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Basic leucine zipper domain transcription factors: the vanguards in plant immunity

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Abstract

Regulation of spatio-temporal expression patterns of stress tolerance associated plant genes is an essential component of the stress responses. Eukaryotes assign a large amount of their genome to transcription with multiple transcription factors (TFs). Often, these transcription factors fit into outsized gene groups which, in several cases, exclusively belong to plants. Basic leucine zipper domain (bZIP) transcription factors regulate vital processes in plants and animals. In plants, bZIPs are implicated in numerous fundamental processes like seed development, energy balance, and responses to abiotic or biotic stresses. Systematic analysis of the information obtained over the last two decades disclosed a constitutive role of bZIPs against biotic stress. bZIP TFs are vital players in plant innate immunity due to their ability to regulate genes associated with PAMP-triggered immunity, effector-triggered immunity, and hormonal signaling networks. Expression analysis of studied bZIP genes suggests that exploration and functional characterization of novel bZIP TFs in planta is helpful in improving crop resistance against pathogens and environmental stresses. Our review focuses on major advancements in bZIP TFs and plant responses against different pathogens. The integration of genomics information with the functional studies provides new insights into the regulation of plant defense mechanisms and engineering crops with improved resistance to invading pathogens. Conclusively, succinct functions of bZIPs as positive or negative regulator mediate resistance to the plant pathogens and lay a foundation for understanding associated genes and TFs regulating different pathways. Moreover, bZIP TFs may offer a comprehensive transgenic gizmo for engineering disease resistance in plant breeding programs.

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References

  • Agarwal P, Reddy MP, Chikara J (2011) WRKY: its structure, evolutionary relationship, DNA-binding selectivity, role in stress tolerance and development of plants. Mol Biol Rep 38:3883–3896

    Article  CAS  PubMed  Google Scholar 

  • Ali Q, Haider MZ, Iftikhar W, Jamil S, Javed MT, Noman A, Iqbal M, Perveen R (2016) Drought tolerance potential of Vigna mungo L. lines as deciphered by modulated growth, antioxidant defense, and nutrient acquisition patterns. Braz J Bot 39:801–812

    Article  Google Scholar 

  • Ali Q, Javed MT, Noman A, Haider MZ, Waseem M, Iqbal N, Waseem M, Shah MS, Shahzad F, Perveen R (2017) Assessment of drought tolerance in mung bean cultivars/lines as depicted by the activities of germination enzymes, seedling’s antioxidative potential and nutrient acquisition. Arch Agron Soil Sci 63:1–9

    Article  CAS  Google Scholar 

  • Alves MS, Dadalto SP, Goncalves AB, De Souza GB, Barros VA, Fietto LG (2013) Plant bZIP transcription factors responsive to pathogens: a review. Int J Mol Sci 14:7815–7828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Alves MS, Dadalto SP, Gonçalves AB, de Souza GB, Barros VA, Fietto LG (2014) Transcription factor functional protein–protein interactions in plant defense responses. Proteomes 2:85–106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baek JH, Park JA, Kim JM, Oh JM, Park SM, Kim DH (2014) Functional analysis of a tannic-acid-inducible and hypoviral-regulated small heat-shock protein Hsp24 from the chestnut blight fungus Cryphonectria parasitica. Mol Plant-Microbe Interact 27:56–65

    Article  CAS  PubMed  Google Scholar 

  • Blanco F, Garreton V, Frey N, Dominguez C, Perez-Acle T, van der Straeten D, Jordana X, Holuigue L (2005) Identification of NPR1-dependent and independent genes early induced by salicylic acid treatment in Arabidopsis. Plant Mol Biol 59:927–944

    Article  CAS  PubMed  Google Scholar 

  • Blanco F, Garreton BF, Salinas P, Cecchini NM, Jordana X, Van Hummelen P, Alvarez ME, Holuigue L (2009) Early genomic responses to salicylic acid in Arabidopsis. Plant Mol Biol 70:79–102

    Article  CAS  PubMed  Google Scholar 

  • Caarls L, Pieterse CM, Van Wees SC (2015) How salicylic acid takes transcriptional control over jasmonic acid signaling. Front Plant Sci 6:170

    Article  PubMed  PubMed Central  Google Scholar 

  • Catinot J, Huang JB, Huang PY, Tseng MY, Chen YL, Gu SY, Lo WS, Wang LC, Chen YR, Zimmerli L (2015) Ethylene response factor 96 positively regulates Arabidopsis resistance to necrotrophic pathogens by direct binding to GCC elements of jasmonate and ethylene-responsive defence genes. Plant Cell Environ 38:2721–2734

    Article  CAS  PubMed  Google Scholar 

  • Cheong YH, Moon BC, Kim JK, Kim CY, Kim MC, Kim IH, Park CY, Kim JC, Park BO, Koo SC, Yoon HW, Chung WS, Lim CO, Lee SY, Cho MJ (2003) BWMK1, a rice mitogen-activated protein kinase, locates in the nucleus and mediates pathogenesis-related gene expression by activation of a transcription factor. Plant Physiol 132:1961–1972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chern MS, Fitzgerald HA, Yadav RC, Canlas PE, Dong X, Ronald PC (2001) Evidence for a disease-resistance pathway in rice similar to the NPR1-mediated signaling pathway in Arabidopsis. Plant J 27:101–113

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Stakawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  PubMed  Google Scholar 

  • Choi DS, Hwang BK (2011) Proteomics and functional analyses of pepper abscisic acid-responsive 1 (ABR1), which is involved in cell death and defense signaling. Plant Cell 23:823–842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200

    Article  CAS  PubMed  Google Scholar 

  • Correa LGG (2004) Ana´liseFilogene´tica de Fatores de Transcric¸a˜obZIPemAngiospermas (Phylogenetic analyses of bZIP transcription factors in angiosperms) [dissertation] Universida de Estadual de Campinas, Campinas, Brazil

  • Correa LG, Riaño-Pachón DM, Guerra Schrago C, Vicentini dos Santos R, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS ONE 3:e2944

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 36:757–774

    Article  CAS  PubMed  Google Scholar 

  • Datta R, Kumar D, Sultana A, Bhattacharyya D, Chattopadhyay S (2015) Glutathione regulates ACC synthase transcription via WRKY33 and ACC oxidase by modulating mRNA stability to induce ethylene synthesis during stress. Plant Physiol 169:2963–2981

    CAS  PubMed  PubMed Central  Google Scholar 

  • Deslandes L, Rivas S (2011) The plant cell nucleus: a true arena for the fight between plants and pathogens. Plant Signal Behav 6:42–48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Després C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12:279–290

    Article  PubMed  PubMed Central  Google Scholar 

  • Dröge-Laser W, Kaiser A, Lindsay WP, Halkier BA, Loake GJ, Doerner P, Dixon R, Lamb C (1997) Rapid stimulation of a soybean protein-serine kinase that phosphorylates a novel bZIP DNA-binding protein, G/HBF-1, during the induction of early transcription-dependent defenses. EMBO J 16:726–738

    Article  PubMed  PubMed Central  Google Scholar 

  • Du Z, Chen A, Chen W, Liao Q, Zhang H, Bao Y, Roossinck MJ, Carr JP (2014) Nuclear–cytoplasmic partitioning of cucumber mosaic virus protein 2b determines the balance between its roles as a virulence determinant and an RNA-silencing suppressor. J Virol 88:5228–5241

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fan W, Dong X (2002) In vivo interaction between NPR1 and transcription factor TGA2 leads to SA-mediated gene activation in Arabidopsis. Plant Cell 14:1377–1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fitzgerald HA, Canlas PE, Chern MS, Ronald PC (2005) Alteration of TGA factor activity in rice results in enhanced tolerance to Xanthomonas oryzae pv. oryzae. Plant J 43:335–347

    Article  CAS  PubMed  Google Scholar 

  • Foley RC, Grossman C, Ellis JG, Llewellyn DJ, Dennis ES, Peacock WJ, Singh KB (1993) Isolation of a maize bZIP protein subfamily: candidates for the ocs-element transcription factor. Plant J 3:669–679

    Article  CAS  PubMed  Google Scholar 

  • Froidurea S, Canonnea J, Daniela X, Jauneaub A, Brièrec C, Robya D, Rivasa S (2010) AtsPLA2-α nuclear relocalization by the Arabidopsis transcription factor AtMYB30 leads to repression of the plant defense response. PNAS 107(34):15281–15286

    Article  Google Scholar 

  • Fukazawa J, Sakai T, Ishida S, Yamaguchi I, Kamiya Y, Takahashi Y (2000) Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell 12:901–915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gamboa-Meléndez H, Apolonio I, Huerta H, Judelson S (2013) bZIP Transcription Factors in the oomycete Phytophthora infestans with novel DNA-Binding Domains are involved in defense against oxidative stress. Eukaryot Cell 12(10):1403–1412

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hossain MA, Lee Y, Cho JI, Ahn CH, Lee SK, Jeon JS, Kang H, Lee CH, An G, Park PB (2010) The bZIP transcription factor OsABF1 is an ABA responsive element binding factor that enhances abiotic stress signaling in rice. Plant Mol Biol 72:557–566

    Article  CAS  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  CAS  PubMed  Google Scholar 

  • Hu W, Yang H, Yan Y, Wei Y, Tie W, Ding Z, Jiao Z, Ming P, Li K (2016) Genome-wide characterization and analysis of bZIP transcription factor gene family related to abiotic stress in cassava. Sci Rep 6:22783

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishihama N, Yoshioka H (2012) Post-translational regulation of WRKY transcription factors in plant immunity. Curr Opin Plant Biol 15:431–437

    Article  CAS  PubMed  Google Scholar 

  • Islam W, Zhang J, Adnan M, Noman A, Zainab M, Jian W (2017) Plant virus ecology: a glimpse of recent accomplishments. App Eco Environ Res 15:691–705

    Article  Google Scholar 

  • Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20:3107–3121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakoby M, Weisshaar MJB, Dröge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2006) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  Google Scholar 

  • Jensen MK, Hagedorn PH, de Torres-Zabala M, Grant MR, Rung JH, Collinge DB, Lyngkjaer MF (2008) Transcriptional regulation by anNAC (NAMATAF1,2-CUC2) transcription factor attenuates ABA signaling for efficient basal defence towards Blumeria graminis f. sp. hordei in Arabidopsis. Plant J 56:867–880

    Article  CAS  PubMed  Google Scholar 

  • 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 171:2771–2782

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kaminaka H, Näke C, Epple P, Dittgen J, Schütze K, Chaban C, Holt BF, Merkle T, Schäfer E, Harter K, Dangl JL (2006a) bZIP10-LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J 25:4400–4411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaminaka H, Nake C, Epple P, Dittgen J, Schutze K, Chaban C, Holt BF 3rd, Merkle T, Schäfer E, Harter K, Dangl JL (2006b) bZIP10- LSD1 antagonism modulates basal defense and cell death in Arabidopsis following infection. EMBO J 25:4400–4411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang JH, Wang L, Giri A, Baldwin IT (2006) Silencing threonine deaminase and JAR4 in Nicotiana attenuata impairs jasmonic acid-isoleucine-mediated defenses against Manduca sexta. Plant Cell 18:3303–3320

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karlowski WM, Hirsch AM (2003) The over-expression of an alfalfa RING-H2 gene induces pleiotropic effects on plant growth and development. Plant Mol Biol 52:121–133

    Article  CAS  PubMed  Google Scholar 

  • Kegler C, Lenk I, Krawczyk S, Scholz R, Gatz C (2004) Functional characterization of tobacco transcription factor TGA2.1. Plant Mol Biol 55:153–164

    Article  CAS  PubMed  Google Scholar 

  • Kesarwani M, Yoo J, Dong X (2007) Genetic interactions of TGA transcription factors in the regulation of pathogenesis-related genes and disease resistance in Arabidopsis. Plant Physiol 144:336–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim HS, Delaney TP (2002) Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J 32:151–163

    Article  CAS  PubMed  Google Scholar 

  • Kim DS, Hwang BK (2012) The pepper MLO gene, CaMLO2, is involved in the susceptibility cell-death response and bacterial and oomycete proliferation. Plant J 72:843–855

    Article  CAS  PubMed  Google Scholar 

  • Kim SH, Son GH, Bhattacharjee S, Kim HJ, Nam JC, Nguyen PDT, Hong JC, Gassmann W (2014) The Arabidopsis immune adaptor SRFR1 interacts with TCP transcription factors that redundantly contribute to effector-triggered immunity. Plant J 78:978–989

    Article  CAS  PubMed  Google Scholar 

  • Kuhlmann M, Horvay K, Stathmann A, Heinekamp T, Fischer U, Böttner S, Dröge-Laser W (2003a) The alpha-helical D1 domain of the bZIP transcription factor BZI-1 interacts with the ankyrin-repeat protein ANK1, and is essential for BZI-1 function, both in auxin signaling and pathogen response. J Biol Chem 278:8786–8794

    Article  CAS  PubMed  Google Scholar 

  • Kuhlmann M, Horvay K, Stathmann A, Heinekamp T, Fischer U, Böttner S, Dröge-Laser W (2003b) The alpha-helical D1 domain of the bZIP transcription factor BZI-1 interacts with the ankyrin-repeat protein ANK1, and is essential for BZI-1 function, both in auxin signaling and pathogen response. J Biol Chem 278:8786–8794

    Article  CAS  PubMed  Google Scholar 

  • Lai Z, Schluttenhofer CM, Bhide K, Shreve J, Thimmapuram J, Lee SY, Yun D-J, Mengiste T (2014) MED18 interaction with distinct transcription factors regulates multiple plant functions. Nat Commun 5:3064

    Article  PubMed  CAS  Google Scholar 

  • Lara-Rojas F, Sanchez O, Kawasaki L, Aguirre J (2011) Aspergillus nidulans transcription factor AtfA interacts with the MAPK SakA to regulate general stress responses, development and spore functions. Mol Microbiol 80:436–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebel E, Heifetz P, Thorne L, Uknes S, Ryals J, Ward E (1998) Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J 16:223–233

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ, Lee MY, Yi SY, Oh SK, Choi SH, Her NH, Choi D, Min BW, Yang SG, Harn CH (2002a) PPI1: a novel pathogen-induced basic region-leucine zipper (bZIP) transcription factor from pepper. Mol Plant Microbe Interact 15:540–548

    Article  CAS  PubMed  Google Scholar 

  • Lee SJ, Lee MY, Yi SY, Oh SK, Choi SH, Her NH, Choi D, Min BW, Yang SG, Harn CH (2002b) PPI1: a novel pathogen-induced basic region-leucine zipper (bZIP) transcription factor from pepper. Mol Plant Microbe Interact 15(6):540–548

    Article  CAS  PubMed  Google Scholar 

  • Lee S, Kim SY, Chung E, Joung YH, Pai HS, Hur CG, Choi D (2004) EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv. glycine). Funct Integr Genom 4:196–205

    Article  Google Scholar 

  • Lee SC, Choi HW, Hwang IS, Choi DS, Hwang BK (2006a) Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses. Planta 224:1209–1225

    Article  CAS  PubMed  Google Scholar 

  • Lee SC, Choi HW, Hwang IS, Choi DS, Hwang BK (2006b) Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses. Planta 224:1209–1225

    Article  CAS  PubMed  Google Scholar 

  • Lee HJ, Park YJ, Seo PJ, Kim JH, Sim HJ, Kim SG, Park CM (2015) Systemic immunity requires SnRK2.8-mediated nuclear import of NPR1 in Arabidopsis. Plant Cell 27:3425–3438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Lauri A, Ziemann M, Busch A, Bhave M, Zachgo S (2009a) Nuclear activity of ROXY1, a glutaredoxin interacting with TGA factors, is required for petal development in Arabidopsis thaliana. Plant Cell 21:429–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li S, Lauri A, Ziemann M, Busch A, Bhave M, Zachgo S (2009b) Nuclear activity of ROXY1, a glutaredoxin interacting with TGA factors, is required for petal development in Arabidopsis thaliana. Plant Cell 21:429–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li D, Fuyou F, Huijuan Z, Fengming S (2015) Genome-wide systematic characterization of the bZIP transcriptional factor family in tomato (Solanum lycopersicum L.). BMC Genom 16:771

    Article  CAS  Google Scholar 

  • Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008) Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis. Planta 228:225–240

    Article  CAS  PubMed  Google Scholar 

  • Lim CW, Baek W, Lim S, Han SW, Lee SC (2015) Expression and functional roles of the pepper pathogen–induced bZIP Transcription factor CabZIP2 in enhanced disease resistance to bacterial pathogen infection. Mol Plant-Microbe Interact 28:825–833

    Article  CAS  PubMed  Google Scholar 

  • Lindermayr C, Sell S, Müller B, Leister D, Durner J (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894–2907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu JX, Srivastava R, Che P, Howell SH (2007) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J-X, Srivastava R, Howell SH (2008) Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis. Plant Cell Environ 31:1735–1743

    Article  CAS  PubMed  Google Scholar 

  • Liu R, Lü B, Wang X, Zhang C, Zhang S, Qian J, Chen L, Shi H, Dong H (2010) Thirty-seven transcription factor genes differentially respond to a hairpin protein and affect resistance to the green peach aphid in Arabidopsis. J Biol Sci 35:435–450

    CAS  Google Scholar 

  • Liu C, Wu Y, Wang X (2012a) bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta 235:1157–1169

    Article  CAS  PubMed  Google Scholar 

  • Liu C, Wu Y, Wang X (2012b) bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta 235:1157–1169

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Kracher B, Ziegler J, Birkenbihl RP, Somssich IE (2015) Negative regulation of ABA signaling by WRKY33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100. eLife 4:e07295

    PubMed  PubMed Central  Google Scholar 

  • Liu L, Sonbol FM, Huot B, Gu Y, Withers J, Mwimba M, Yao J, He SY, Dong X (2016) Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity. Nat Commun 7:13099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Llorca CM, Potschin M, Zentgraf U (2014) bZIPs and WRKYs: two large transcrip tion factor families executing two different functional strategies. Front Plant Sci 5:169

    Article  PubMed  PubMed Central  Google Scholar 

  • Loake G, Grant M (2007) Salicylic acid in plant defence-the players and protagonists. Curr Opin Plant Biol 10:466–472

    Article  CAS  PubMed  Google Scholar 

  • Lopes MA, Hora BT Jr, Dias CV, Santos GC, Gramacho KP, Cascardo JC, Gesteira AS, Micheli F (2010) Expression analysis of transcription factors from the interaction between cacao and Moniliophthora perniciosa (Tricholomataceae). Genet Mol Res 9:1279–1297

    Article  CAS  PubMed  Google Scholar 

  • Mair A, Pedrotti L, Wurzinger B, Anrather D, Simeunovic A, Weiste C, Valerio C, Dietrich K, Kirchler T, Nägele T, Vicente Carbajosa J, Hanson J, Baena-González E, Chaban C, Weckwerth W, Dröge-Laser W, Teige M (2015) SnRK1-triggered switch of bZIP63 dimerization mediates the low-energy response in plants. eLife 11:4

    Google Scholar 

  • Mateo A, Muhlenbock P, Rusterucci C, Chang CC, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) Lesion simulating disease 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiol 136:2818–2830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Memelink J (2009) Regulation of gene expression by jasmonate homones. Phytochemistry 70:1560–1570

    Article  CAS  PubMed  Google Scholar 

  • Murmu J, Bush MJ, DeLong C, Li S, Xu M, Khan M, Malcolmson C, Fobert PR, Zachgo S, Hepworth SR (2010) Arabidopsis basic leucine-zipper transcription factors TGA9 and TGA10 interact with floral glutaredoxins ROXY1 and ROXY2 and are redundantly required for anther development. Plant Physiol 154:1492–1504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakashima K, Tran LS, Van Nguyen D, Fujita M, Maruyama K, Todaka D, Ito Y, Hayashi N, Shinozaki K, Yamaguchi-Shinozaki K (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630

    Article  CAS  PubMed  Google Scholar 

  • Nieva C, Busk PK, Dominguez-Puigjaner E, Lumbreras V, Testillano PS, Risueño MC, Pagès M (2005) Isolation and functional characterization of two new bZIP maize regulators of the ABA responsive gene rab28. Plant Mol Biol 58:899–914

    Article  CAS  PubMed  Google Scholar 

  • Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noman A, Aqeel M (2017) miRNA-based heavy metal homeostasis and plant growth. Environ Sci Pollut Res 24:10068–10082

    Article  CAS  Google Scholar 

  • Noman A, Aqeel M, Deng J, Khalid N, Sanaullah T, Shuilin H (2017a) Biotechnological advancements for improving floral attributes in ornamental plants. Front Plant Sci 8:530

    Article  PubMed  PubMed Central  Google Scholar 

  • Noman A, Fahad S, Aqeel M, Ali U, Amanullah Anwer S, Baloch SK, Zainab M (2017b) miRNAs: major modulators for crop growth and development under abiotic stresses. Biotechnol Lett 39:685–700

    Article  CAS  PubMed  Google Scholar 

  • Oh SK, Lee S, Yu SH, Choi D (2005) Expression of a novel NAC domain-containing transcription factor (CaNAC1) is preferentially associated with incompatible interactions between chili pepper and pathogens. Planta 222:876–887

    Article  CAS  PubMed  Google Scholar 

  • Ohme-Takagi M, Shinshi H (1995) Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H (2009a) OsTGAP1 a bZIP transcription factor coordinately regulates the inductive production of diterpenoid phytoalexins in rice. J Biol Chem 284:26510–26518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H (2009b) OsTGAP1, abZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice. J Biol Chem 284:26510–26518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orellana S, Yañez M, Espinoza A, Verdugo I, González E, Ruiz-Lara S, Casaretto JA (2010) The transcription factor SlAREB1 confers drought salt stress tolerance and regulates biotic and abiotic stress-related genes in tomato. Plant Cell Environ 33:2191–2208

    Article  CAS  PubMed  Google Scholar 

  • Pajerowska-Mukhtar KM, Emerine DK, Mukhtar MS (2013) Tell me more: roles of NPRs in plant immunity. Trend Plant Sci 18:402–411

    Article  CAS  Google Scholar 

  • Pieterse CMJ, van der Does D, Zamioudis C, Leon-Reyes A, van Wees SCM (2012) Hormonal modulation of plant immunity. Ann Rev Cell Dev Biol 28:489–521

    Article  CAS  Google Scholar 

  • Pontier D, Miao ZH, Lam E (2001) Trans-dominant suppression of plant TGA factors reveals their negative and positive roles in plant defense responses. Plant J27:529–538

    Google Scholar 

  • Ram H, Chattopadhyay S (2012) Molecular interaction of bZIP domains of GBF1, HY5 and HYH in Arabidopsis seedling development. Plant Signal Behav 8:e22703

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Resende MLV, Salgado SML, Chaves ZM (2003) Reactive oxygen species on plant defense responses to pathogens. Fitopatol Bras 28:123–130

    Article  Google Scholar 

  • Saleh A, Withers J, Mohan R, Marqués J, Gu Y, Yan S, Zavaliev R, Nomoto M, Tada Y, Dong X (2015) Post translational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host Microbe 18:169–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato F, Katajima S, Koyama T, Yamada Y (1996) Ethylene-induced gene expression of osmotin-like protein a neutral isoform of tobacco PR-5 is mediated by the AGCCGCC cis-sequence. Plant Cell Physiol 37:249–255

    Article  CAS  PubMed  Google Scholar 

  • Schiermeyer A, Thurow C, Gatz C (2003) Tobacco bZIP factor TGA10 is a novel member of the TGA family of transcription factors. Plant Mol Biol 51:817–829

    Article  CAS  PubMed  Google Scholar 

  • Segarra G, Van der Ent S, Trillas I, Pieterse CMJ (2009) MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial Microbe. Plant Biol 11:90–96

    Article  CAS  PubMed  Google Scholar 

  • Seo PJ, Park CM (2010) MYB96-mediated abscisic acid signals induce pathogen resistance response by promoting salicylic acid biosynthesis in Arabidopsis. New Phytol 186:471–483

    Article  CAS  PubMed  Google Scholar 

  • Shah J (2003) The salicylic acid loop in plant defence. Curr Opin Plant Biol 6:365–371

    Article  CAS  PubMed  Google Scholar 

  • Sheikh AH, Eschen-Lippold L, Pecher P, Hoehenwarter W, Sinha AK, Scheel D, Lee J (2016) Regulation of WRKY46 transcription factor function by mitogen-activated protein kinases in Arabidopsis thaliana. Front Plant Sci 7:61

    Article  PubMed  PubMed Central  Google Scholar 

  • Shen H, Cao K, Wang X (2007) A conserved proline residue in the leucine zipper region of AtbZIP34 and AtbZIP61 in Arabidopsis thaliana interferes with the formation of homodimer. Biochem Biophys Res Commun 362:425–430

    Article  CAS  PubMed  Google Scholar 

  • Shen L, Liu Z, Yang S, Yang T, Liang J, Wen J, Liu Y, Li J, Shi L, Tang Q, Shi W, Hu J, Liu C, Zhang Y, Lin W, Wang R, Yu H, Mou S, Hussain A, Cheng W, Cai H, He L, Guan D, Wu Y, He S (2016a) Pepper CabZIP63 acts as a positive regulator during Ralstonia solanacearum or high temperature-high humidity challenge in a positive feedback loop with CaWRKY40. J Exp Bot 67:2439–2451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen L, Liu Z, Yang S, Yang T, Liang J, Wen J, Liu Y, Li J, Shi L, Tang Q, Shi W, Hu J, Liu C, Zhang Y, Lin W, Wang R, Yu H, Mou S, Hussain A, Cheng W, Cai H, He L, Guan D, Wu Y, He S (2016b) Pepper CabZIP63 acts as a positive regulator during Ralstonia solanacearum or high temperature-high humidity challenge in a positive feedback loop with CaWRKY40. J Exp Bot 67:2439–2451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  CAS  PubMed  Google Scholar 

  • Spoel SH, Koornneef A, Claessens SM, Korzelius JP, Van Pelt JA, Mueller MJ, Buchala AJ, Métraux JP, Brown R, Kazan K, Van Loon LC, Dong X, Pieterse CM (2003) NPR1 modulates cross-talk between salicylate- and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 15:760–770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun L, Zhang H, Li D, Huang L, Hong Y, Ding XS (2013) Functions of rice NAC transcriptional factors, ONAC122 and ONAC131, in defense responses against Magna porthegrisea. Plant Mol Biol 81(41–56):10

    Google Scholar 

  • Tak H, Mhatre M (2012a) Cloning and molecular characterization of a putative bZIP transcription factor VvbZIP23 from Vitis vinifera. Protoplasma 250:333–345

    Article  PubMed  CAS  Google Scholar 

  • Tak H, Mhatre M (2012b) Cloning and molecular characterization of a putative bZIP transcription factor VvbZIP23 from Vitis vinifera. Protoplasma 250:333–345

    Article  PubMed  CAS  Google Scholar 

  • Tang N, Zhang H, Li X, Xiao J, Xiong L (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158:1755–1768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tateda C, Ozaki R, Onodera Y, Takahashi Y, Yamaguchi K, Berberich T, Koizumi N, Kusano T (2008) NtbZIP60, an endoplasmic reticulum-localized transcription factor, plays a role in the defense response against bacterial pathogens in Nicotiana tabacum. J Plant Res 121:603–611

    Article  CAS  PubMed  Google Scholar 

  • Thurow C, Schiermeyer A, Krawczyk S, Butterbrodt T, Nickolov K, Gatz C (2005a) Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. Plant J 44:100–113

    Article  CAS  PubMed  Google Scholar 

  • Thurow C, Schiermeyer A, Krawczyk S, Butterbrodt T, Nickolov K, Gatz C (2005b) Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. Plant J 44:100–113

    Article  CAS  PubMed  Google Scholar 

  • Tian C, Li J, Glass NL (2011) Exploring the bZIP transcription factor regulatory network in Neurospora crassa. Microbiology 157:747–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsugama D, Liu S, Takano T (2012) A bZIP protein, VIP1, is a regulator of osmosensory signaling in Arabidopsis. Plant Physiol 159:144–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Udvardi MK, Kakar K, Wandrey M, Montanari O, Murray J, Andriankaja A, Zhang J, Benedito V, Hofer JMI, Chueng F, Town CD (2007) Legume transcription factors: global regulators of plant development and response to the environment. Plant Physiol 144:538–549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uquillas C, Letelier I, Blanco F, Jordana X, Holuigue L (2004) NPR1-independent activation of immediate early salicylic acid-responsive genes in Arabidopsis. Mol Plant Microbe Interact 17:34–42

    Article  CAS  PubMed  Google Scholar 

  • Ustun S, Bartetzko V, Bornke F (2013) The Xanthomonascampestris type III effector XopJ targets the host cell proteasome to suppress salicylic-acid mediated plant defence. PLoS Pathog 9:e1003427

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • vanVerk MC, Pappaioannou D, Neeleman L, Bol JF, Linthorst HJM (2008) A Novel WRKY transcription factor is required for induction of PR-1a gene expression by salicylic acid and bacterial elicitors. Plant Physiol 146:1983–1995

    Article  CAS  Google Scholar 

  • vanVerk MC, Bol JF, Linthorst HJ (2011) WRKY transcription factors involved in activation of SA biosynthesis genes. BMC Plant Biol 11:p89

    Article  CAS  Google Scholar 

  • Vincentz M, Bandeira-Kobarg C, Gauer L, Schlogl P, Leite A (2003) Evolutionary pattern of angiosperm bZIP factors homologous to the maize Opaque2 regulatory protein. J Mol Evol 56:105–116

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Gao J, Zhu Z, Dong X, Wang X, Ren G, Zhou X, Kuai B (2015) TCP transcription factors are critical for the coordinated regulation of Isochorismate synthase 1 expression in Arabidopsis thaliana. Plant J 82:151–162

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Hongli C, Wenjun Q, Lina Y, Xinyuan H, Nana L, Yajun Y, Xinchao W (2017) Identification of a novel bZIP transcription factor in Camellia sinensis as a negative regulator of freezing tolerance in transgenic Arabidopsis. Ann Bot 119:1195–1209

    Article  PubMed  Google Scholar 

  • Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012) Genome-wide analysis of bZIP-encoding genes in maize. DNA Res 19:463–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weßling R, Epple P, Altmann S, He Y, Yang L, Henz SR, McDonald N, Wiley K, Bader KC, Gläßer C, Mukhtar MS, Haigis S, Ghamsari L, Stephens AE, Ecker JR, Vidal M, Jones JD, Mayer KF, Loren Ver, van Themaat E, Weigel D, Schulze-Lefert P, Dangl JL, Panstruga R, Braun P (2014) Convergent targeting of a common host proteinnetwork by pathogen effectors from three kingdoms of life. Cell Host Microbe 16:364–375

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wingender E, Chen X, Fricke E, Geffers R, Hehl R, Liebich I, Krull M, Matys V, Michae H, Ohnhäuser R, Prüß M, Schacherer F, Thiele S, Urbach S (2001) The transfac system on gene expression regulation. Nucleic Acid Res 29:281–283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu L, Zhu L, Tu L, Liu L, Yuan D, Jin L, Long L, Zhang X (2011) Lignin metabolism has a central role in the resistance of cotton to the wilt fungus Verticillium dahlia as revealed by RNA-Seq-dependent transcriptional analysis and histochemistry. J Exp Bot 62:5607–5621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida K, Wakamatsu S, Sakuta M (2008) Characterization of SBZ1 a soybean bZIP protein that binds to the chalcone synthase gene promoter. Plant Biotechnol 25:131–140

    Article  CAS  Google Scholar 

  • Zander M, Chen S, Imkampe J, Thurow C, Gatz C (2012) Repression of the Arabidopsis thaliana jasmonic acid/ethylene-induced defense pathway by TGA-interacting glutaredoxins depends on their C-terminal ALWL motif. Mol Plant 5:831–840

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Tessaro MJ, Lassner M, Li X (2003) Knockout analysis of Arabidopsis transcription factors TGA2 TGA5 and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15:2647–2653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Zhang G, Xia N, Wang XJ, Huang LL, Kang ZS (2008) Cloning and characterization of a bZIP transcription factor gene in wheat and its expression in response to stripe rust pathogen infection and abiotic stresses. Physiol Mol Plant Pathol 73:88–94

    Article  CAS  Google Scholar 

  • Zhang N, Liu D, Zheng W, He H, Ji B, Han Q, Ge F, Chen C (2014) A bZIP transcription factor, LrbZIP1, is involved in Lilium regale Wilson defense responses against Fusarium oxysporum f. sp. Lilii. Genes Genom 36:789

    Article  CAS  Google Scholar 

  • Zhang L, Zhang L, Xia C, Zhao G, Liu J, Jia J, Kong X (2015) A novel wheat bZIP transcription factor, TabZIP60, confers multiple abiotic stress tolerances in transgenic Arabidopsis. Physiol Plant 153:538–554

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Hong Y, Huang L, Li D, Song F (2016) Arabidopsis AtERF014 acts as a dual regulator that differentially modulates immunity against Pseudomonas syringae pv. tomato and Botrytis cinerea. Sci Rep 6:30251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou YL, Xu MR, Zhao MF, Xie XW, Zhu LH, Fu BY, Li ZK (2010) Genome-wide gene responses in a transgenic rice line carrying the maize resistance gene Rxo1 to the rice bacterial streak pathogen Xanthomonas oryzae pv oryzicola. BMC Genom 1:11–78

    Google Scholar 

  • Zhu Y, Schluttenhoffer CM, Wang P, Fu F, Thimmapuram J, Zhu JK, Lee SY, Yun DJ, Mengiste T (2014) CYCLINDEPENDENT KINASE8 differentially regulates plant immunity to fungal pathogens through kinase dependent and independent functions in Arabidopsis. Plant Cell 26:4149–4170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. Ali Noman and Zhiqin Liu have contributed equally to this manuscript.

Authors and Affiliations

  1. College of Crop Science, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, People’s Republic of China

    Ali Noman, Zhiqin Liu, Muhammad Ifnan Khan, Ansar Hussain, Muhammad Furqan Ashraf, Xia Li, Yahong Weng & Shuilin He

  2. State Key Laboratory of Grassland Agro-Ecosystems, School of Life Science, Lanzhou University, Lanzhou, Gansu, People’s Republic of China

    Muhammad Aqeel

  3. College of Life Science, Fujian Agriculture and Forestry University, Fuzhou, 350002, Fujian, People’s Republic of China

    Madiha Zainab

  4. National Education Minister Key Laboratory for Plant Genetic Improvement and Comprehensive Utilization, College of Crop Science, Fujian Agriculture and Forestry University, Fuzhou, 35002, Fujian, People’s Republic of China

    Shuilin He

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  1. Ali Noman
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  2. Zhiqin Liu
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Correspondence to Shuilin He.

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Noman, A., Liu, Z., Aqeel, M. et al. Basic leucine zipper domain transcription factors: the vanguards in plant immunity. Biotechnol Lett 39, 1779–1791 (2017). https://doi.org/10.1007/s10529-017-2431-1

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