Skip to main content
SpringerLink
Log in

Genome-wide identification of WRKY transcription factors in kiwifruit (Actinidia spp.) and analysis of WRKY expression in responses to biotic and abiotic stresses

  • Research Article
  • Published:
Genes & Genomics Aims and scope Submit manuscript

Abstract

As one of the largest transcriptional factor families in plants, WRKY transcription factors play important roles in various biotic and abiotic stress responses. To date, WRKY genes in kiwifruit (Actinidia spp.) remain poorly understood. In our study, o total of 97 AcWRKY genes have been identified in the kiwifruit genome. An overview of these AcWRKY genes is analyzed, including the phylogenetic relationships, exon–intron structures, synteny and expression profiles. The 97 AcWRKY genes were divided into three groups based on the conserved WRKY domain. Synteny analysis indicated that segmental duplication events contributed to the expansion of the kiwifruit AcWRKY family. In addition, the synteny analysis between kiwifruit and Arabidopsis suggested that some of the AcWRKY genes were derived from common ancestors before the divergence of these two species. Conserved motifs outside the AcWRKY domain may reflect their functional conservation. Genome-wide segmental and tandem duplication were found, which may contribute to the expansion of AcWRKY genes. Furthermore, the analysis of selected AcWRKY genes showed a variety of expression patterns in five different organs as well as during biotic and abiotic stresses. The genome-wide identification and characterization of kiwifruit WRKY transcription factors provides insight into the evolutionary history and is a useful resource for further functional analyses of kiwifruit.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488

    Article  CAS  PubMed  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 4:10

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129:706–716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen M, Tan QP, Sun MY, Li DM, Fu XL, Chen XD, Xiao W, Li L, Gao DS (2016) Genome-wide identification of WRKY family genes in peach and analysis of WRKY expression during bud dormancy. Mol Genet Genom 291:1319–1332

    Article  CAS  Google Scholar 

  • Duan YJ, Jiang YZ, Ye SL, Karim A, Ling ZY, He YQ, Yang SQ, Luo KM (2015) PtrWRKY73, a salicylic acid-inducible poplar WRKY transcription factor, is involved in disease resistance in Arabidopsis thaliana. Plant Cell Rep 34:831–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ferradás Y, Rey L, Martínez Ó, Rey M, González MV (2016) Identification and validation of reference genes for accurate normalization of real-time quantitative PCR data in kiwifruit. Plant Physiol Biochem 102:27–36

    Article  PubMed  Google Scholar 

  • Gao M, Zhang HJ, Guo CL, Cheng CX, Guo RR, Mao LY, Fei ZJ, Wang XP (2014) Evolutionary and expression analyses of basic zipper transcription factors in the highly homozygous model grape PN40024 (Vitis vinifera L.). Plant Mol Biol Rep 32:1085–1102

    Article  CAS  Google Scholar 

  • Guo C, Guo R, Xu X, Gao M, Li X, Song J, Wang XP (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 

  • Han Y, Gasic K, Marron B, Beever JE, Korban SS (2007) A BAC-based physical map of the apple genome. Genomics 89:630–637

    Article  CAS  PubMed  Google Scholar 

  • He HS, Dong Q, Shao YH, Jiang HY, Zhu SW, Cheng BJ, 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 

  • Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297

    Article  PubMed  Google Scholar 

  • Hu B, Jin JP, Guo AY, Zhang H, Luo JC, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    Article  PubMed  Google Scholar 

  • Huang HW, Ferguson AR (2007) Actinidia in China: natural diversity, phylogeographical evolution, interspecific gene flow and kiwifruit cultivar improvement. Acta Hortic 753:31–40

    Article  Google Scholar 

  • Huang SX, Gao YF, Liu JK, Peng XL, Niu XL, Fei ZJ, Cao SQ, Liu YS (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Genet Genom 287:495–513

    Article  CAS  Google Scholar 

  • Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P et al (2009) The genome of the cucumber, Cucumis sativus L. Nat Genet 41(12):1275–1281

    Article  CAS  PubMed  Google Scholar 

  • Huang SX, Ding J, Deng DJ, Tang W, Sun HH, Liu DY, Zhang L, Niu XL, Zhang X, Meng M et al (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat commun 4:2640

    PubMed  PubMed Central  Google Scholar 

  • Huang X, Li K, Xu X, Yao Z, Jin C, Zhang S (2015) Genome-wide analysis of WRKY transcription factors in white pear (Pyrus bretschneideri) reveals evolution and patterns under drought stress. BMC Genom 16:1104

    Article  Google Scholar 

  • Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Jing ZB, Yang HB, Yang YW, Shen J, Zhou SM, Xu M (2016) Isolation and identification of Pseudomonas syringae PV. Actinidiae in Northern Area of Qinling Mountains. J Northwest For Univ 31:188–193 (Chinese)

    Google Scholar 

  • Johnso CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359–1375

    Article  Google Scholar 

  • Journot-Catalino N, Somssich IE, Roby D, Kroj T (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18:3289–3302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim KC, Lai ZB, Fan BF, Chen ZX (2008) Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 20:2357–2371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Lagace M, Matton DP (2004) Characterization of a WRKY transcription factor expressed in late torpedo-stage embryos of Solanum chacoense. Planta 219:185–189

    Article  CAS  PubMed  Google Scholar 

  • Lai Z, Vinod K, Zheng Z, Fan B, Chen Z (2008) Roles of Arabidopsis WRKY3 and WRKY4 transcription factors in plant responses to pathogens. BMC Plant Biol 8:68

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee TH, Tang H, Wang X, Paterson AH (2013) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152-D1158

    Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acid Res 40:D302-D305

    Article  Google Scholar 

  • Li JB, Luan YS (2014) Molecular cloning and characterization of a pathogen-induced WRKY transcription factor gene from late blight resistant tomato varieties Solanum pimpinellifolium L3708. Physiol Mol Plant 87:25–31

    Article  CAS  Google Scholar 

  • Li X, Li J, Doejarto DD (2009) Advances in the study of the systematics of Actinidia Lindley. Front Biol China 1:55–61

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Li J, Wang J, Wang NX, Guo XQ, Gao Z (2015) GhWRKY44, a WRKY transcription factor of cotton, mediates defense responses to pathogen infection in transgenic Nicotiana benthamiana. Plant Cell Tissue Organ Cult 121:127–140

    Article  CAS  Google Scholar 

  • Li W, Wang H, Yu D (2016) Arabidopsis WRKY transcription factors WRKY12 and WRKY13 oppositely regulate flowering under short-day conditions. Mol Plant 9:1492–1503

    Article  CAS  PubMed  Google Scholar 

  • Ling J, Jiang WJ, Zhang Y, Yu HJ, Mao ZC, Gu XF, Huang SW, Xie BY (2011) Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genom 12:471

    Article  CAS  Google Scholar 

  • Lippok B, Birkenbihl RP, Rivory G, Brümmer J, Schmelzer E, Logemann E, Somssich IE (2007) Expression of AtWRKY33 encoding a pathogen-or PAMP-responsive WRKY transcription factor is regulated by a composite DNA motif containing W box elements. Mol Plant Microbe Interact 20:420–429

    Article  CAS  PubMed  Google Scholar 

  • Liu XF, Song YZ, Xiang FY, Wang N, Wen FJ, Zhu CX (2016) GhWRKY25, a group I WRKY gene from cotton, confers differential tolerance to abiotic and biotic stresses in transgenic Nicotiana benthamiana. Protoplasma 253:1265–1281

    Article  CAS  PubMed  Google Scholar 

  • Meng D, Li YY, Bai Y, Li MJ, Cheng LL (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 Bioch 103:71–83

    Article  CAS  Google Scholar 

  • Miao Y, Zentgraf U (2007) The antagonist function of Arabidopsis WRKY53 and ESR/ESP in leaf senescence is modulated by the jasmonic and salicylic acid equilibrium. Plant Cell 19:819–830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mzid R, Marchive C, Blancard D, Deluc L, Barrieu F, Corio-Costet MF, Drira N, Hamdi S, Lauvergeat V (2007) Overexpression of VvWRKY2 in tobacco enhances broad resistance to necrotrophic fungal pathogens. Physiol Plant 131:434–447

    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 

  • Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paterson AH, Wang X, Tang H, Lee TH (2012) Synteny and genomic rearrangements. Plant Gen Div 1:195–207

    Google Scholar 

  • Qin YS, Tian YC, Liu XZ (2015) A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana. Biochem Biophys Res Commun 464:428–433

    Article  CAS  PubMed  Google Scholar 

  • Rabara RC, Tripathi P, Lin J, Rushton RJ (2013) Dehydration-induced WRKY genes from tobacco and soybean respond to jasmonic acid treatments in BY-2 cell culture. Biochem Biophys Res Commun 431:409–414

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Song H, Wang P, Hou L, Zhao S, Zhao C, Xia H, Li P, Zhang Y, Bian Wang X (2016) Global analysis of WRKY genes and their response to dehydration and salt stress in soybean. Front Plant Sci 7:9

    PubMed  PubMed Central  Google Scholar 

  • Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang SY (2011) Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Bio 53:212–231

    Article  CAS  Google Scholar 

  • Wang N, Xia EH, Gao LZ (2016a) Genome-wide analysis of WRKY family of transcription factors in common bean, Phaseolus vulgaris: chromosomal localization, structure, evolution and expression divergence. Plant Gene 5:22–30

    Article  CAS  Google Scholar 

  • Wang Y, Shu Z, Wang W, Jiang X, Li D, Pan J, Li X (2016b) CsWRKY2, a novel WRKY gene from Camellia sinensis, is involved in cold and drought stress responses. Biol Plant 60:443–451

    Article  CAS  Google Scholar 

  • Wu ZJ, Li XH, Liu ZW, Li H, Wang YX, Zhuang J (2016) Transcriptome-wide identification of Camellia sinensis WRKY transcription factors in response to temperature stress. Mol Genet Genom 29:255–269

    Article  Google Scholar 

  • Xin PF, Gao CS, Cheng CH, Tang Q, Dong ZX, Zhao LN, Zang GG (2016) Identification and characterization of hemp WRKY transcription factors in response to abiotic stresses. Biol Plantarum 60:489–495

    Article  CAS  Google Scholar 

  • Xiong W, Xu X, Zhang L, Wu P, Chen Y, Li M, Jiang H, Wu G (2013) Genome-wide analysis of the WRKY gene family in physic nut (Jatropha curcas L.). Gene 524:124–132

    Article  CAS  PubMed  Google Scholar 

  • Zhang YC, Mao LY, Wang H, Brocker C, Yin XJ, Vasiliou V, Fei Z, Wangm X (2012) Genome-wide identification and analysis of grape aldehyde dehydrogenase (ALDH) gene superfamily. PLoS ONE 7:e32153

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Zhao ZB, Gao XN, Yang DH, Huang LL, Qin HQ, Kang ZS, Wang NN (2015b) Field detection of canker-causing bacteria on kiwifruit trees: Pseudomonas syringae pv. actinidiae is the major causal agent. Crop Prot 75:55–62

    Article  Google Scholar 

  • Zhao J, Guo RR, Guo CL, Hou HM, Wang XP, Gao H (2016) Evolutionary and expression analyses of the apple basic leucine zipper transcription factor family. Front Plant Sci 7:376

    PubMed  PubMed Central  Google Scholar 

  • Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605

    Article  CAS  PubMed  Google Scholar 

  • Zhou X, Jiang YJ, Yu DQ (2011) WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Mol Cells 31:303–313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zou Z, Yang L, Wang D, Huang Q, Mo Y, Xie G (2016) Gene structures, evolution and transcriptional profiling of the WRKY gene family in castor bean (Ricinus communis L.). PLoS ONE 11(2):e0148243

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the earmarked fund for China Postdoctoral Science Foundation (2015M582712), Postdoctoral Science Foundation of Shaanxi Province (2016BSHYDZZ07), Science and Technology Research and Development Program of Shaanxi Province (2015KTZDNY02-03-01, 2016KJXX-58). We thank AJE (https://www.aje.com/) for editing this manuscript, Chunlei Guo, Li Wang, Jinhua Yang, and Jiao Zhao for teaching data analysis.

Author information

Authors and Affiliations

  1. College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, China

    Zhaobin Jing & Zhande Liu

  2. Weinan Vocational and Technical College, Weinan Fruit Industry Institute, Weinan, 714026, Shaanxi, China

    Zhaobin Jing

Authors
  1. Zhaobin Jing
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhande Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhaobin Jing.

Ethics declarations

Conflict of interest

Zhaobin Jing, Zhande Liu declares that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

13258_2017_645_MOESM1_ESM.tif

The distribution of AcWRKY genes in kiwifruit chromosomes. The number of WRKY genes shown at the top in each chromosome. Thirteen of the 97 AcWRKY could not be mapped to any chromosome and not shown. Supplementary material 1 (TIF 2450 KB)

13258_2017_645_MOESM2_ESM.tif

Expression profiles of ten AcWRKY genes under salt, drought and Psa treatments analyzed using semi-quantitative PCR. Supplementary material 2 (TIF 4886 KB)

13258_2017_645_MOESM3_ESM.tif

Expression profiles of ten AcWRKY genes under hormone treatments analyzed using semi-quantitative PCR. (Ethylene-Eth; methyl jasmonic acid-MeJA; abscisic acid-ABA; gibberellins-GA; salisylic acid-SA). Supplementary material 3 (TIF 4622 KB)

Supplementary material 4 (XLS 32 KB)

Supplementary material 5 (DOCX 16 KB)

Supplementary material 6 (DOCX 18 KB)

Supplementary material 7 (XLSX 14 KB)

Supplementary material 8 (XLSX 12 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jing, Z., Liu, Z. Genome-wide identification of WRKY transcription factors in kiwifruit (Actinidia spp.) and analysis of WRKY expression in responses to biotic and abiotic stresses. Genes Genom 40, 429–446 (2018). https://doi.org/10.1007/s13258-017-0645-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-017-0645-1

Keywords

Search

Navigation