Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Functional characterisation of a WRKY transcription factor of wheat and its expression analysis during leaf rust pathogenesis

Dhananjay Kumar A , Anjali Kapoor A , Dharmendra Singh A , Lopamudra Satapathy A , Ashwini Kumar Singh B , Manish Kumar A , Kumble Vinod Prabhu C and Kunal Mukhopadhyay A D
+ Author Affiliations
- Author Affiliations

A Department of Biotechnology, Birla Institute of Technology, Mesra, Ranchi 835215, India.

B Central Instrumentation Facility, Birla Institute of Technology, Mesra, Ranchi 835215, India.

C National Phytotron Facility, Indian Agricultural Research Institute, New Delhi 110012, India.

D Corresponding author. Email: kmukhopadhyay@bitmesra.ac.in

Functional Plant Biology 41(12) 1295-1309 https://doi.org/10.1071/FP14077
Submitted: 7 March 2014  Accepted: 4 June 2014   Published: 5 August 2014

Abstract

WRKY proteins are a large family of plant-specific transcription factors associated with regulation of biotic and abiotic stress responses, but how they respond to cereal rust pathogens has never been explored at the molecular level. Full-length cDNA of TaWRKY1B was obtained from a wheat cultivar HD2329 derivative containing leaf rust resistance gene Lr28 based on domain characteristics. The unique feature of this WRKY transcription factor gene was the close proximity of the DNA-binding domain and consensus DNA element W-Box within the open reading frame. Infection with a virulent race of leaf rust fungus resulted in 146-fold induction of the gene in resistant plants, but only 12-fold in the susceptible plants as compared with mock-inoculated controls. Docking models of 74 amino acids DNA-binding domain and 26 bp W-Box element showed that the WRKY domain, located on the β1 strand, only interacts with the W-Box at positions corresponding to W125, R126, K127 and Y128 amino acids. A truncated recombinant protein of 9.0 kD, encompassing the DNA-binding domain also showed binding specificity to the 32 bp W-Box element in electrophoretic mobility shift assays. The protein–DNA ensemble was also characterised using high-resolution atomic force microscopic imaging. The results contribute to an understanding of the molecular structure and function of a previously uncharacterised WRKY transcription factor in wheat that can be manipulated to improve biotic stress tolerance.

Additional keywords: atomic force microscopy, gene expression, in silico modeling and docking, in silico modelling and docking, leaf-rust of wheat, WRKY transcription factors.


References

Bahrini I, Sugisawa M, Kikuchi R, Ogawa T, Kawahigashi H, Ban T, Handa H (2011) Characterization of wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants. Breeding Science 61, 121–129.
Characterization of wheat transcription factor, TaWRKY45, and its effect on Fusarium head blight resistance in transgenic wheat plants.CrossRef | 1:CAS:528:DC%2BC3MXhtV2js7jL&md5=89e4bb5fd2d8811b4ddcd72b8328a750CAS |

Bipinraj A, Honrao B, Prashar M, Bhardwaj S, Rao S, Tamhankar S (2011) Validation and identification of molecular markers linked to the leaf rust resistance gene Lr28 in wheat. Journal of Applied Genetics 52, 171–175.
Validation and identification of molecular markers linked to the leaf rust resistance gene Lr28 in wheat.CrossRef | 1:CAS:528:DC%2BC3MXhtlSksr7O&md5=8e6991d3eaebfe2c9074dc590eed021dCAS | 21225387PubMed |

Bradford MM (1976) Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.CrossRef | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2c2ac7310259d1cb1f812f0521809a93CAS | 942051PubMed |

Brenchley R, Spannagl M, Pfeifer M, Barker GLA, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo M-C, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KFX, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491, 705–710.
Analysis of the bread wheat genome using whole-genome shotgun sequencing.CrossRef | 1:CAS:528:DC%2BC38XhslCnu7nL&md5=1c8e71cbab490652f473b7c419513a80CAS | 23192148PubMed |

Carey MF, Peterson CL, Smale ST (2012) Experimental strategies for the identification of DNA-binding proteins. Cold Spring Harbor Protocols 1, 18–33.

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 Molecular Biology 68, 81–92.
Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function.CrossRef | 1:CAS:528:DC%2BD1cXptVGltbw%3D&md5=5ea6338342b03f6c13051af35f9aa02fCAS | 18523729PubMed |

de Vries SJ, van Dijk ADJ, Krzeminski M, van Dijk M, Thureau A, Hsu V, Wassenaar T, Bonvin AMJJ (2007) HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets. Proteins: Structure, Function, and Bioinformatics 69, 726–733.
HADDOCK versus HADDOCK: new features and performance of HADDOCK2.0 on the CAPRI targets.CrossRef | 1:CAS:528:DC%2BD2sXhtl2qsbrM&md5=2b99b9317e3cfd11af62e4e63bd17abdCAS |

Dong J, Chen CH, Chen ZX (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Molecular Biology 51, 21–37.
Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response.CrossRef | 1:CAS:528:DC%2BD38XnvFOitL4%3D&md5=5af89db80e26eb4a6c8f6659f86f5d88CAS | 12602888PubMed |

Duan MR, Nan J, Liang YH, Mao P, Lu L, Li L, Wei C, Lai L, Li Y, Su XD (2007) DNA-binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Research 35, 1145–1154.
DNA-binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein.CrossRef | 1:CAS:528:DC%2BD2sXjslOgtrc%3D&md5=c7eba6691616786b0989f7668c5ee678CAS | 17264121PubMed |

Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A (2006) Comparative protein structure modeling using Modeller. Current Protocols in Bioinformatics 5.6, 5.6.1–5.6.30.

Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Current Opinion in Plant Biology 10, 366–371.
Networks of WRKY transcription factors in defense signaling.CrossRef | 1:CAS:528:DC%2BD2sXosFGrsb8%3D&md5=d702f7bdc6edf30ea257e27d11bcf388CAS | 17644023PubMed |

Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends in Plant Science 5, 199–206.
The WRKY superfamily of plant transcription factors.CrossRef | 1:STN:280:DC%2BD3c3kvFalsw%3D%3D&md5=cbe7ba252f2aec8b700c7e9fb3008fe8CAS | 10785665PubMed |

Heinig M, Frishman D (2004) STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Research 32, W500–W502.
STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins.CrossRef | 1:CAS:528:DC%2BD2cXlvFKmsrw%3D&md5=befb4dd57a64aeb38499c0a7d4a91552CAS | 15215436PubMed |

Hu G, Rijkenberg FHJ (1998) Scanning electron microscopy of early infection structure formation by Puccinia recondita f. sp. tritici on and in susceptible and resistant wheat lines. Mycological Research 102, 391–399.
Scanning electron microscopy of early infection structure formation by Puccinia recondita f. sp. tritici on and in susceptible and resistant wheat lines.CrossRef |

Jin JP, Zhang H, Kang L, Guo G, Luo GC (2014) Plant TFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Research 42, D1182–D1187.
Plant TFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors.CrossRef | 1:CAS:528:DC%2BC2cXos1Cq&md5=d357c49467befcd13c110d9583bd32f8CAS |

Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. Journal of Molecular Biology 292, 195–202.
Protein secondary structure prediction based on position-specific scoring matrices.CrossRef | 1:CAS:528:DyaK1MXlvFyksb0%3D&md5=7ef7c45f2a62b1945cf3286ae59829bbCAS | 10493868PubMed |

Kalde M, Barth M, Somssich IE, Lippok B (2003) Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways. Molecular Plant-Microbe Interactions 16, 295–305.
Members of the Arabidopsis WRKY group III transcription factors are part of different plant defense signaling pathways.CrossRef | 1:CAS:528:DC%2BD3sXisVehu74%3D&md5=8bfb1a59c0522f05c3b0972af24cfa60CAS | 12744458PubMed |

Kelley LA, Sternberg MJE (2009) Protein structure prediction on the web: a case study using the Phyre server. Nature Protocols 4, 363–371.
Protein structure prediction on the web: a case study using the Phyre server.CrossRef | 1:CAS:528:DC%2BD1MXivF2itbs%3D&md5=878be2d3af126adf3c849f3a8c1dc117CAS | 19247286PubMed |

Kim KC, Lai Z, Fan B, Chen Z (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. The Plant Cell 20, 2357–2371.
Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense.CrossRef | 1:CAS:528:DC%2BD1cXhtlCnsLvL&md5=03a02fc43f9fa18a02a740c11e00610dCAS | 18776063PubMed |

Liu X, Bai X, Wang X, Chu C (2007) OsWRKY71, a rice transcription factor, is involved in rice defense response. Journal of Plant Physiology 164, 969–979.
OsWRKY71, a rice transcription factor, is involved in rice defense response.CrossRef | 1:CAS:528:DC%2BD2sXhtVSmsL3L&md5=3e689adf0947eab2454734a1936e2878CAS | 16919842PubMed |

Lo Piero AR, Puglisi I, Petrone G (2006) Gene characterization, analysis of expression and in-vitro synthesis of dihdroflavonol 4-reductase from Citrus sinensis (L.) Osback. Phytochemistry 67, 684–695.
Gene characterization, analysis of expression and in-vitro synthesis of dihdroflavonol 4-reductase from Citrus sinensis (L.) Osback.CrossRef | 1:CAS:528:DC%2BD28XivVarur0%3D&md5=f4c8a270d977a7afa09d138f47eff6d1CAS | 16524606PubMed |

Loke JC, Stahlberg EA, Strenski DG, Haas BJ, Wood PC, Li QQ (2005) Compilation of mRNA polyadenylation signals in Arabidopsis revealed a new signal element and potential secondary structures. Plant Physiology 138, 1457–1468.
Compilation of mRNA polyadenylation signals in Arabidopsis revealed a new signal element and potential secondary structures.CrossRef | 1:CAS:528:DC%2BD2MXmvV2ksr8%3D&md5=44f6a856ad6ffee9965ed4955c1ff38eCAS | 15965016PubMed |

Maeo K, Hayashi S, Kojima-Suzuki H, Morikama A, Nakamura K (2001) Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins. Bioscience, Biotechnology, and Biochemistry 65, 2428–2436.
Role of conserved residues of the WRKY domain in the DNA-binding of tobacco WRKY family proteins.CrossRef | 1:CAS:528:DC%2BD3MXovFOgsL8%3D&md5=26ee1291ce88ad4319f08630129a5bb3CAS | 11791715PubMed |

Mangelsen E, Kilian J, Berendzen KW, Kolukisaoglu UH, Harter K, Jansson C, Wanke D (2008) Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare). WRKY transcription factor family reveals putatively retained functions between monocots and dicots. BMC Genomics 9, 194
Phylogenetic and comparative gene expression analysis of barley (Hordeum vulgare). WRKY transcription factor family reveals putatively retained functions between monocots and dicots.CrossRef | 18442363PubMed |

McIntosh RA, Pretorius ZA (2011) Borlaug Global Rust Initiative provides momentum for wheat rust research. Euphytica 179, 1–2.
Borlaug Global Rust Initiative provides momentum for wheat rust research.CrossRef |

Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran LS (2011) In silico analysis of transcription factor repertoires and prediction of stress-responsive transcription factors from six major gramineae plants. DNA Research 18, 321–332.
In silico analysis of transcription factor repertoires and prediction of stress-responsive transcription factors from six major gramineae plants.CrossRef | 1:CAS:528:DC%2BC3MXhtlaisLzK&md5=21897719171e9eec6dc02271b2fd2679CAS | 21729923PubMed |

Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4326.
Rapid isolation of high molecular weight plant DNA.CrossRef | 1:CAS:528:DyaL3cXmtVSmtL8%3D&md5=5b3e7876affb7ca9aa7f5338cd92e00dCAS | 7433111PubMed |

Niu CF, Wei W, Zhou QY, Tian AG, Hao YJ, Zhang WK, Ma B, Lin Q, Zhang ZB, Zhang JS, Chen SY (2012) Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in Arabidopsis plants. Plant, Cell & Environment 35, 1156–1170.
Wheat WRKY genes TaWRKY2 and TaWRKY19 regulate abiotic stress tolerance in Arabidopsis plants.CrossRef | 1:CAS:528:DC%2BC38XptF2ktb0%3D&md5=127adc82dcf387e8bd605e3468e83df6CAS |

Paolacci AR, Tanzarella OA, Porceddu E, Ciaffi M (2009) Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Molecular Biology 10, 11
Identification and validation of reference genes for quantitative RT-PCR normalization in wheat.CrossRef | 19232096PubMed |

Proietti S, Bertini L, Van der Ent S, Leon-Reyes A, Pieterse CMJ, Tucci M, Caporale C, Caruso C (2011) Cross activity of orthologous WRKY transcription factors in wheat and Arabidopsis. Journal of Experimental Botany 62, 1975–1990.
Cross activity of orthologous WRKY transcription factors in wheat and Arabidopsis.CrossRef | 1:CAS:528:DC%2BC3MXjsFyjur8%3D&md5=06363afffef8d9fa2669387aa3ea4403CAS | 21193575PubMed |

Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant & Cell Physiology 49, 865–879.
A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments.CrossRef | 1:CAS:528:DC%2BD1cXpt1Wjtbw%3D&md5=44a923ae157a29817656df43601b458dCAS |

Rieu I, Powers SJ (2009) Real-time quantitative RT-PCR: design, calculations and statistics. The Plant Cell 21, 1031–1033.
Real-time quantitative RT-PCR: design, calculations and statistics.CrossRef | 1:CAS:528:DC%2BD1MXntFamsrY%3D&md5=c0485f17179892af2d27b40f6174f34dCAS | 19395682PubMed |

Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends in Plant Science 15, 247–258.
WRKY transcription factors.CrossRef | 1:CAS:528:DC%2BC3cXlvVaqsbk%3D&md5=b9769266d0904cdb07624c61f1d74ad6CAS | 20304701PubMed |

Ryu HS, Han M, Lee SK, Cho JI, Ryoo N, Heu S, Lee YH, Bhoo SH, Wang GL, Hahn TR, Jeon JS (2006) A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response. Plant Cell Reports 25, 836–847.
A comprehensive expression analysis of the WRKY gene superfamily in rice plants during defense response.CrossRef | 1:CAS:528:DC%2BD28XmvFarsL0%3D&md5=714429a1cd9ca512ce2cf1cd027eb426CAS | 16528562PubMed |

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. The Plant Cell 19, 2064–2076.
Rice WRKY45 plays a crucial role in benzothiadiazole-inducible blast resistance.CrossRef | 1:CAS:528:DC%2BD2sXptFKns7c%3D&md5=13b84d2e1e376f81329aa39269ee06b9CAS | 17601827PubMed |

Singh KB, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Current Opinion in Plant Biology 5, 430–436.
Transcription factors in plant defense and stress responses.CrossRef | 1:CAS:528:DC%2BD38XmtlGjtbw%3D&md5=531842ec85eaa9e669147de4557b5fa4CAS |

Singh D, Bhaganagare G, Bandopadhyay R, Prabhu KV, Gupta PK, Mukhopadhyay K (2012) Targeted spatio-temporal expression based characterization of state of infection and time-point of maximum defense in wheat NILs during leaf-rust infection. Molecular Biology Reports 39, 9373–9382.
Targeted spatio-temporal expression based characterization of state of infection and time-point of maximum defense in wheat NILs during leaf-rust infection.CrossRef | 1:CAS:528:DC%2BC38Xht1ynsbrI&md5=5077b2c09cd3a53f0451794bd0a39cb3CAS | 22736109PubMed |

Tamura K, Peterson D, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 2731–2739.
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.CrossRef | 1:CAS:528:DC%2BC3MXht1eiu73K&md5=40ed56ce26272e9b9c9349302f2346caCAS | 21546353PubMed |

Tina KG, Bhadra R, Srinivasan N (2007) PIC: protein interactions calculator. Nucleic Acids Research 35, W473–W476.
PIC: protein interactions calculator.CrossRef | 1:STN:280:DC%2BD2svhsVOltQ%3D%3D&md5=baf5827a9b53a57a3d054d9f3d4f9120CAS | 17584791PubMed |

Tripathi P, Rabara RC, Langum TJ, Boken AK, Rushton DL, Boomsma DD, Rinerson CI, Rabara J, Reese RN, Chen X, Rohila JS, Rushton PJ (2012) The WRKY transcription factor family in Brachypodium distachyon. BMC Genomics 13, 270
The WRKY transcription factor family in Brachypodium distachyon.CrossRef | 1:CAS:528:DC%2BC3sXot1Wmt7g%3D&md5=bec3ebce3f380e78999327622574a66fCAS | 22726208PubMed |

Ülker B, Somssich IE (2004) WRKY transcription factors: from DNA-binding towards biological function. Current Opinion in Plant Biology 7, 491–498.
WRKY transcription factors: from DNA-binding towards biological function.CrossRef | 15337090PubMed |

van Aken O, Zhang B, Law S, Narsai R, Whelan J (2013) AtWRKY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondria and chloroplast proteins. Plant Physiology 162, 254–271.
AtWRKY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondria and chloroplast proteins.CrossRef | 1:CAS:528:DC%2BC3sXnvVWksL0%3D&md5=4cc07317594ab5c001e3485f0c1ad215CAS | 23509177PubMed |

van Dijk M, Bonvin AMJJ (2009) 3D-DART: a DNA structure modeling server. Nucleic Acids Research 37, W235–W239.
3D-DART: a DNA structure modeling server.CrossRef | 1:CAS:528:DC%2BD1MXosFSrsL8%3D&md5=1afe168c3dc8fc61b2e2d255b97654fbCAS | 19417072PubMed |

Wei KF, Chen J, Chen YF, Wu LJ, Xie DX (2012) Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize. DNA Research 19, 153–164.
Molecular phylogenetic and expression analysis of the complete WRKY transcription factor family in maize.CrossRef | 1:CAS:528:DC%2BC38XlsFektrk%3D&md5=bfe8f919c15e6b1fdce5402648c2dbdcCAS | 22279089PubMed |

Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research 35, W407–W410.
ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins.CrossRef | 17517781PubMed |

Wu KL, Guo ZJ, Wang HH, Li J (2005) The WRKY family of transcription factors in rice and Arabidopsis and their origins. DNA Research 12, 9–26.
The WRKY family of transcription factors in rice and Arabidopsis and their origins.CrossRef | 1:CAS:528:DC%2BD2MXktFKqs7k%3D&md5=19d74a842c905093102cd7a48fb1b901CAS | 16106749PubMed |

Wu H, Ni Z, Yao Y, Guo G, Sun Q (2008) Cloning and expression profiles of 15 genes encoding WRKY transcription factor in wheat (Triticum aestivem L.). Progress in Natural Science 18, 697–705.
Cloning and expression profiles of 15 genes encoding WRKY transcription factor in wheat (Triticum aestivem L.).CrossRef | 1:CAS:528:DC%2BD1cXhtVSgsbrJ&md5=cce170d02d55bffa4a0df29a3f4502c7CAS |

Yamasaki K, Kigawa T, Inoue M, Watanabe S, Tateno M, Seki M, Shinozaki K, Yokoyama S (2008) Structures and evolutionary origins of plant-specific transcription factor DNA-binding domains. Plant Physiology and Biochemistry 46, 394–401.
Structures and evolutionary origins of plant-specific transcription factor DNA-binding domains.CrossRef | 1:CAS:528:DC%2BD1cXjs1KmsLY%3D&md5=614ed62da5270742f946d69504b0d8d5CAS | 18272381PubMed |

Yamasaki K, Kigawa T, Watanabe S, Inoue M, Yamasaki T, Seki M, Shinozaki K, Yokoyama S (2012) Structural basis of sequence-specific DNA recognition by an Arabidopsis WRKY transcription factor. Journal of Biological Chemistry 287, 7683–7691.
Structural basis of sequence-specific DNA recognition by an Arabidopsis WRKY transcription factor.CrossRef | 1:CAS:528:DC%2BC38XjtFyksLs%3D&md5=775f3e4e179ff18e9df01c002afa0e74CAS | 22219184PubMed |

Yaneva M, Kowalewski T, Lieber MR (1997) Interaction of DNA-dependent protein kinase with DNA and with Ku: biochemical and atomic-force microscopy studies. EMBO Journal 16, 5098–5112.
Interaction of DNA-dependent protein kinase with DNA and with Ku: biochemical and atomic-force microscopy studies.CrossRef | 1:CAS:528:DyaK2sXlslyjtr0%3D&md5=20ee5c2e4c33a1b5c03ed4b1aa508d65CAS | 9305651PubMed |

Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 23, 9–40.

Zhang YJ, Wang LJ (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evolutionary Biology 5, 1
The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants.CrossRef | 1:CAS:528:DC%2BD2MXhvVeqt74%3D&md5=b23236aa83fb0cca043b69675ed676faCAS |

Zhu X, Liu S, Meng C, Quin L, Kong L, Xia G (2013) WRKY transcription factors in wheat and their induction by biotic and abiotic stress. Plant Molecular Biology Reporter 31, 1053–1067.
WRKY transcription factors in wheat and their induction by biotic and abiotic stress.CrossRef | 1:CAS:528:DC%2BC3sXhtlOju77K&md5=9f7dbf9bc4959c1ade90d9ffdf3b16eeCAS |



Rent Article (via Deepdyve) Supplementary MaterialSupplementary Material (545 KB) Export Citation Cited By (4)