Molecular Genetics and Genomics

, Volume 289, Issue 6, pp 1103–1121 | Cite as

Genome-wide analysis of the WRKY gene family in cotton

  • Lingling Dou
  • Xiaohong Zhang
  • Chaoyou Pang
  • Meizhen Song
  • Hengling Wei
  • Shuli Fan
  • Shuxun YuEmail author
Original Paper


WRKY proteins are major transcription factors involved in regulating plant growth and development. Although many studies have focused on the functional identification of WRKY genes, our knowledge concerning many areas of WRKY gene biology is limited. For example, in cotton, the phylogenetic characteristics, global expression patterns, molecular mechanisms regulating expression, and target genes/pathways of WRKY genes are poorly characterized. Therefore, in this study, we present a genome-wide analysis of the WRKY gene family in cotton (Gossypium raimondii and Gossypium hirsutum). We identified 116 WRKY genes in G. raimondii from the completed genome sequence, and we cloned 102 WRKY genes in G. hirsutum. Chromosomal location analysis indicated that WRKY genes in G. raimondii evolved mainly from segmental duplication followed by tandem amplifications. Phylogenetic analysis of alga, bryophyte, lycophyta, monocot and eudicot WRKY domains revealed family member expansion with increasing complexity of the plant body. Microarray, expression profiling and qRT-PCR data revealed that WRKY genes in G. hirsutum may regulate the development of fibers, anthers, tissues (roots, stems, leaves and embryos), and are involved in the response to stresses. Expression analysis showed that most group II and III GhWRKY genes are highly expressed under diverse stresses. Group I members, representing the ancestral form, seem to be insensitive to abiotic stress, with low expression divergence. Our results indicate that cotton WRKY genes might have evolved by adaptive duplication, leading to sensitivity to diverse stresses. This study provides fundamental information to inform further analysis and understanding of WRKY gene functions in cotton species.


WRKY transcription factor Cotton Expression profile Development 



We thanks for the National Basic Research Program of China (Grant No. 2010CB126006) and the China Agriculture Research System (Grant No. CARS-18) providing the financial support for this project. We are grateful to the researchers who submitted the microarray data to the public expression databases. We are also grateful to all of the members of our laboratories who completed the expression profiling. We also thanks for EVans Ondati to help us revise the language.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

438_2014_872_MOESM1_ESM.tif (115.7 mb)
Supplementary material 1 (TIFF 118435 kb) Phylogenetic relationships between all species investigated in this study. The tree was constructed by the simplified phylogeny of species investigated in this study. The total number of WRKY proteins found in each species is indicated on the right of each species
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Supplementary material 2 (XLSX 19 kb)
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Supplementary material 6 (XLSX 10 kb)


  1. Alexandrova KS, Conger BV (2002) Isolation of two somatic embryogenesis-related genes from orchardgrass (Dactylis glomerata). Plant Sci 162(2):301–307. doi: 10.1016/S0168-9452(01)00571-4 CrossRefGoogle Scholar
  2. Alkan C, Coe BP, Eichler EE (2011) Applications of next-generation sequencing genome structural variation discovery and genotyping. Nat Rev Genet 12(5):363–375. doi: 10.1038/Nrg2958 PubMedCentralPubMedCrossRefGoogle Scholar
  3. Besseau S, Li J, Palva ET (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J Exp Bot 63(7):2667–2679. doi: 10.1093/Jxb/Err450 PubMedCentralPubMedCrossRefGoogle Scholar
  4. Brand LH, Fischer NM, Harter K, Kohlbacher O, Wanke D (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res 41(21):9764–9778. doi: 10.1093/nar/gkt732 PubMedCentralPubMedCrossRefGoogle Scholar
  5. Cai CP, Niu E, Du H, Zhao L, Feng Y, Guo WZ (2014) Genome-wide analysis of the WRKY transcription factor gene family in Gossypium raimondii and the expression of orthologs in cultivated tetraploid. Crop J 3. doi: 10.1016/j.cj.2014.03.001
  6. 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). doi: 10.1186/1471-2229-4-10
  7. Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW (2010) Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.). Plant Cell Physiol 51(1):21–37. doi: 10.1093/Pcp/Pcp163 PubMedCrossRefGoogle Scholar
  8. Cottee NS, Wilson IW, Tan DKY, Bange MP (2014) Understanding the molecular events underpinning cultivar differences in the physiological performance and heat tolerance of cotton (Gossypium hirsutum). Funct Plant Biol 41(1):56–67. doi: 10.1071/Fp13140 CrossRefGoogle Scholar
  9. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5(5):199–206. doi: 10.10/S1360-1385(00)01600-9 PubMedCrossRefGoogle Scholar
  10. Gou JY, Wang LJ, Chen SP, Hu WL, Chen XY (2007) Gene expression and metabolite profiles of cotton fiber during cell elongation and secondary cell wall synthesis. Cell Res 17(5):422–434. doi: 10.1038/ PubMedGoogle Scholar
  11. Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148(1):358–368. doi: 10.1104/pp.108.119131 PubMedCentralPubMedCrossRefGoogle Scholar
  12. Guo RY, Yu FF, Gao Z, An HL, Cao XC, Guo XQ (2011) GhWRKY3, a novel cotton (Gossypium hirsutum L.) WRKY gene, is involved in diverse stress responses. Mol Biol Rep 38(1):49–58. doi: 10.1007/s11033-010-0076-4 PubMedCrossRefGoogle Scholar
  13. Hara K, Yagi M, Kusano T, Sano H (2000) Rapid systemic accumulation of transcripts encoding a tobacco WRKY transcription factor upon wounding. Mol Gen Genet 263(1):30–37. doi: 10.1007/Pl00008673 PubMedCrossRefGoogle Scholar
  14. 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(7):1199–1217. doi: 10.1007/s00299-012-1241-0 PubMedCrossRefGoogle Scholar
  15. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5 (11). doi: 10.1186/Gb-2004-5-11-R85
  16. Hou XJ, Liu SR, Khan MRG, Hu CG, Zhang JZ (2014) Genome-wide identification, classification, expression profiling, and SSR marker development of the MADS-box gene family in citrus. Plant Mol Biol Rep 32(1):28–41. doi: 10.1007/s11105-013-0597-9 CrossRefGoogle Scholar
  17. Hu G, Koh J, Yoo MJ, Grupp K, Chen S, Wendel JF (2013) Proteomic profiling of developing cotton fibers from wild and domesticated Gossypium barbadense. New Phytol 200(2):570–582. doi: 10.1111/nph.12381 PubMedCrossRefGoogle Scholar
  18. Huang T, Duman JG (2002) Cloning and characterization of a thermal hysteresis (antifreeze) protein with DNA-binding activity from winter bittersweet nightshade, Solanum dulcamara. Plant Mol Biol 48(4):339–350. doi: 10.1023/A:1014062714786 PubMedCrossRefGoogle Scholar
  19. Ishida T, Hattori S, Sano R, Inoue K, Shirano Y, Hayashi H, Shibata D, Sato S, Kato T, Tabata S, Okada K, Wada T (2007) Arabidopsis TRANSPARENT TESTA GLABRA2 is directly regulated by R2R3 MYB transcription factors and is involved in regulation of GLABRA2 transcription in epidermal differentiation. Plant Cell 19(8):2531–2543. doi: 10.1105/tpc.107.052274 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Ishiguro S, Nakamura K (1994) Characterization of a cDNA encoding a novel DNA-binding protein, SPF1, that recognizes SP8 sequences in the 5′ upstream regions of genes coding for sporamin and beta-amylase from sweet potato. Mol Gen Genet 244(6):563–571. doi: 10.1007/BF00282746 PubMedCrossRefGoogle Scholar
  21. Johnson 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(6):1359–1375. doi: 10.1105/Tpc.001404 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Kantety RV, La Rota M, Matthews DE, Sorrells ME (2002) Data mining for simple sequence repeats in expressed sequence tags from barley, maize, rice, sorghum and wheat. Plant Mol Biol 48(5):501–510. doi: 10.1023/A:1014875206165 PubMedCrossRefGoogle Scholar
  23. Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genomics 285(3):245–260. doi: 10.1007/s00438-011-0602-7 PubMedCrossRefGoogle Scholar
  24. Lai DY, Li HZ, Fan SL, Song MZ, Pang CY, Wei HL, Liu JJ, Wu D, Gong WF, Yu SX (2011) Generation of ESTs for flowering gene discovery and SSR marker development in upland cotton. PLoS ONE 6 (12). doi: 10.1371/journal.pone.0028676
  25. Li HL, Zhang LB, Guo D, Li CZ, Peng SQ (2012) Identification and expression profiles of the WRKY transcription factor family in Ricinus communis. Gene 503(2):248–253. doi: 10.1016/j.gene.2012.04.069 PubMedCrossRefGoogle Scholar
  26. 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 Genomics 12. doi: 10.1186/1471-2164-12-471
  27. Lippok B, Birkenbihl RP, Rivory G, Brummer J, Schmelzer E, Logemann E, Somissich 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 In 20(4):420–429. doi: 10.1094/Mpmi-20-4-0420 CrossRefGoogle Scholar
  28. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. doi: 10.1006/meth.2001.1262 PubMedCrossRefGoogle Scholar
  29. Ma JH, Wei HL, Song MZ, Pang CY, Liu J, Wang L, Zhang JF, Fan SL, Yu SX (2012) Transcriptome Profiling Analysis Reveals That Flavonoid and Ascorbate-Glutathione Cycle Are Important during Anther Development in Upland Cotton. PLoS ONE 7 (11). doi: 10.1371/journal.pone.0049244
  30. Ma JH, Wei HL, Liu J, Song MZ, Pang CY, Wang L, Zhang WX, Fan SL, Yu SX (2013) Selection and characterization of a novel photoperiod-sensitive male sterile line in upland cotton. J Integr Plant Biol 55(7):608–618. doi: 10.1111/Jipb.12067 PubMedCrossRefGoogle Scholar
  31. Matsuzaki M, Misumi O, Shin-I T, Maruyama S, Takahara M, Miyagishima SY, Mori T, Nishida K, Yagisawa F, Nishida K, Yoshida Y, Nishimura Y, Nakao S, Kobayashi T, Momoyama Y, Higashiyama T, Minoda A, Sano M, Nomoto H, Oishi K, Hayashi H, Ohta F, Nishizaka S, Haga S, Miura S, Morishita T, Kabeya Y, Terasawa K, Suzuki Y, Ishii Y, Asakawa S, Takano H, Ohta N, Kuroiwa H, Tanaka K, Shimizu N, Sugano S, Sato N, Nozaki H, Ogasawara N, Kohara Y, Kuroiwa T (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428(6983):653–657. doi: 10.1038/Nature02398 PubMedCrossRefGoogle Scholar
  32. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15(4):809–834. doi: 10.1102/Tpc.009308 PubMedCentralPubMedCrossRefGoogle Scholar
  33. Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55(6):853–867. doi: 10.1007/s11103-004-2142-6 PubMedCrossRefGoogle Scholar
  34. Nagata T, Hara H, Saitou K, Kobashi A, Kojima K, Yuasa T, Ueno O (2012) Activation of ADP-Glucose Pyrophosphorylase Gene Promoters by a WRKY Transcription Factor, AtWRKY20, in Arabidopsis thaliana L. and Sweet Potato (Ipomoea batatas Lam.). Plant Prod Sci 15(1):10–18CrossRefGoogle Scholar
  35. Nigam D, Sawant SV (2013) Identification and Analyses of AUX-IAA target genes controlling multiple pathways in developing fiber cells of Gossypium hirsutum L. Bioinformation 9(20):996–1002. doi: 10.6026/97320630009996 PubMedCentralPubMedCrossRefGoogle Scholar
  36. Padmalatha KV, Dhandapani G, Kanakachari M, Kumar S, Dass A, Patil DP, Rajamani V, Kumar K, Pathak R, Rawat B, Leelavathi S, Reddy PS, Jain N, Powar KN, Hiremath V, Katageri IS, Reddy MK, Solanke AU, Reddy VS, Kumar PA (2012) Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes. Plant Mol Biol 78(3):223–246. doi: 10.1007/s11103-011-9857-y PubMedCrossRefGoogle Scholar
  37. Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin DC, Llewellyn D, Showmaker KC, Shu SQ, Udall J, Yoo MJ, Byers R, Chen W, Doron-Faigenboim A, Duke MV, Gong L, Grimwood J, Grover C, Grupp K, Hu GJ, Lee TH, Li JP, Lin LF, Liu T, Marler BS, Page JT, Roberts AW, Romanel E, Sanders WS, Szadkowski E, Tan X, Tang HB, Xu CM, Wang JP, Wang ZN, Zhang D, Zhang L, Ashrafi H, Bedon F, Bowers JE, Brubaker CL, Chee PW, Das S, Gingle AR, Haigler CH, Harker D, Hoffmann LV, Hovav R, Jones DC, Lemke C, Mansoor S, Rahman MU, Rainville LN, Rambani A, Reddy UK, Rong JK, Saranga Y, Scheffler BE, Scheffler JA, Stelly DM, Triplett BA, Van Deynze A, Vaslin MFS, Waghmare VN, Walford SA, Wright RJ, Zaki EA, Zhang TZ, Dennis ES, Mayer KFX, Peterson DG, Rokhsar DS, Wang XY, Schmutz J (2012) Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature 492:423–427. doi: 10.1038/Nature11798 PubMedCrossRefGoogle Scholar
  38. Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. Plant J 31(3):319–330. doi: 10.1046/j.1365-313X.2002.01364.x PubMedCrossRefGoogle Scholar
  39. 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 Physiol 49(6):865–879. doi: 10.1093/Pcp/Pcn061 PubMedCrossRefGoogle Scholar
  40. Reik W, Walter J (2001) Genomic imprinting: parental influence on the genome. Nat Rev Genet 2(1):21–32. doi: 10.1038/35047554 PubMedCrossRefGoogle Scholar
  41. Rizhsky L, Davletova S, Liang HJ, Mittler R (2004) The zinc finger protein Zat12 is required for cytosolic ascorbate peroxidase 1 expression during oxidative stress in Arabidopsis. J Biol Chem 279(12):11736–11743. doi: 10.1074/jbc.M313350200 PubMedCrossRefGoogle Scholar
  42. Rizzon C, Ponger L, Gaut BS (2006) Striking similarities in the genomic distribution of tandemly arrayed genes in Arabidopsis and rice. PLoS Comput Biol 2(9):989–1000. doi: 10.1371/Journal.Pcbi.0020115 CrossRefGoogle Scholar
  43. Ross CA, Liu Y, Shen QXJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49(6):827–842. doi: 10.1111/j.1744-7909.2007.00504.x CrossRefGoogle Scholar
  44. Schauser L, Wieloch W, Stougaard J (2005) Evolution of NIN-Like proteins in Arabidopsis, rice, and Lotus japonicus. J Mol Evol 60(2):229–237. doi: 10.1007/s00239-004-0144-2 PubMedCrossRefGoogle Scholar
  45. Senchina DS, Alvarez I, Cronn RC, Liu B, Rong JK, Noyes RD, Paterson AH, Wing RA, Wilkins TA, Wendel JF (2003) Rate variation among nuclear genes and the age of polyploidy in Gossypium. Mol Biol Evol 20(4):633–643. doi: 10.1093/molbev/msg065 PubMedCrossRefGoogle Scholar
  46. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, Seki H, Ulker B, Somssich IE, Schulze-Lefert P (2007) Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315(5815):1098–1103. doi: 10.1126/science.1136372 PubMedCrossRefGoogle Scholar
  47. Soltis DE, Soltis PS, Tate JA (2004) Advances in the study of polyploidy since Plant speciation. New Phytol 161(1):173–191. doi: 10.1046/j.1469-8137.2003.00948.x CrossRefGoogle Scholar
  48. Song Y, Gao J (2014) Genome-wide analysis of WRKY gene family in Arabidopsis lyrata and comparison with Arabidopsis thaliana and Populus trichocarpa. Chin Sci Bull 59(8):754–765. doi: 10.1007/s11434-013-0057-9 CrossRefGoogle Scholar
  49. Sunilkumar G, Campbell LM, Puckhaber L, Stipanovic RD, Rathore KS (2006) Engineering cottonseed for use in human nutrition by tissue-specific reduction of toxic gossypol. P Natl Acad Sci USA 103(48):18054–18059. doi: 10.1073/pnas.0605389103 CrossRefGoogle Scholar
  50. Tang J, Wang F, Wang Z, Huang ZN, Xiong AS, Hou XL (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. doi: 10.1186/1471-2229-13-188
  51. Tu LL, Zhang XL, Liu DQ, Jin SX, Cao JL, Zhu LF, Deng FL, Tan JF, Zhang CB (2007) Suitable internal control genes for qRT-PCR normalization in cotton fiber development and somatic embryogenesis. Chin Sci Bull 52(22):3110–3117. doi: 10.1007/s11434-007-0461-0 CrossRefGoogle Scholar
  52. Wang KB, Wang ZW, Li FG, Ye WW, Wang JY, Song GL, Yue Z, Cong L, Shang HH, Zhu SL, Zou CS, Li Q, Yuan YL, Lu CR, Wei HL, Gou CY, Zheng ZQ, Yin Y, Zhang XY, Liu K, Wang B, Song C, Shi N, Kohel RJ, Percy RG, Yu JZ, Zhu YX, Wang J, Yu SX (2012) The draft genome of a diploid cotton Gossypium raimondii. Nat Genet 44(10):1098–1103. doi: 10.1038/Ng.2371 PubMedCrossRefGoogle Scholar
  53. Wang X, Yan Y, Li Y, Chu X, Wu C, Guo X (2014) GhWRKY40, a Multiple Stress-Responsive Cotton WRKY Gene, Plays an Important Role in the Wounding Response and Enhances Susceptibility to Ralstonia solanacearum Infection in Transgenic Nicotiana benthamiana. PLoS ONE 9 (4). doi: 10.1371/journal.pone.0093577
  54. 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(2):153–164. doi: 10.1093/dnares/dsr048 PubMedCentralPubMedCrossRefGoogle Scholar
  55. Woo HR, Kim JH, Kim J, Kim J, Lee U, Song IJ, Kim JH, Lee HY, Nam HG, Lim PO (2010) The RAV1 transcription factor positively regulates leaf senescence in Arabidopsis. J Exp Bot 61(14):3947–3957. doi: 10.1093/Jxb/Erq206 PubMedCentralPubMedCrossRefGoogle Scholar
  56. Xu GX, Ma H, Nei M, Kong HZ (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. P Natl Acad Sci USA 106(3):835–840. doi: 10.1073/pnas.0812043106 CrossRefGoogle Scholar
  57. Xu L, Jin L, Long L, Liu LL, He X, Gao W, Zhu LF, Zhang XL (2012) Overexpression of GbWRKY1 positively regulates the Pi starvation response by alteration of auxin sensitivity in Arabidopsis. Plant Cell Rep 31(12):2177–2188. doi: 10.1007/s00299-012-1328-7 PubMedCrossRefGoogle Scholar
  58. Yang PZ, Chen ZX (2001) A family of dispersed repetitive DNA sequences in tobacco contain clusters of W-box elements recognized by pathogen-induced WRKY DNA-binding proteins. Plant Sci 161(4):655–664. doi: 10.1016/S0168-9452(01)00454-X CrossRefGoogle Scholar
  59. Yang B, Jiang YQ, Rahman MH, Deyholos MK, Kav NNV (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9. doi: 10.1186/1471-2229-9-68
  60. Yu FF, Huaxia YF, Lu WJ, Wu CG, Cao XC, Guo XQ (2012) GhWRKY15, a member of the WRKY transcription factor family identified from cotton (Gossypium hirsutum L.), is involved in disease resistance and plant development. BMC Plant Biol 12. doi: 10.1186/1471-2229-12-144
  61. Zhang LQ, Gaut BS (2003) Does recombination shape the distribution and evolution of tandemly arrayed genes (TAGs) in the Arabidopsis thaliana genome? Genome Res 13(12):2533–2540. doi: 10.1101/Gr.1318503 PubMedCentralPubMedCrossRefGoogle Scholar
  62. Zhang YJ, Wang LJ (2005) The WRKY transcription factor superfamily: its origin in eukaryotes and expansion in plants. BMC Evol Biol 5(1):1. doi: 10.1186/1471-2148-5-1 PubMedCentralPubMedCrossRefGoogle Scholar
  63. Zhang ZL, Xie Z, Zou XL, Casaretto J, Ho THD, Shen QXJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134(4):1500–1513. doi: 10.1104/pp.103.034967 PubMedCentralPubMedCrossRefGoogle Scholar
  64. Zheng ZY, Abu Qamar S, Chen ZX, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48(4):592–605. doi: 10.1111/j.1365-313X.2006.02901.x PubMedCrossRefGoogle Scholar
  65. Zhu YN, Shi DQ, Ruan MB, Zhang LL, Meng ZH, Liu J, Yang WC (2013) Transcriptome Analysis Reveals Crosstalk of Responsive Genes to Multiple Abiotic Stresses in Cotton (Gossypium hirsutum L.). PLoS ONE 8 (11). doi: 10.1371/journal.pone.0080218

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Lingling Dou
    • 1
    • 2
  • Xiaohong Zhang
    • 1
    • 2
  • Chaoyou Pang
    • 2
  • Meizhen Song
    • 2
  • Hengling Wei
    • 2
  • Shuli Fan
    • 2
  • Shuxun Yu
    • 1
    • 2
    Email author
  1. 1.College of AgronomyNorthwest A&F UniversityYanglingPeople’s Republic of China
  2. 2.State Key Laboratory in Cotton Biology, Cotton Research InstituteP. R. Chinese Academy of Agriculture Sciences (CAAS)AnyangPeople’s Republic of China

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