Genes & Genomics

, Volume 40, Issue 4, pp 429–446 | Cite as

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

  • Zhaobin Jing
  • Zhande Liu
Research Article


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.


Abiotic and biotic stress Evolution Expression profile Kiwifruit Phylogenetic analysis WRKY genes 



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 ( for editing this manuscript, Chunlei Guo, Li Wang, Jinhua Yang, and Jiao Zhao for teaching data analysis.

Compliance with ethical standards

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.

Supplementary material

13258_2017_645_MOESM1_ESM.tif (2.4 mb)
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 (4.8 mb)
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 (4.5 mb)
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)
13258_2017_645_MOESM4_ESM.xls (32 kb)
Supplementary material 4 (XLS 32 KB)
13258_2017_645_MOESM5_ESM.docx (17 kb)
Supplementary material 5 (DOCX 16 KB)
13258_2017_645_MOESM6_ESM.docx (19 kb)
Supplementary material 6 (DOCX 18 KB)
13258_2017_645_MOESM7_ESM.xlsx (15 kb)
Supplementary material 7 (XLSX 14 KB)
13258_2017_645_MOESM8_ESM.xlsx (13 kb)
Supplementary material 8 (XLSX 12 KB)


  1. Bari R, Jones JD (2009) Role of plant hormones in plant defence responses. Plant Mol Biol 69:473–488CrossRefPubMedGoogle 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 4:10CrossRefPubMedPubMedCentralGoogle Scholar
  3. Chen C, Chen Z (2002) Potentiation of developmentally regulated plant defense response by AtWRKY18, a pathogen-induced Arabidopsis transcription factor. Plant Physiol 129:706–716CrossRefPubMedPubMedCentralGoogle Scholar
  4. 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 291:1319–1332CrossRefGoogle Scholar
  5. 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 34:831–841CrossRefPubMedPubMedCentralGoogle Scholar
  6. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206CrossRefPubMedGoogle Scholar
  7. 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 102:27–36CrossRefPubMedGoogle Scholar
  8. 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 32:1085–1102CrossRefGoogle Scholar
  9. 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 65:1513–1528CrossRefPubMedPubMedCentralGoogle Scholar
  10. Han Y, Gasic K, Marron B, Beever JE, Korban SS (2007) A BAC-based physical map of the apple genome. Genomics 89:630–637CrossRefPubMedGoogle Scholar
  11. 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 31:1199–1217CrossRefPubMedGoogle Scholar
  12. Hu Y, Dong Q, Yu D (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297CrossRefPubMedGoogle Scholar
  13. Hu B, Jin JP, Guo AY, Zhang H, Luo JC, Gao G (2015) GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297CrossRefPubMedGoogle Scholar
  14. Huang HW, Ferguson AR (2007) Actinidia in China: natural diversity, phylogeographical evolution, interspecific gene flow and kiwifruit cultivar improvement. Acta Hortic 753:31–40CrossRefGoogle Scholar
  15. 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 287:495–513CrossRefGoogle Scholar
  16. 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):1275–1281CrossRefPubMedGoogle Scholar
  17. 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 4:2640PubMedPubMedCentralGoogle Scholar
  18. 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 16:1104CrossRefGoogle Scholar
  19. 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 449:463–467CrossRefPubMedGoogle Scholar
  20. 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
  21. 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 14:1359–1375CrossRefGoogle Scholar
  22. 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 18:3289–3302CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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 20:2357–2371CrossRefPubMedPubMedCentralGoogle Scholar
  24. Koonin EV (2005) Orthologs, paralogs, and evolutionary genomics. Annu Rev Genet 39:309–338CrossRefPubMedGoogle Scholar
  25. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefPubMedGoogle Scholar
  26. Lagace M, Matton DP (2004) Characterization of a WRKY transcription factor expressed in late torpedo-stage embryos of Solanum chacoense. Planta 219:185–189CrossRefPubMedGoogle Scholar
  27. 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 8:68CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lee TH, Tang H, Wang X, Paterson AH (2013) PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res 41:D1152-D1158Google Scholar
  29. Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acid Res 40:D302-D305CrossRefGoogle Scholar
  30. 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 87:25–31CrossRefGoogle Scholar
  31. Li X, Li J, Doejarto DD (2009) Advances in the study of the systematics of Actinidia Lindley. Front Biol China 1:55–61CrossRefGoogle Scholar
  32. 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 70:207–216CrossRefGoogle Scholar
  33. 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 121:127–140CrossRefGoogle Scholar
  34. Li W, Wang H, Yu D (2016) Arabidopsis WRKY transcription factors WRKY12 and WRKY13 oppositely regulate flowering under short-day conditions. Mol Plant 9:1492–1503CrossRefPubMedGoogle Scholar
  35. 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 12:471CrossRefGoogle Scholar
  36. 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 20:420–429CrossRefPubMedGoogle Scholar
  37. 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 253:1265–1281CrossRefPubMedGoogle Scholar
  38. 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 103:71–83CrossRefGoogle Scholar
  39. 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 19:819–830CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 131:434–447CrossRefPubMedGoogle Scholar
  41. 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 146:333–350CrossRefPubMedPubMedCentralGoogle Scholar
  42. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655CrossRefPubMedPubMedCentralGoogle Scholar
  43. Paterson AH, Wang X, Tang H, Lee TH (2012) Synteny and genomic rearrangements. Plant Gen Div 1:195–207Google Scholar
  44. 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 464:428–433CrossRefPubMedGoogle Scholar
  45. 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 431:409–414CrossRefPubMedGoogle Scholar
  46. Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842CrossRefGoogle Scholar
  47. 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 7:9PubMedPubMedCentralGoogle Scholar
  48. 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 53:212–231CrossRefGoogle Scholar
  49. 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 5:22–30CrossRefGoogle Scholar
  50. 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 60:443–451CrossRefGoogle Scholar
  51. 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 29:255–269CrossRefGoogle Scholar
  52. 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 60:489–495CrossRefGoogle Scholar
  53. 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 524:124–132CrossRefPubMedGoogle Scholar
  54. 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:e32153CrossRefPubMedPubMedCentralGoogle Scholar
  55. 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 565:130–139CrossRefPubMedGoogle Scholar
  56. 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 75:55–62CrossRefGoogle Scholar
  57. 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 7:376PubMedPubMedCentralGoogle Scholar
  58. Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605CrossRefPubMedGoogle Scholar
  59. Zhou X, Jiang YJ, Yu DQ (2011) WRKY22 transcription factor mediates dark-induced leaf senescence in Arabidopsis. Mol Cells 31:303–313CrossRefPubMedPubMedCentralGoogle Scholar
  60. 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):e0148243CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.College of HorticultureNorthwest A&F UniversityYanglingChina
  2. 2.Weinan Vocational and Technical CollegeWeinan Fruit Industry InstituteWeinanChina

Personalised recommendations