Plant Cell Reports

, Volume 36, Issue 11, pp 1757–1773 | Cite as

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

  • Bernard Kinuthia Karanja
  • Lianxue Fan
  • Liang Xu
  • Yan Wang
  • Xianwen Zhu
  • Mingjia Tang
  • Ronghua Wang
  • Fei Zhang
  • Everlyne M’mbone Muleke
  • Liwang Liu
Original Article

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.

Keywords

Raphanus sativus WRKY transcription factor Abiotic stress RT-qPCR 

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

Notes

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).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

299_2017_2190_MOESM1_ESM.tif (248 kb)
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 (498 kb)
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 (410 kb)
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 (2 mb)
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 (1.3 mb)
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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References

  1. 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 14:236CrossRefPubMedPubMedCentralGoogle Scholar
  2. 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 4:1–21CrossRefGoogle Scholar
  3. 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 10:281CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 1819:120–128CrossRefPubMedGoogle Scholar
  5. 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 464:962–968CrossRefPubMedGoogle Scholar
  6. 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:e0157026CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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 68:81–92CrossRefGoogle Scholar
  8. 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 21:3674–3676CrossRefPubMedGoogle Scholar
  9. Crooks GE, Hon G, Chandonia J-M, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14:1188–1190CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dai X, Wang Y, Zhang W-H (2015) OsWRKY74, a WRKY transcription factor, modulates tolerance to phosphate starvation in rice. J Exp Bot 67:947–960CrossRefPubMedPubMedCentralGoogle Scholar
  11. Eulgem T, Rushton P, Robatzek S (2000) Somssich I (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206CrossRefPubMedGoogle Scholar
  12. 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–D815CrossRefPubMedGoogle Scholar
  13. 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 22:121–129CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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 7:209CrossRefGoogle Scholar
  15. Göhre V, Jones AM, Sklenář J, Robatzek S, Weber AP (2012) Molecular crosstalk between PAMP-triggered immunity and photosynthesis. Mol Plant Microbe Interact 25:1083–1092CrossRefPubMedGoogle Scholar
  16. 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 65:1513–1528CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hall BG (2013) Building phylogenetic trees from molecular data with MEGA. Mol Biol Evol 30:1229–1235CrossRefPubMedGoogle Scholar
  18. 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 31:1199–1217CrossRefPubMedGoogle Scholar
  19. 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:e0157558CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 25:2699–2713CrossRefPubMedPubMedCentralGoogle Scholar
  21. 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 197:50–58CrossRefPubMedGoogle Scholar
  22. Jiang Y, Deyholos MK (2006) Comprehensive transcriptional profiling of NaCl-stressed Arabidopsis roots reveals novel classes of responsive genes. BMC Plant Biol 6:1CrossRefGoogle Scholar
  23. 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):6629–6644CrossRefPubMedPubMedCentralGoogle Scholar
  24. 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 7:1029CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 21:481–490CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 2:676CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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 23:3824–3841CrossRefPubMedPubMedCentralGoogle Scholar
  28. 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–D260CrossRefPubMedGoogle Scholar
  29. Li S, Fu Q, Chen L, Huang W, Yu D (2011) Arabidopsis thaliana WRKY25, WRKY26, and WRKY33 coordinate induction of plant thermotolerance. Planta 233:1237–1252CrossRefPubMedGoogle Scholar
  30. 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:e1002767CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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 70:207–216CrossRefGoogle Scholar
  32. 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 200:457–472CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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 12:454CrossRefGoogle Scholar
  34. Liu RH, Meng J (2003) MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Yi Chuan 25:317–321PubMedGoogle Scholar
  35. 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:e1003790CrossRefPubMedPubMedCentralGoogle Scholar
  36. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408CrossRefPubMedGoogle Scholar
  37. 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 65:2428–2436CrossRefPubMedGoogle Scholar
  38. 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 103:71–83CrossRefPubMedGoogle Scholar
  39. 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:e52784CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 5:10835CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mukhopadhyay M, Mondal TK (2015) Effect of zinc and boron on growth and water relations of Camellia sinensis. Natl Acad Sci Lett 38:283–286CrossRefGoogle Scholar
  42. 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 5:14034CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 457:551–556CrossRefPubMedGoogle Scholar
  44. Qiu Y, Yu D (2009) Over-expression of the stress-induced OsWRKY45 enhances disease resistance and drought tolerance in Arabidopsis. Environ Exp Bot 65:35–47CrossRefGoogle Scholar
  45. 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 53:94–100CrossRefPubMedGoogle Scholar
  46. Ross C, Liu Y, Shen Q (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842CrossRefGoogle Scholar
  47. Rushton P, Somssich I, Ringler P, Shen Q (2010) WRKY transcription factors. Trends Plant Sci 15:247–258CrossRefPubMedGoogle Scholar
  48. 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 34:374–378PubMedGoogle Scholar
  49. 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 83:265–277CrossRefPubMedGoogle Scholar
  50. Schluttenhofer C, Yuan L (2015) Regulation of specialized metabolism by WRKY transcription factors. Plant Physiol 167:295–306CrossRefPubMedGoogle Scholar
  51. Shaik R, Ramakrishna W (2013) Genes and co-expression modules common to drought and bacterial stress responses in Arabidopsis and rice. PLoS One 8:e77261CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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 13:2498–2504CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 14:721CrossRefGoogle Scholar
  54. 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 14:1CrossRefGoogle Scholar
  55. 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 16:197CrossRefGoogle Scholar
  56. 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 569:118–126CrossRefPubMedGoogle Scholar
  57. 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 35:329–346CrossRefPubMedGoogle Scholar
  58. 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 13:1CrossRefGoogle Scholar
  59. 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 15:141–152CrossRefPubMedGoogle Scholar
  60. 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 68:1563–1575CrossRefPubMedGoogle Scholar
  61. 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 230:1155CrossRefPubMedGoogle Scholar
  62. 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:e66539CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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 14:1CrossRefGoogle Scholar
  64. 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 6:417PubMedPubMedCentralGoogle Scholar
  65. 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 33:867–880CrossRefGoogle Scholar
  66. 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 16:17CrossRefGoogle Scholar
  67. 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 27:795–803CrossRefPubMedGoogle Scholar
  68. 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 19:153–164CrossRefPubMedPubMedCentralGoogle Scholar
  69. 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 15:741–752CrossRefGoogle Scholar
  70. 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 6:202PubMedPubMedCentralGoogle Scholar
  71. 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 201–202:108–114CrossRefPubMedGoogle Scholar
  72. 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 64:4271–4287CrossRefPubMedPubMedCentralGoogle Scholar
  73. 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 6:18752CrossRefPubMedPubMedCentralGoogle Scholar
  74. 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 15:30CrossRefPubMedPubMedCentralGoogle Scholar
  75. Zentgraf U, Laun T, Miao Y (2010) The complex regulation of WRKY53 during leaf senescence of Arabidopsis thaliana. Eur J Cell Biol 89:133–137CrossRefPubMedGoogle Scholar
  76. 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 6:21652CrossRefPubMedPubMedCentralGoogle Scholar
  77. 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–D1117CrossRefPubMedGoogle Scholar
  78. 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 7:1054Google Scholar
  79. 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 169:1243–1252CrossRefPubMedGoogle Scholar
  80. 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 565:130–139CrossRefPubMedGoogle Scholar
  81. 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 6:486–503CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Bernard Kinuthia Karanja
    • 1
  • Lianxue Fan
    • 1
  • Liang Xu
    • 1
  • Yan Wang
    • 1
  • Xianwen Zhu
    • 2
  • Mingjia Tang
    • 1
  • Ronghua Wang
    • 1
  • Fei Zhang
    • 1
  • Everlyne M’mbone Muleke
    • 1
  • Liwang Liu
    • 1
  1. 1.National Key Laboratory of Crop Genetics and Germplasm Enhancement, Key Laboratory of Horticultural Crop Biology and Genetic Improvement (East China) of MOA, College of HorticultureNanjing Agricultural UniversityNanjingPeople’s Republic of China
  2. 2.Department of Plant SciencesNorth Dakota State UniversityFargoUSA

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