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Genome-wide characterization of the WRKY gene family in radish (Raphanus sativus L.) reveals its critical functions under different abiotic stresses

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Abstract

Key message

The radish WRKY gene family was genome-widely identified and played critical roles in response to multiple abiotic stresses.

Abstract

The WRKY is among the largest transcription factors (TFs) associated with multiple biological activities for plant survival, including control response mechanisms against abiotic stresses such as heat, salinity, and heavy metals. Radish is an important root vegetable crop and therefore characterization and expression pattern investigation of WRKY transcription factors in radish is imperative. In the present study, 126 putative WRKY genes were retrieved from radish genome database. Protein sequence and annotation scrutiny confirmed that RsWRKY proteins possessed highly conserved domains and zinc finger motif. Based on phylogenetic analysis results, RsWRKYs candidate genes were divided into three groups (Group I, II and III) with the number 31, 74, and 20, respectively. Additionally, gene structure analysis revealed that intron–exon patterns of the WRKY genes are highly conserved in radish. Linkage map analysis indicated that RsWRKY genes were distributed with varying densities over nine linkage groups. Further, RT-qPCR analysis illustrated the significant variation of 36 RsWRKY genes under one or more abiotic stress treatments, implicating that they might be stress-responsive genes. In total, 126 WRKY TFs were identified from the R. sativus genome wherein, 35 of them showed abiotic stress-induced expression patterns. These results provide a genome-wide characterization of RsWRKY TFs and baseline for further functional dissection and molecular evolution investigation, specifically for improving abiotic stress resistances with an ultimate goal of increasing yield and quality of radish.

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Abbreviations

aa:

Amino acids

BLAST:

Basic local alignment search tool

bp:

Base pair

Cd:

Cadmium

CDS:

Coding sequence

GO:

Gene ontology

HM:

Heavy metal

LG:

Linkage group

MW:

Molecular weight

Pb:

Lead

pI:

Isoelectric point

RT-qPCR:

Reverse transcription-quantitative polymerase chain reaction

TF:

Transcription factor

References

  • Bencke-Malato M, Cabreira C, Wiebke-Strohm B, Bücker-Neto L, Mancini E, Osorio MB, Homrich MS, Turchetto-Zolet AC, De Carvalho MC, Stolf R (2014) Genome-wide annotation of the soybean WRKY family and functional characterization of genes involved in response to Phakopsora pachyrhizi infection. BMC Plant Biol 14:236

    Article  PubMed  PubMed Central  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:1–21

    Article  Google Scholar 

  • Chen H, Lai Z, Shi J, Xiao Y, Chen Z, Xu X (2010) Roles of Arabidopsis WRKY18, WRKY40 and WRKY60 transcription factors in plant responses to abscisic acid and abiotic stress. BMC Plant Biol 10:281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1819:120–128

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Yang Y, Liu C, Zheng Y, Xu M, Wu N, Sheng J, Shen L (2015) Characterization of WRKY transcription factors in Solanum lycopersicum reveals collinearity and their expression patterns under cold treatment. Biochem Biophys Res Commun 464:962–968

    Article  CAS  PubMed  Google Scholar 

  • Chu X, Wang C, Chen X, Lu W, Li H, Wang X, Hao L, Guo X (2016) Correction: the cotton WRKY gene GhWRKY41 positively regulates salt and drought stress tolerance in transgenic Nicotiana benthamiana. PLoS One 11:e0157026

    Article  PubMed  PubMed Central  Google Scholar 

  • Ciolkowski I, Wanke D, Birkenbihl R, Somssich I (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol Rep 68:81–92

    Article  CAS  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dai X, Wang Y, Zhang W-H (2015) OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Exp Bot 67:947–960

    Article  PubMed  PubMed Central  Google Scholar 

  • Eulgem T, Rushton P, Robatzek S (2000) Somssich I (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  CAS  PubMed  Google Scholar 

  • Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, Von Mering C (2013) STRING v9. 1: protein–protein interaction networks, with increased coverage and integration. Nucleic Acids Res 41:D808–D815

    Article  CAS  PubMed  Google Scholar 

  • Gautam S, Anjani K, Srivastava N (2016) In vitro evaluation of excess copper affecting seedlings and their biochemical characteristics in Carthamus tinctorius L. (variety PBNS-12). Physiol Mol Biol Plants 22:121–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 7:209

    Article  Google Scholar 

  • Göhre V, Jones AM, Sklenář J, Robatzek S, Weber AP (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol Plant Microbe Interact 25:1083–1092

    Article  PubMed  Google Scholar 

  • Guo C, Guo R, Xu X, Gao M, Li X, Song J, Zheng Y, Wang X (2014) Evolution and expression analysis of the grape (Vitis vinifera L.) WRKY gene family. J Exp Bot 65:1513–1528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235

    Article  CAS  PubMed  Google Scholar 

  • He H, Dong Q, Shao Y, Jiang H, Zhu S, Cheng B, Xiang Y (2012) Genome-wide survey and characterization of the WRKY gene family in Populus trichocarpa. Plant Cell Rep 31:1199–1217

    Article  CAS  PubMed  Google Scholar 

  • He Y, Mao S, Gao Y, Zhu L, Wu D, Cui Y, Li J, Qian W (2016) Genome-wide identification and expression analysis of WRKY transcription factors under multiple stresses in Brassica napus. PLoS One 11:e0157558

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsu F-C, Chou M-Y, Chou S-J, Li Y-R, Peng H-P, Shih M-C (2013) Submergence confers immunity mediated by the WRKY22 transcription factor in Arabidopsis. Plant Cell 25:2699–2713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:1

    Article  Google Scholar 

  • Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Fan D, Luo K (2014) Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot 65(22):6629–6644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joshi R, Wani SH, Singh B, Bohra A, Dar ZA, Lone AA, Pareek A, Singla-Pareek SL (2016) Transcription factors and plants response to drought stress: current understanding and future directions. Front Plant Sci 7:1029

    Article  PubMed  PubMed Central  Google Scholar 

  • Kitashiba H, Li F, Hirakawa H, Kawanabe T, Zou Z, Hasegawa Y, Tonosaki K, Shirasawa S, Fukushima A, Yokoi S (2014) Draft sequences of the radish (Raphanus sativus L.) genome. DNA Res 21:481–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulhari A, Sheorayan A, Bajar S, Sarkar S, Chaudhury A, Kalia RK (2013) Investigation of heavy metals in frequently utilized medicinal plants collected from environmentally diverse locations of north western India. SpringerPlus 2:676

    Article  PubMed  PubMed Central  Google Scholar 

  • Lai Z, Li Y, Wang F, Cheng Y, Fan B, Yu J-Q, Chen Z (2011) Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in plant defense. Plant Cell 23:3824–3841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Copley RR, Pils B, Pinkert S, Schultz J, Bork P (2006) SMART 5: domains in the context of genomes and networks. Nucleic Acids Res 34:D257–D260

    Article  CAS  PubMed  Google Scholar 

  • Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233:1237–1252

    Article  CAS  PubMed  Google Scholar 

  • 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:e1002767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li H, Gao Y, Xu H, Dai Y, Deng D, Chen J (2013a) ZmWRKY33, a WRKY maize transcription factor conferring enhanced salt stress tolerances in Arabidopsis. J Plant Growth Regul 70:207–216

    Article  CAS  Google Scholar 

  • Li J, Besseau S, Törönen P, Sipari N, Kollist H, Holm L, Palva ET (2013b) Defense-related transcription factors WRKY70 and WRKY54 modulate osmotic stress tolerance by regulating stomatal aperture in Arabidopsis. New Phytol 200:457–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ling J, Jiang W, Zhang Y, Yu H, Mao Z, Gu X, Huang S, Xie B (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genom 12:454

    Article  Google Scholar 

  • Liu RH, Meng J (2003) MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Yi Chuan 25:317–321

    PubMed  Google Scholar 

  • Liu S, Wang X, Wang H, Xin H, Yang X, Yan J, Li J, Tran L-SP, Shinozaki K, Yamaguchi-Shinozaki K (2013) Genome-wide analysis of ZmDREB genes and their association with natural variation in drought tolerance at seedling stage of Zea mays L. PLoS Genet 9:e1003790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • 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 65:2428–2436

    Article  CAS  PubMed  Google Scholar 

  • Meng D, Li Y, Bai Y, Li M, Cheng L (2016) Genome-wide identification and characterization of WRKY transcriptional factor family in apple and analysis of their responses to waterlogging and drought stress. Plant Physiol Biochem 103:71–83

    Article  CAS  PubMed  Google Scholar 

  • Mishra S, Triptahi V, Singh S, Phukan UJ, Gupta M, Shanker K, Shukla RK (2013) Wound induced tanscriptional regulation of benzylisoquinoline pathway and characterization of wound inducible PsWRKY transcription factor from Papaver somniferum. PLoS One 8:e52784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitsui Y, Shimomura M, Komatsu K, Namiki N, Shibata-Hatta M, Imai M, Katayose Y, Mukai Y, Kanamori H, Kurita K (2015) The radish genome and comprehensive gene expression profile of tuberous root formation and development. Sci Rep 5:10835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukhopadhyay M, Mondal TK (2015) Effect of zinc and boron on growth and water relations of Camellia sinensis. Natl Acad Sci Lett 38:283–286

    Article  CAS  Google Scholar 

  • Nie S, Xu L, Wang Y, Huang D, Muleke EM, Sun X, Wang R, Xie Y, Gong Y, Liu L (2015) Identification of bolting-related microRNAs and their targets reveals complex miRNA-mediated flowering-time regulatory networks in radish (Raphanus sativus L.). Sci Rep 5:14034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556

    Article  CAS  PubMed  Google Scholar 

  • Qiu Y, Yu D (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65:35–47

    Article  CAS  Google Scholar 

  • Rodriguez E, Santos C, Azevedo R, Moutinho-Pereira J, Correia C, Dias MC (2012) Chromium (VI) induces toxicity at different photosynthetic levels in pea. Plant Physiol Biochem 53:94–100

    Article  CAS  PubMed  Google Scholar 

  • Ross C, Liu Y, Shen Q (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842

    Article  CAS  Google Scholar 

  • Rushton P, Somssich I, Ringler P, Shen Q (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  CAS  PubMed  Google Scholar 

  • Saeed A, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378

    CAS  PubMed  Google Scholar 

  • Scarpeci TE, Zanor MI, Mueller-Roeber B, Valle EM (2013) Overexpression of AtWRKY30 enhances abiotic stress tolerance during early growth stages in Arabidopsis thaliana. Plant Mol Biol 83:265–277

    Article  CAS  PubMed  Google Scholar 

  • Schluttenhofer C, Yuan L (2015) Regulation of specialized metabolism by WRKY transcription factors. Plant Physiol 167:295–306

    Article  CAS  PubMed  Google Scholar 

  • Shaik R, Ramakrishna W (2013) Genes and co-expression modules common to drought and bacterial stress responses in Arabidopsis and rice. PLoS One 8:e77261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen D, Sun H, Huang M, Zheng Y, Qiu Y, Li X, Fei ZJ (2013) Comprehensive analysis of expressed sequence tags from cultivated and wild radish (Raphanus spp.). BMC Genom 14:721

    Article  CAS  Google Scholar 

  • Song X, Li Y, Hou X (2013) Genome-wide analysis of the AP2/ERF transcription factor superfamily in Chinese cabbage (Brassica rapa ssp. pekinensis). BMC Genom 14:1

    Article  CAS  Google Scholar 

  • Sun X, Xu L, Wang Y, Yu R, Zhu X, Luo X, Gong Y, Wang R, Limera C, Zhang K, Liu L (2015a) Identification of novel and salt-responsive miRNAs to explore miRNA-mediated regulatory network of salt stress response in radish (Raphanus sativus L.). BMC Genom 16:197

    Article  Google Scholar 

  • Sun Y, Qiu Y, Zhang X, Chen X, Shen D, Wang H, Li X (2015b) Genome-wide identification of microRNAs associated with taproot development in radish (Raphanus sativus L.). Gene 569:118–126

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Xu L, Wang Y, Luo X, Zhu X, Kinuthia KB, Nie S, Feng H, Li C, Liu L (2016) Transcriptome-based gene expression profiling identifies differentially expressed genes critical for salt stress response in radish (Raphanus sativus L.). Plant Cell Rep 35:329–346

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Wang F, Wang Z, Huang Z, Xiong A, Hou X (2013) Characterization and co-expression analysis of WRKY orthologs involved in responses to multiple abiotic stresses in Pak-choi (Brassica campestris ssp. chinensis). BMC Plant Biol 13:1

    Article  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Dóczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152

    Article  CAS  PubMed  Google Scholar 

  • Vernay P, Gauthier-Moussard C, Hitmi A (2007) Interaction of bioaccumulation of heavy metal chromium with water relation, mineral nutrition and photosynthesis in developed leaves of Lolium perenne L. Chemosphere 68:1563–1575

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Xu L, Chen Y, Shen H, Gong Y, Limera C, Liu L (2013) Transcriptome profiling of radish (Raphanus sativus L.) root and identification of genes involved in response to Lead (Pb) stress with next generation sequencing. PLoS One 8:e66539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Zhu W, Fang L, Sun X, Su L, Liang Z, Wang N, Londo JP, Li S, Xin H (2014) Genome-wide identification of WRKY family genes and their response to cold stress in Vitis vinifera. BMC Plant Biol 14:1

    Article  Google Scholar 

  • Wang M, Vannozzi A, Wang G, Zhong Y, Corso M, Cavallini E, Cheng Z-MM (2015a) A comprehensive survey of the grapevine VQ gene family and its transcriptional correlation with WRKY proteins. Front Plant Sci 6:417

    PubMed  PubMed Central  Google Scholar 

  • Wang R, Xu L, Zhu X, Zhai L, Wang Y, Yu R, Gong Y, Limera C, Liu L (2015b) Transcriptome-wide characterization of novel and heat-stress-responsive microRNAs in radish (Raphanus sativus L.) using next-generation sequencing. Plant Mol Biol Rep 33:867–880

    Article  CAS  Google Scholar 

  • Wang Z, Tang J, Hu R, Wu P, Hou XL, Song XM, Xiong AS (2015c) Genome-wide analysis of the R2R3-MYB transcription factor genes in Chinese cabbage (Brassica rapa ssp. pekinensis) reveals their stress and hormone responsive patterns. BMC Genom 16:17

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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 Res 19:153–164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu Z-J, Li X-H, Liu Z-W, Li H, Wang Y-X, Zhuang J (2015) Transcriptome-based discovery of AP2/ERF transcription factors related to temperature stress in tea plant (Camellia sinensis). Funct Integr Genom 15:741–752

    Article  CAS  Google Scholar 

  • Xie Y, Ye S, Wang Y, Xu L, Zhu X, Yang J, Feng H, Yu R, Karanja B, Gong Y (2015) Transcriptome-based gene profiling provides novel insights into the characteristics of radish root response to Cr stress with next-generation sequencing. Front Plant Sci 6:202

    PubMed  PubMed Central  Google Scholar 

  • Xu L, Wang Y, Xu Y, Wang L, Zhai L, Zhu X, Gong Y, Ye S, Liu L (2013a) Identification and characterization of novel and conserved microRNAs in radish (Raphanus sativus L.) using high-throughput sequencing. Plant Sci 201–202:108–114

    Article  PubMed  Google Scholar 

  • Xu L, Wang Y, Zhai LL, Xu Y, Wang LJ, Zhu XW, Gong YQ, Yu RG, Limera C, Liu LW (2013b) Genome-wide identification and characterization of cadmium-responsive microRNAs and their target genes in radish (Raphanus sativus L.) roots. J Exp Bot 64:4271–4287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang G, Wang C, Wang Y, Guo Y, Zhao Y, Yang C, Gao C (2016) Overexpression of ThVHAc1 and its potential upstream regulator, ThWRKY7, improved plant tolerance of cadmium stress. Sci Rep 6:18752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu R, Wang Y, Xu L, Zhu X, Zhang W, Wang R, Gong Y, Limera C, Liu L (2015) Transcriptome profiling of root microRNAs reveals novel insights into taproot thickening in radish (Raphanus sativus L.). BMC Plant Biol 15:30

    Article  PubMed  PubMed Central  Google Scholar 

  • Zentgraf U, Laun T, Miao Y (2010) The complex regulation of WRKY53 during leaf senescence of Arabidopsis thaliana. Eur J Cell Biol 89:133–137

    Article  CAS  PubMed  Google Scholar 

  • Zhai L, Xu L, Wang Y, Zhu X, Feng H, Li C, Luo X, Everlyne MM, Liu L (2016) Transcriptional identification and characterization of differentially expressed genes associated with embryogenesis in radish (Raphanus sativus L.). Sci Rep 6:21652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39:D1114–D1117

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Xie Y, Xu L, Wang Y, Zhu X, Wang R, Zhang Y, Muleke E, Liu L (2016) Identification of microRNAs and their target genes explores miRNA-mediated regulatory network of cytoplasmic male sterility occurrence during anther development in radish (Raphanus sativus L.). Front. Plant Sci 7:1054

    Google Scholar 

  • Zhao H, Wu L, Chai T, Zhang Y, Tan J, Ma S (2012) The effects of copper, manganese and zinc on plant growth and elemental accumulation in the manganese-hyperaccumulator Phytolacca americana. J Plant Physiol 169:1243–1252

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Wang S, Chen S, Jiang J, Liu G (2015) Phylogenetic and stress-responsive expression analysis of 20 WRKY genes in Populus simonii × Populus nigra. Gene 565:130–139

    Article  CAS  PubMed  Google Scholar 

  • Zhou QY, Tian AG, Zou HF, Xie ZM, Lei G, Huang J, Wang CM, Wang HW, Zhang JS, Chen SY (2008) Soybean WRKY-type transcription factor genes, GmWRKY13, GmWRKY21, and GmWRKY54, confer differential tolerance to abiotic stresses in transgenic Arabidopsis plants. Plant Biotechnol J 6:486–503

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The current work was partly funded by Grants from the Natural Science Foundation of China (31372064, 31501759, 31601766), National Key Technology Research and Development Program of China (2016YFD0100204-25), Key Technology R&D Program of Jiangsu Province (BE2016379), and Jiangsu Agricultural Science and Technology Innovation Fund (CX(16)1012).

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Correspondence to Liwang Liu.

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Communicated by Qiaochun Wang.

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299_2017_2190_MOESM1_ESM.tif

Fig. S1 Putative isoelectric points and molecular weights of WRKY proteins Group I, II and III in R. sativus (TIFF 248 kb)

299_2017_2190_MOESM2_ESM.tif

Fig. S2 The schematic diagram of the logo diagrams of ten motifs analyzed in all the 126 WRKY protein sequence in radish (TIFF 497 kb)

299_2017_2190_MOESM3_ESM.tif

Fig. S3 Gene ontology (GO) analysis and distribution of 126 RsWRKY genes into biological process, cellular component, and molecular functions (TIFF 410 kb)

299_2017_2190_MOESM4_ESM.tif

Fig. S4 Heat map showing WRKY genes expression pattern in radish expressed at various developmental stages in leaves, root, root tips, and cambium of radish. The heat map was created using Multi-Experiment Viewer (MeV 4.8) program (TIFF 2064 kb)

299_2017_2190_MOESM5_ESM.tif

Fig. S5 Heat map illustrating WRKY gene transcripts pattern from our radish lab data at different growth stages and biotic stresses. The heat map was created using Multi-Experiment Viewer (MeV 4.8) program (TIFF 1381 kb)

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Karanja, B.K., Fan, L., Xu, L. et al. Genome-wide characterization of the WRKY gene family in radish (Raphanus sativus L.) reveals its critical functions under different abiotic stresses. Plant Cell Rep 36, 1757–1773 (2017). https://doi.org/10.1007/s00299-017-2190-4

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