H, Choi C, Park S, Ahn I, Bae SC, Hwang DJ (2016) OsWRKY51, a rice transcription factor, functions as a positive regulator in defense response against Xanthomonas oryzae pv. oryzae. Plant Cell Rep 35(9):1975–1985. https://doi.org/10.1007/s00299-016-2012-0
Ichimura K, Shinozaki K, Tena G, Sheen J, Henry Y, Champion A, Kreis M, Zhang S, Hirt H, Wilson C (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7(7):301–308
Ifnan Khan M, Zhang Y, Liu Z, Hu J, Liu C, Yang S, Hussain A, Furqan Ashraf M, Noman A, Shen L, Xia X, Yang F, Guan D, He S (2018) CaWRKY40b in pepper acts as a negative regulator in response to Ralstonia solanacearum by directly modulating defense genes including CaWRKY40. Int J Mol Sci 19(5):1403. https://doi.org/10.3390/ijms19051403
Ishihama N, Yamada R, Yoshioka M, Katou S, Yoshioka H (2011) Phosphorylation of the Nicotiana benthamiana WRKY8 transcription factor by MAPK functions in the defense response. Plant Cell 23(3):1153–1170. https://doi.org/10.1105/tpc.110.081794
Jalmi SK, Sinha AK (2016) Functional involvement of a mitogen activated protein kinase module, OsMKK3-OsMPK7-OsWRK30 in mediating resistance against Xanthomonas oryzae in Rice. Sci Rep 6(1):37974. https://doi.org/10.1038/srep37974
Jaskiewicz M, Conrath U, Peterhänsel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12(1):50–55
Javed T, Shabbir R, Ali A, Afzal I, Zaheer U, Gao SJ (2020) Transcription factors in plant stress responses: challenges and potential for sugarcane improvement. Plants (basel) 9(4):491. https://doi.org/10.3390/plants9040491
Javed T, Zhou JR, Li J, Hu ZT, Wang QN, Gao SJ (2022) Identification and expression profiling of WRKY family genes in sugarcane in response to bacterial pathogen infection and nitrogen implantation dosage. Front Plant Sci 13:917953. https://doi.org/10.3389/fpls.2022.917953
Jha UC, Bohra A, Pandey S, Parida SK (2020) Breeding, genetics, and genomics approaches for improving fusarium wilt resistance in major grain legumes. Front Genet 11:1001. https://doi.org/10.3389/fgene.2020.01001
Jiang Y, Yu D (2016) The WRKY57 transcription factor affects the expression of jasmonate ZIM-domain genes transcriptionally to compromise botrytis cinerea resistance. Plant Physiol 171(4):2771–2782. https://doi.org/10.1104/pp.16.00747
Jiang X, Cao Y, Wang Y, Liu L, Shen F, Wang R (2010) A unique approach to the concise synthesis of highly optically active spirooxazolines and the discovery of a more potent oxindole-type phytoalexin analogue. J Am Chem Soc 132(43):15328–15333. https://doi.org/10.1021/ja106349m
Jiang C, Shen QJ, Wang B, He B, Xiao S, Chen L, Yu T, Ke X, Zhong Q, Fu J, Chen Y, Wang L, Yin F, Zhang D, Ghidan W, Huang X, Cheng Z (2017) Transcriptome analysis of WRKY gene family in Oryza officinalis Wall ex Watt and WRKY genes involved in responses to Xanthomonas oryzae pv. oryzae stress. PLoS ONE 12(11):e0188742. https://doi.org/10.1371/journal.pone.0188742
Jiang J, Xi H, Dai Z, Lecourieux F, Yuan L, Liu X, Patra B, Wei Y, Li S, Wang L (2019) VvWRKY8 represses stilbene synthase genes through direct interaction with VvMYB14 to control resveratrol biosynthesis in grapevine. J Exp Bot 70(2):715–729
Jing S, Zhou X, Song Y, Yu D (2009) Heterologous expression of OsWRKY23 gene enhances pathogen defense and dark-induced leaf senescence in Arabidopsis. Plant Growth Regul 58(2):181–190. https://doi.org/10.1007/s10725-009-9366-z
Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329. https://doi.org/10.1038/nature05286
Kage U, Yogendra KN, Kushalappa AC (2017) TaWRKY70 transcription factor in wheat QTL-2DL regulates downstream metabolite biosynthetic genes to resist Fusarium graminearum infection spread within spike. Sci Rep 7(1):42596
Kajla M, Roy A, Singh IK, Singh A (2023) Regulation of the regulators: transcription factors controlling biosynthesis of plant secondary metabolites during biotic stresses and their regulation by miRNAs. Front Plant Sci 14:1126567. https://doi.org/10.3389/fpls.2023.1126567
Kang G, Yan D, Chen X, Li Y, Yang L, Zeng R (2020) Molecular characterization and functional analysis of a novel WRKY transcription factor HbWRKY83 possibly involved in rubber production of Hevea brasiliensis. Plant Physiol Biochem 155:483–493. https://doi.org/10.1016/j.plaphy.2020.08.013
Karre S, Kumar A, Yogendra K, Kage U, Kushalappa A, Charron J-B (2019) HvWRKY23 regulates flavonoid glycoside and hydroxycinnamic acid amide biosynthetic genes in barley to combat Fusarium head blight. Plant Mol Biol 100:591–605
Katou S, Yoshioka H, Kawakita K, Rowland O, Jones JD, Mori H, Doke N (2005) Involvement of PPS3 phosphorylated by elicitor-responsive mitogen-activated protein kinases in the regulation of plant cell death. Plant Physiol 139(4):1914–1926. https://doi.org/10.1104/pp.105.066795
Khan M, Khan AU, Hasan MA, Yadav KK, Pinto MMC, Malik N, Yadav VK, Khan AH, Islam S, Sharma GK (2021) Agro-nanotechnology as an emerging field: a novel sustainable approach for improving plant growth by reducing biotic stress. Appl Sci 11(5):2282
Khan I, Jan R, Asaf S, Khan AL, Bilal S, Kim KM, Al-Harrasi A (2022) Genome and transcriptome-wide analysis of OsWRKY and OsNAC gene families in Oryza sativa and their response to white-backed planthopper infestation. Int J Mol Sci 23(23):15396. https://doi.org/10.3390/ijms232315396
Kim KC, Fan B, Chen Z (2006) Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol 142(3):1180–1192. https://doi.org/10.1104/pp.106.082487
Kim KC, Lai Z, Fan B, Chen Z (2008a) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20(9):2357–2371. https://doi.org/10.1105/tpc.107.055566
Kim SS, Ko YJ, Jang JY, Lee T, Lim MH, Park SY, Bae SC, Yun CH, Park BS, Hwang DJ (2008b) Isolation and expression analysis of Brassica rapa WRKY 7. Plant Pathol J 24(4):478–481
Kishi-Kaboshi M, Okada K, Kurimoto L, Murakami S, Umezawa T, Shibuya N, Yamane H, Miyao A, Takatsuji H, Takahashi A, Hirochika H (2010) A rice fungal MAMP-responsive MAPK cascade regulates metabolic flow to antimicrobial metabolite synthesis. Plant J 63(4):599–612. https://doi.org/10.1111/j.1365-313X.2010.04264.x
Koo SC, Moon BC, Kim JK, Kim CY, Sung SJ, Kim MC, Cho MJ, Cheong YH (2009) OsBWMK1 mediates SA-dependent defense responses by activating the transcription factor OsWRKY33. Biochem Biophys Res Commun 387(2):365–370. https://doi.org/10.1016/j.bbrc.2009.07.026
Kravchuk Z, Vicedo B, Flors V, Camanes G, Gonzalez-Bosch C, Garcia-Agustin P (2011) Priming for JA-dependent defenses using hexanoic acid is an effective mechanism to protect Arabidopsis against B. cinerea. J Plant Physiol 168(4):359–366. https://doi.org/10.1016/j.jplph.2010.07.028
Kuki Y, Ohno R, Yoshida K, Takumi S (2020) Heterologous expression of wheat WRKY transcription factor genes transcriptionally activated in hybrid necrosis strains alters abiotic and biotic stress tolerance in transgenic Arabidopsis. Plant Physiol Biochem 150:71–79. https://doi.org/10.1016/j.plaphy.2020.02.029
Kumar D, Kapoor A, Singh D, Satapathy L, Singh AK, Kumar M, Prabhu KV, Mukhopadhyay K (2014) Functional characterisation of a WRKY transcription factor of wheat and its expression analysis during leaf rust pathogenesis. Funct Plant Biol 41(12):1295–1309. https://doi.org/10.1071/FP14077
Kyndt T, Denil S, Haegeman A, Trooskens G, Bauters L, Van Criekinge W, De Meyer T, Gheysen G (2012) Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytol 196(3):887–900. https://doi.org/10.1111/j.1469-8137.2012.04311.x
Lai Z, Vinod K, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol 8:68. https://doi.org/10.1186/1471-2229-8-68
Lan A, Huang J, Zhao W, Peng Y, Chen Z, Kang D (2013) A salicylic acid-induced rice (Oryza sativa L.) transcription factor OsWRKY77 is involved in disease resistance of Arabidopsis thaliana. Plant Biol (stuttg) 15(3):452–461. https://doi.org/10.1111/j.1438-8677.2012.00664.x
Lanz T, Tropf S, Marner F, Schröder J, Schröder G (1991) The role of cysteines in polyketide synthases. Site-directed mutagenesis of resveratrol and chalcone synthases, two key enzymes in different plant-specific pathways. J Biol Chem 266(15):9971–9976
Li J-b, Luan Y-s (2014) Molecular cloning and characterization of a pathogen-induced WRKY transcription factor gene from late blight resistant tomato varieties Solanum pimpinellifolium L3708. Physiol Mol Plant Pathol 87:25–31
Li J, Brader G, Kariola T, Palva ET (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46(3):477–491. https://doi.org/10.1111/j.1365-313X.2006.02712.x
Li G, Meng X, Wang R, Mao G, Han L, Liu Y, Zhang S (2012) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8(6):e1002767. https://doi.org/10.1371/journal.pgen.1002767
Li S, Zhang P, Zhang M, Fu C, Yu L (2013) Functional analysis of a WRKY transcription factor involved in transcriptional activation of the DBAT gene in Taxus chinensis. Plant Biol 15(1):19–26
Li J-b, Luan Y-s, Liu Z (2015a) SpWRKY1 mediates resistance to Phytophthora infestans and tolerance to salt and drought stress by modulating reactive oxygen species homeostasis and expression of defense-related genes in tomato. Plant Cell Tiss Organ Cult (PCTOC) 123(1):67–81. https://doi.org/10.1007/s11240-015-0815-2
Li JB, Luan YS, Liu Z (2015b) Overexpression of SpWRKY1 promotes resistance to Phytophthora nicotianae and tolerance to salt and drought stress in transgenic tobacco. Physiol Plant 155(3):248–266. https://doi.org/10.1111/ppl.12315
Li P, Song A, Gao C, Jiang J, Chen S, Fang W, Zhang F, Chen F (2015c) The over-expression of a chrysanthemum WRKY transcription factor enhances aphid resistance. Plant Physiol Biochem 95:26–34. https://doi.org/10.1016/j.plaphy.2015.07.002
Li J, Zhu L, Hull JJ, Liang S, Daniell H, Jin S, Zhang X (2016) Transcriptome analysis reveals a comprehensive insect resistance response mechanism in cotton to infestation by the phloem feeding insect Bemisia tabaci (whitefly). Plant Biotechnol J 14(10):1956–1975. https://doi.org/10.1111/pbi.12554
Li D, Liu P, Yu J, Wang L, Dossa K, Zhang Y, Zhou R, Wei X, Zhang X (2017) Genome-wide analysis of WRKY gene family in the sesame genome and identification of the WRKY genes involved in responses to abiotic stresses. BMC Plant Biol 17(1):152. https://doi.org/10.1186/s12870-017-1099-y
Li H, Wu J, Shang X, Geng M, Gao J, Zhao S, Yu X, Liu D, Kang Z, Wang X, Wang X (2020a) WRKY transcription factors shared by BTH-induced resistance and NPR1-mediated acquired resistance improve broad-spectrum disease resistance in wheat. Mol Plant Microbe Interact 33(3):433–443. https://doi.org/10.1094/MPMI-09-19-0257-R
Li Z, Kim JH, Kim J, Lyu JI, Zhang Y, Guo H, Nam HG, Woo HR (2020b) ATM suppresses leaf senescence triggered by DNA double-strand break through epigenetic control of senescence-associated genes in Arabidopsis. New Phytol 227(2):473–484
Lippok B, Birkenbihl RP, Rivory G, Brummer J, Schmelzer E, Logemann E, Somssich IE (2007) Expression of AtWRKY33 encoding a pathogen- or PAMP-responsive WRKY transcription factor is regulated by a composite DNA motif containing W box elements. Mol Plant Microbe Interact 20(4):420–429. https://doi.org/10.1094/MPMI-20-4-0420
Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. J Plant Physiol 164(8):969–979. https://doi.org/10.1016/j.jplph.2006.07.006
Liu X, Song Y, Xing F, Wang N, Wen F, Zhu C (2016) GhWRKY25, a group I WRKY gene from cotton, confers differential tolerance to abiotic and biotic stresses in transgenic Nicotiana benthamiana. Protoplasma 253(5):1265–1281. https://doi.org/10.1007/s00709-015-0885-3
Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from ’omics to the field. Annu Rev Phytopathol 48:395–417. https://doi.org/10.1146/annurev-phyto-073009-114314
Lui S, Luo C, Zhu L, Sha R, Qu S, Cai B, Wang S (2017) Identification and expression analysis of WRKY transcription factor genes in response to fungal pathogen and hormone treatments in apple (Malus domestica). J Plant Biol 60:215–230
Maeo K, Hayashi S, Kojima-Suzuki H, Morikami A, Nakamura K (2001) Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins. Biosci Biotechnol Biochem 65(11):2428–2436. https://doi.org/10.1271/bbb.65.2428
Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23(4):1639–1653. https://doi.org/10.1105/tpc.111.084996
Martinez-Medina A, Fernandez I, Sanchez-Guzman MJ, Jung SC, Pascual JA, Pozo MJ (2013) Deciphering the hormonal signalling network behind the systemic resistance induced by Trichoderma harzianum in tomato. Front Plant Sci 4:206. https://doi.org/10.3389/fpls.2013.00206
Matsushita A, Inoue H, Goto S, Nakayama A, Sugano S, Hayashi N, Takatsuji H (2013) Nuclear ubiquitin proteasome degradation affects WRKY 45 function in the rice defense program. Plant J 73(2):302–313
Miao Y, Zentgraf U (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J 63(2):179–188
Moran-Diez E, Rubio B, Dominguez S, Hermosa R, Monte E, Nicolas C (2012) Transcriptomic response of Arabidopsis thaliana after 24 h incubation with the biocontrol fungus Trichoderma harzianum. J Plant Physiol 169(6):614–620. https://doi.org/10.1016/j.jplph.2011.12.016
Mukhtar MS, Deslandes L, Auriac MC, Marco Y, Somssich IE (2008) The Arabidopsis transcription factor WRKY27 influences wilt disease symptom development caused by Ralstonia solanacearum. Plant J 56(6):935–947. https://doi.org/10.1111/j.1365-313X.2008.03651.x
Murray SL, Ingle RA, Petersen LN, Denby KJ (2007) Basal resistance against Pseudomonas syringae in Arabidopsis involves WRKY53 and a protein with homology to a nematode resistance protein. Mol Plant Microbe Interact 20(11):1431–1438. https://doi.org/10.1094/MPMI-20-11-1431
Muthamilarasan M, Bonthala VS, Khandelwal R, Jaishankar J, Shweta S, Nawaz K, Prasad M (2015) Global analysis of WRKY transcription factor superfamily in Setaria identifies potential candidates involved in abiotic stress signaling. Front Plant Sci 6:910. https://doi.org/10.3389/fpls.2015.00910
Mzid R, Marchive C, Blancard D, Deluc L, Barrieu F, Corio-Costet MF, Drira N, Hamdi S, Lauvergeat V (2007) Overexpression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiol Plant 131(3):434–447. https://doi.org/10.1111/j.1399-3054.2007.00975.x
Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signalling. Trends Plant Sci 10(7):339–346. https://doi.org/10.1016/j.tplants.2005.05.009
Nakashima K, Jan A, Todaka D, Maruyama K, Goto S, Shinozaki K, Yamaguchi-Shinozaki K (2014) Comparative functional analysis of six drought-responsive promoters in transgenic rice. Planta 239(1):47–60. https://doi.org/10.1007/s00425-013-1960-7
Nguyễn PV, Bellafiore S, Petitot A-S, Haidar R, Bak A, Abed A, Gantet P, Mezzalira I, de Almeida EJ, Fernandez D (2014) Meloidogyne incognita-rice (Oryza sativa) interaction: a new model system to study plant-root-knot nematode interactions in monocotyledons. Rice 7(1):1–13
Nicol J, Turner S, Coyne DL, Nijs Ld, Hockland S, Maafi ZT (2011) Current nematode threats to world agriculture. Genomics and molecular genetics of plant-nematode interactions. Springer, The Netherlands, pp 21–43
Ning P, Liu C, Kang J, Lv J (2017) Genome-wide analysis of WRKY transcription factors in wheat (Triticum aestivum L.) and differential expression under water deficit condition. PeerJ 5:e3232. https://doi.org/10.7717/peerj.3232
Niu Y, Figueroa P, Browse J (2011) Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis. J Exp Bot 62(6):2143–2154. https://doi.org/10.1093/jxb/erq408
Nuruzzaman M, Cao H, Xiu H, Luo T, Li J, Chen X, Luo J, Luo Z (2016) Transcriptomics-based identification of WRKY genes and characterization of a salt and hormone-responsive PgWRKY1 gene in Panax ginseng. Acta Biochim Biophys Sin (shanghai) 48(2):117–131. https://doi.org/10.1093/abbs/gmv122
Obata T (2019) Metabolons in plant primary and secondary metabolism. Phytochem Rev 18(6):1483–1507. https://doi.org/10.1007/s11101-019-09619-x
Oh SK, Baek KH, Park JM, Yi SY, Yu SH, Kamoun S, Choi D (2008) Capsicum annuum WRKY protein CaWRKY1 is a negative regulator of pathogen defense. New Phytol 177(4):977–989. https://doi.org/10.1111/j.1469-8137.2007.02310.x
Pandey SP, Roccaro M, Schon M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64(6):912–923. https://doi.org/10.1111/j.1365-313X.2010.04387.x
Park CY, Lee JH, Yoo JH, Moon BC, Choi MS, Kang YH, Lee SM, Kim HS, Kang KY, Chung WS, Lim CO, Cho MJ (2005) WRKY group IId transcription factors interact with calmodulin. FEBS Lett 579(6):1545–1550. https://doi.org/10.1016/j.febslet.2005.01.057
Patra B, Schluttenhofer C, Wu Y, Pattanaik S, Yuan L (2013) Transcriptional regulation of secondary metabolite biosynthesis in plants. Biochim Biophys Acta (BBA) Gene Regul Mech 11:1236–1247. https://doi.org/10.1016/j.bbagrm.2013.09.006
Peng Y, Bartley LE, Chen X, Dardick C, Chern M, Ruan R, Canlas PE, Ronald PC (2008) OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol Plant 1(3):446–458. https://doi.org/10.1093/mp/ssn024
Phukan UJ, Jeena GS, Shukla RK (2016) WRKY transcription factors: molecular regulation and stress responses in plants. Front Plant Sci 7:760. https://doi.org/10.3389/fpls.2016.00760
Poosapati S, Poretsky E, Dressano K, Ruiz M, Vazquez A, Sandoval E, Estrada-Cardenas A, Duggal S, Lim J-H, Morris G (2022) A sorghum genome-wide association study (GWAS) identifies a WRKY transcription factor as a candidate gene underlying sugarcane aphid (Melanaphis sacchari) resistance. Planta 255(2):37
Qiu D, Xiao J, Ding X, Xiong M, Cai M, Cao Y, Li X, Xu C, Wang S (2007) OsWRKY13 mediates rice disease resistance by regulating defense-related genes in salicylate- and jasmonate-dependent signaling. Mol Plant Microbe Interact 20(5):492–499. https://doi.org/10.1094/MPMI-20-5-0492
Qiu D, Xiao J, Xie W, Liu H, Li X, Xiong L, Wang S (2008a) Rice gene network inferred from expression profiling of plants overexpressing OsWRKY13, a positive regulator of disease resistance. Mol Plant 1(3):538–551. https://doi.org/10.1093/mp/ssn012
Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J (2008b) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27(16):2214–2221
Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Curr Opin Plant Biol 1(5):404–411. https://doi.org/10.1016/s1369-5266(98)80264-1
Rinerson CI, Rabara RC, Tripathi P, Shen QJ, Rushton PJ (2015) The evolution of WRKY transcription factors. BMC Plant Biol 15:66. https://doi.org/10.1186/s12870-015-0456-y
Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16(9):1139–1149. https://doi.org/10.1101/gad.222702
Rosado D, Ackermann A, Spassibojko O, Rossi M, Pedmale UV (2022) WRKY transcription factors and ethylene signaling modify root growth during the shade-avoidance response. Plant Physiol 188(2):1294–1311. https://doi.org/10.1093/plphys/kiab493
Rushton PJ, Macdonald H, Huttly AK, Lazarus CM, Hooley R (1995) Members of a new family of DNA-binding proteins bind to a conserved cis-element in the promoters of alpha-Amy2 genes. Plant Mol Biol 29(4):691–702. https://doi.org/10.1007/BF00041160
Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15(5):247–258. https://doi.org/10.1016/j.tplants.2010.02.006
Sáenz-Mata J, Salazar-Badillo FB, Jiménez-Bremont JF (2014) Transcriptional regulation of Arabidopsis thaliana WRKY genes under interaction with beneficial fungus Trichoderma atroviride. Acta Physiol Plant 36(5):1085–1093. https://doi.org/10.1007/s11738-013-1483-7
Santner A, Estelle M (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J 61(6):1029–1040. https://doi.org/10.1111/j.1365-313X.2010.04112.x
Schon M, Toller A, Diezel C, Roth C, Westphal L, Wiermer M, Somssich IE (2013) Analyses of wrky18 wrky40 plants reveal critical roles of SA/EDS1 signaling and indole-glucosinolate biosynthesis for Golovinomyces orontii resistance and a loss-of resistance towards Pseudomonas syringae pv. tomato AvrRPS4. Mol Plant Microbe Interact 26(7):758–767. https://doi.org/10.1094/MPMI-11-12-0265-R
Schweizer F, Bodenhausen N, Lassueur S, Masclaux FG, Reymond P (2013) Differential contribution of transcription factors to Arabidopsis thaliana defense against Spodoptera littoralis. Front Plant Sci 4:13. https://doi.org/10.3389/fpls.2013.00013
Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Wu FQ, Wang XF, Du SY, Jiang T, Zhang XF, Zhao R, Sun HL, Liu R, Yu YT, Zhang DP (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22(6):1909–1935. https://doi.org/10.1105/tpc.110.073874
Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315(5815):1098–1103. https://doi.org/10.1126/science.1136372
Shen DW, Pouliot LM, Hall MD, Gottesman MM (2012) Cisplatin resistance: a cellular self-defense mechanism resulting from multiple epigenetic and genetic changes. Pharmacol Rev 64(3):706–721. https://doi.org/10.1124/pr.111.005637
Shimono M, Sugano S, Nakayama A, Jiang CJ, Ono K, Toki S, Takatsuji H (2007) Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance. Plant Cell 19(6):2064–2076. https://doi.org/10.1105/tpc.106.046250
Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43. https://doi.org/10.1146/annurev-phyto-073009-114450
Singh V, Roy S, Singh D, Nandi AK (2014) Arabidopsis flowering locus D influences systemic-acquired-resistance-induced expression and histone modifications of WRKY genes. J Biosci 39(1):119–126. https://doi.org/10.1007/s12038-013-9407-7
Singh AK, Kumar SR, Dwivedi V, Rai A, Pal S, Shasany AK, Nagegowda DA (2017) A WRKY transcription factor from Withania somnifera regulates triterpenoid withanolide accumulation and biotic stress tolerance through modulation of phytosterol and defense pathways. New Phytol 215(3):1115–1131
Singh D, Debnath P, Roohi SAP, Sane VA (2020) Expression of the tomato WRKY gene, SlWRKY23, alters root sensitivity to ethylene, auxin and JA and affects aerial architecture in transgenic Arabidopsis. Physiol Mol Biol Plants 26(6):1187–1199. https://doi.org/10.1007/s12298-020-00820-3
Skibbe M, Qu N, Galis I, Baldwin IT (2008a) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 Coordinate Responses to Herbivory. Plant Cell 20(7):1984–2000. https://doi.org/10.1105/tpc.108.058594
Skibbe M, Qu N, Galis I, Baldwin IT (2008b) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20(7):1984–2000. https://doi.org/10.1105/tpc.108.058594
Song Y, Gao J (2014) Genome-wide analysis of WRKY gene family in Arabidopsis lyrata and comparison with Arabidopsis thaliana and Populus trichocarpa. Chin Sci Bull 59(8):754–765. https://doi.org/10.1007/s11434-013-0057-9
Spanu PD, Panstruga R (2017) Editorial: biotrophic plant–microbe interactions. Front Plant Sci 8:192. https://doi.org/10.3389/fpls.2017.00192
Srivastava R, Sahoo L (2021) Balancing yield trade-off in legumes during multiple stress tolerance via strategic crosstalk by native NAC transcription factors. J Plant Biochem Biotechnol 30(4):708–729. https://doi.org/10.1007/s13562-021-00749-y
Srivastava R, Sahoo L (2022) Genome-wide analysis of cowpea NAC transcription factor family elucidating the genetic & molecular relationships that interface stress and growth regulatory signals. Plant Gene 31:100363. https://doi.org/10.1016/j.plgene.2022.100363
Srivastava R, Kumar S, Kobayashi Y, Kusunoki K, Tripathi P, Kobayashi Y, Koyama H, Sahoo L (2018) Comparative genome-wide analysis of WRKY transcription factors in two Asian legume crops: Adzuki bean and Mung bean. Sci Rep 8(1):16971. https://doi.org/10.1038/s41598-018-34920-8
Stout MJ, Thaler JS, Thomma BP (2006) Plant-mediated interactions between pathogenic microorganisms and herbivorous arthropods. Annu Rev Entomol 51:663–689. https://doi.org/10.1146/annurev.ento.51.110104.151117
Sun X-c, Gao Y-f, Li H-r, Yang S-z, Liu Y-s (2015) Over-expression of SlWRKY39 leads to enhanced resistance to multiple stress factors in tomato. J Plant Biol 58(1):52–60. https://doi.org/10.1007/s12374-014-0407-4
Sun S, Ren Y, Wang D, Farooq T, He Z, Zhang C, Li S, Yang X, Zhou X (2022) A group I WRKY transcription factor regulates mulberry mosaic dwarf-associated virus-triggered cell death in Nicotiana benthamiana. Mol Plant Pathol 23(2):237–253. https://doi.org/10.1111/mpp.13156
Tanaka S, Ishihama N, Yoshioka H, Huser A, O’Connell R, Tsuji G, Tsuge S, Kubo Y (2009) The Colletotrichum orbiculare SSD1 mutant enhances Nicotiana benthamiana basal resistance by activating a mitogen-activated protein kinase pathway. Plant Cell 21(8):2517–2526. https://doi.org/10.1105/tpc.109.068023
Tao Z, Liu H, Qiu D, Zhou Y, Li X, Xu C, Wang S (2009) A pair of allelic WRKY genes play opposite roles in rice–bacteria interactions. Plant Physiol 151(2):936–948. https://doi.org/10.1104/pp.109.145623
Tolosa LN, Zhang Z (2020) The role of major transcription factors in solanaceous food crops under different stress conditions: current and future perspectives. Plants (basel) 9(1):56. https://doi.org/10.3390/plants9010056
Turck F, Zhou A, Somssich IE (2004) Stimulus-dependent, promoter-specific binding of transcription factor WRKY1 to Its native promoter and the defense-related gene PcPR1-1 in Parsley. Plant Cell 16(10):2573–2585. https://doi.org/10.1105/tpc.104.024810
Villacastin AJ, Adams KS, Boonjue R, Rushton PJ, Han M, Shen JQ (2021) Dynamic differential evolution schemes of WRKY transcription factors in domesticated and wild rice. Sci Rep 11(1):14887. https://doi.org/10.1038/s41598-021-94109-4
Vo KTX, Kim CY, Hoang TV, Lee SK, Shirsekar G, Seo YS, Lee SW, Wang GL, Jeon JS (2017) OsWRKY67 plays a positive role in basal and XA21-mediated resistance in rice. Front Plant Sci 8:2220. https://doi.org/10.3389/fpls.2017.02220
Vogt T (2010) Phenylpropanoid biosynthesis. Mol Plant 3(1):2–20. https://doi.org/10.1093/mp/ssp106
Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2(11):e123. https://doi.org/10.1371/journal.ppat.0020123
Wang H, Hao J, Chen X, Hao Z, Wang X, Lou Y, Peng Y, Guo Z (2007) Overexpression of rice WRKY89 enhances ultraviolet B tolerance and disease resistance in rice plants. Plant Mol Biol 65(6):799–815. https://doi.org/10.1007/s11103-007-9244-x
Wang H, Avci U, Nakashima J, Hahn MG, Chen F, Dixon RA (2010) Mutation of WRKY transcription factors initiates pith secondary wall formation and increases stem biomass in dicotyledonous plants. Proc Natl Acad Sci 107(51):22338–22343. https://doi.org/10.1073/pnas.1016436107
Wang JN, Kuang JF, Shan W, Chen J, Xie H, Lu WJ, Chen JW, Chen JY (2012) Expression profiles of a banana fruit linker histone H1 gene MaHIS1 and its interaction with a WRKY transcription factor. Plant Cell Rep 31(8):1485–1494. https://doi.org/10.1007/s00299-012-1263-7
Wang M, Vannozzi A, Wang G, Liang YH, Tornielli GB, Zenoni S, Cavallini E, Pezzotti M, Cheng ZM (2014) Genome and transcriptome analysis of the grapevine (Vitis vinifera L.) WRKY gene family. Hortic Res 1:14016. https://doi.org/10.1038/hortres.2014.16
Wang H, Meng J, Peng X, Tang X, Zhou P, Xiang J, Deng X (2015) Rice WRKY4 acts as a transcriptional activator mediating defense responses toward Rhizoctonia solani, the causing agent of rice sheath blight. Plant Mol Biol 89(1–2):157–171. https://doi.org/10.1007/s11103-015-0360-8
Wang J, Tao F, Tian W, Guo Z, Chen X, Xu X, Shang H, Hu X (2017) The wheat WRKY transcription factors TaWRKY49 and TaWRKY62 confer differential high-temperature seedling-plant resistance to Puccinia striiformis f. sp. tritici. PLoS ONE 12(7):e0181963. https://doi.org/10.1371/journal.pone.0181963
Wang N, Zhao P, Ma Y, Yao X, Sun Y, Huang X, Jin J, Zhang Y, Zhu C, Fang R, Ye J (2019) A whitefly effector Bsp9 targets host immunity regulator WRKY33 to promote performance. Philos Trans R Soc Lond B Biol Sci 374(1767):20180313. https://doi.org/10.1098/rstb.2018.0313
Wang H, Zou S, Li Y, Lin F, Tang D (2020) An ankyrin-repeat and WRKY-domain-containing immune receptor confers stripe rust resistance in wheat. Nat Commun 11(1):1353. https://doi.org/10.1038/s41467-020-15139-6
Wani SH, Anand S, Singh B, Bohra A, Joshi R (2021) WRKY transcription factors and plant defense responses: latest discoveries and future prospects. Plant Cell Rep 40(7):1071–1085. https://doi.org/10.1007/s00299-021-02691-8
Wei Y, Shi H, Xia Z, Tie W, Ding Z, Yan Y, Wang W, Hu W, Li K (2016) Genome-wide identification and expression analysis of the WRKY gene family in Cassava. Front Plant Sci 7:25. https://doi.org/10.3389/fpls.2016.00025
Wei W, Cui MY, Hu Y, Gao K, Xie YG, Jiang Y, Feng JY (2018) Ectopic expression of FvWRKY42, a WRKY transcription factor from the diploid woodland strawberry (Fragaria vesca), enhances resistance to powdery mildew, improves osmotic stress resistance, and increases abscisic acid sensitivity in Arabidopsis. Plant Sci 275:60–74. https://doi.org/10.1016/j.plantsci.2018.07.010
Wen F, Wu X, Li T, Jia M, Liao L (2022) Characterization of the WRKY gene family in Akebia trifoliata and their response to Colletotrichum acutatum. BMC Plant Biol 22(1):115. https://doi.org/10.1186/s12870-022-03511-1
Wu J, Chen J, Wang L, Wang S (2017) Genome-wide investigation of WRKY transcription factors involved in terminal drought stress response in common bean. Front Plant Sci 8:380. https://doi.org/10.3389/fpls.2017.00380
Xie Z, Zhang ZL, Zou X, Huang J, Ruas P, Thompson D, Shen QJ (2005) Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiol 137(1):176–189. https://doi.org/10.1104/pp.104.054312
Xing DH, Lai ZB, Zheng ZY, Vinod KM, Fan BF, Chen ZX (2008) Stress- and pathogen-induced Arabidopsis WRKY48 is a transcriptional activator that represses plant basal defense. Mol Plant 1(3):459–470. https://doi.org/10.1093/mp/ssn020
Xu Y-H, Wang J-W, Wang S, Wang J-Y, Chen X-Y (2004) Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-δ-Cadinene Synthase-A. Plant Physiol 135(1):507–515. https://doi.org/10.1104/pp.104.038612
Xu X, Chen C, Fan B, Chen Z (2006) Physical and functional interactions between pathogen-induced Arabidopsis WRKY18, WRKY40, and WRKY60 transcription factors. Plant Cell 18(5):1310–1326. https://doi.org/10.1105/tpc.105.037523
Xu H, Watanabe KA, Zhang L, Shen QJ (2016) WRKY transcription factor genes in wild rice Oryza nivara. DNA Res 23(4):311–323. https://doi.org/10.1093/dnares/dsw025
Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, Yabuki T, Aoki M, Seki E, Matsuda T, Tomo Y, Hayami N, Terada T, Shirouzu M, Tanaka A, Seki M, Shinozaki K, Yokoyama S (2005) Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell 17(3):944–956. https://doi.org/10.1105/tpc.104.026435
Yan L, Jin H, Raza A, Huang Y, Gu D, Zou X (2022) WRKY genes provide novel insights into their role against Ralstonia solanacearum infection in cultivated peanut (Arachis hypogaea L.). Front Plant Sci 13:986673. https://doi.org/10.3389/fpls.2022.986673
Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NN (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9:68. https://doi.org/10.1186/1471-2229-9-68
Yang S, Zhou L, Miao L-y, Shi J-n, Sun C-q, Fan W, Lan J-p, Chen H, Liu L-j, Dou S-j, Liu G-z, Li L-y (2016) The expression and binding properties of the rice WRKY68 protein in the Xa21-mediated resistance response to Xanthomonas oryzae pv. Oryzae. J Integr Agric 15(11):2451–2460. https://doi.org/10.1016/s2095-3119(15)61265-5
Yang Y, Zhou Y, Chi Y, Fan B, Chen Z (2017) Characterization of soybean WRKY gene family and identification of soybean WRKY genes that promote resistance to soybean cyst nematode. Sci Rep 7(1):17804. https://doi.org/10.1038/s41598-017-18235-8
Yao DM, Zou C, Shu YN, Liu SS (2020) WRKY transcription factors in Nicotiana tabacum modulate plant immunity against whitefly via interacting with MAPK cascade pathways. InSects 12(1):16. https://doi.org/10.3390/insects12010016
Yoda H, Ogawa M, Yamaguchi Y, Koizumi N, Kusano T, Sano H (2002) Identification of early-responsive genes associated with the hypersensitive response to tobacco mosaic virus and characterization of a WRKY-type transcription factor in tobacco plants. Mol Genet Genomics 267(2):154–161. https://doi.org/10.1007/s00438-002-0651-z
Yogendra KN, Kumar A, Sarkar K, Li Y, Pushpa D, Mosa KA, Duggavathi R, Kushalappa AC (2015) Transcription factor StWRKY1 regulates phenylpropanoid metabolites conferring late blight resistance in potato. J Exp Bot 66(22):7377–7389
Yogendra KN, Dhokane D, Kushalappa AC, Sarmiento F, Rodriguez E, Mosquera T (2017) StWRKY8 transcription factor regulates benzylisoquinoline alkaloid pathway in potato conferring resistance to late blight. Plant Sci 256:208–216
Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JD, Doke N (2003) Nicotiana benthamiana gp91 phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. Plant Cell 15(3):706–718
Yu F, Huaxia Y, Lu W, Wu C, Cao X, Guo X (2012) GhWRKY15, a member of the WRKY transcription factor family identified from cotton (Gossypium hirsutum L.), is involved in disease resistance and plant development. BMC Plant Biol 12:144. https://doi.org/10.1186/1471-2229-12-144
Yu Y, Xu W, Wang J, Wang L, Yao W, Yang Y, Xu Y, Ma F, Du Y, Wang Y (2013) The Chinese wild grapevine (Vitis pseudoreticulata) E3 ubiquitin ligase Erysiphe necator-induced RING finger protein 1 (EIRP1) activates plant defense responses by inducing proteolysis of the VpWRKY11 transcription factor. New Phytol 200(3):834–846. https://doi.org/10.1111/nph.12418
Yu Y, Qi Y, Xu J, Dai X, Chen J, Dong CH, Xiang F (2021) Arabidopsis WRKY71 regulates ethylene-mediated leaf senescence by directly activating EIN2, ORE1 and ACS2 genes. Plant J 107(6):1819–1836. https://doi.org/10.1111/tpj.15433
Zhang Y, Wang L (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5:1. https://doi.org/10.1186/1471-2148-5-1
Zhang J, Peng Y, Guo Z (2008) Constitutive expression of pathogen-inducible OsWRKY31 enhances disease resistance and affects root growth and auxin response in transgenic rice plants. Cell Res 18(4):508–521. https://doi.org/10.1038/cr.2007.104
Zhang Y, Yang Y, Fang B, Gannon P, Ding P, Li X, Zhang Y (2010) Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70. Plant Cell 22(9):3153–3163
Zhang Q, Li Y, Zhang Y, Wu C, Wang S, Hao L, Wang S, Li T (2017) Md-miR156ab and Md-miR395 target WRKY transcription factors to influence apple resistance to leaf spot disease. Front Plant Sci 8:526. https://doi.org/10.3389/fpls.2017.00526
Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48(4):592–605. https://doi.org/10.1111/j.1365-313X.2006.02901.x
Zheng Z, Mosher SL, Fan B, Klessig DF, Chen Z (2007) Functional analysis of Arabidopsis WRKY25 transcription factor in plant defense against Pseudomonas syringae. BMC Plant Biol 7:2. https://doi.org/10.1186/1471-2229-7-2
Zhou X, Jiang Y, Yu D (2011) WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Mol Cells 31(4):303–313. https://doi.org/10.1007/s10059-011-0047-1
Zipfel C (2014) Plant pattern-recognition receptors. Trends Immunol 35(7):345–351. https://doi.org/10.1016/j.it.2014.05.004
Acknowledgements
The authors wish to thank Ms. Lani Archer, University of North Texas (USA), for her contribution in editing and improving the English language of the manuscript.
Funding
Mrunmay Kumar Giri acknowledges the Science and Engineering Research Board (SERB), Govt of India, Project Number-ECR/2018/001179 for providing financial support to his laboratory. Mrunmay Kumar Giri also acknowledges infrastructure support available through the Department of Biotechnology, Govt of India, DBT-BUILDER program (BT/INF/22/SP42155/2021) at KIIT deemed to be University, India. Deepak Kumar acknowledges the Science and Engineering Research Board (EEQ/2021/000593), India for providing financial support to the laboratory. Deepak Kumar also acknowledges funding support to his lab from the Institution of Eminence Seed Grant (Dev. scheme No. 6031 (B) and RS acknowledge Malaviya Post Doctoral Fellowship (MPDF) under IoE Scheme, Banaras Hindu University, Varanasi, India.
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Saha, B., Nayak, J., Srivastava, R. et al. Unraveling the involvement of WRKY TFs in regulating plant disease defense signaling. Planta 259, 7 (2024). https://doi.org/10.1007/s00425-023-04269-y
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DOI: https://doi.org/10.1007/s00425-023-04269-y