Skip to main content
SpringerLink
Log in

ABA signaling is negatively regulated by GbWRKY1 through JAZ1 and ABI1 to affect salt and drought tolerance

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

GbWRKY1 can function as a negative regulator of ABA signaling via JAZ1 and ABI1, with effects on salt and drought tolerance.

Abstract

WRKY transcription factors play important roles in plant development and stress responses. GbWRKY1 was initially identified as a defense-related gene in cotton and negatively regulates the response to fungal pathogens by activating the expression of JAZ1. Here, we characterized the role of GbWRKY1, an orthologue of the Arabidopsis gene AtWRKY75, in abiotic stress (salt and drought) and established novel connection between JAZ1 and ABA signaling in Arabidopsis. GbWRKY1 is nucleus localized and its expression is significantly induced by treatment with ABA and osmotic stresses NaCl and PEG. Increased levels of expression of GbWRKY1 in transgenic Arabidopsis enhance sensitivity to salt and drought as revealed by seed germination tests and soil stress experiments. Similarly, GbWRKY1 overexpression cotton plants also display increased sensitivity to PEG treatment and drought. Expression analysis shows that the induction of two ABA responsive genes, RAB18 and RD29A by NaCl, mannitol, and ABA treatment is significantly impaired in GbWRKY1 overexpression Arabidopsis lines. GbWRKY1 overexpression Arabidopsis displays a strong ABA-insensitive phenotype at both germination and early stages of seedling development. Further genetic evidence suggested that the ABA-insensitive phenotype of GbWRKY1 overexpression Arabidopsis was dependent on JAZ1, and overexpression of JAZ1 also displayed an ABA-insensitive phenotype. In addition, yeast two hybrid and bimolecular fluorescence complementation assays showed that JAZ1 directly interacts with ABI1, a key negative regulator of ABA signaling. We, therefore, demonstrate that GbWRKY1 acts as a negative regulator of ABA signaling, through an interaction network involving JAZ1 and ABI1, to regulate salt and drought tolerance.

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

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aleman F, Yazaki J, Lee M, Takahashi Y, Kim AY, Li ZX et al (2016) An ABA-increased interaction of the PYL6 ABA receptor with MYC2 transcription factor: a putative link of ABA and JA signaling. Sci Rep 6:28941

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58

    CAS  Google Scholar 

  • Chen X, Yan D, Sun L, Zeng R, Yang L (2016) Cloning and expression analysis of HbWRKY75 gene in leaf from Hevea brasiliensis. Plant Physiol J 52:250–258

    Google Scholar 

  • Dave A, Hernandez ML, He ZS, Andriotis VME, Vaistij FE, Larson TR, Graham IA (2011) 12-Oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis. Plant Cell 23:583–599

    CAS  PubMed  PubMed Central  Google Scholar 

  • de Ollas C, Arbona V, Gomez-Cadenas A (2015) Jasmonoyl isoleucine accumulation is needed for abscisic acid build-up in roots of Arabidopsis under water stress conditions. Plant Cell Environ 38:2157–2170

    PubMed  Google Scholar 

  • Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ellis C, Turner JG (2002) A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta 215:549–556

    CAS  PubMed  Google Scholar 

  • Fernandez-Arbaizar A, Regalado JJ, Lorenzo O (2012) Isolation and characterization of novel mutant loci suppressing the ABA hypersensitivity of the Arabidopsis Coronatine insensitive 1–16 (coi1-16) mutant during germination and seedling growth. Plant Cell Physiol 53:53–63

    CAS  PubMed  Google Scholar 

  • Golldack D, Luking I, Yang O (2011) Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network. Plant Cell Rep 30:1383–1391

    CAS  PubMed  Google Scholar 

  • Guo PR, Li ZH, Huang PX, Li BS, Fang S, Chu JF, Guo HW (2017) A tripartite amplification loop involving the transcription factor WRKY75, Salicylic Acid, and reactive oxygen species accelerates leaf senescence. Plant Cell 29:2854–2870

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hecker A, Wallmeroth N, Peter S, Blatt MR, Harter K, Grefen C (2015) Binary 2in1 vectors improve in planta (co)localization and dynamic protein interaction studies. Plant Physiol 168:776–787

    PubMed  PubMed Central  Google Scholar 

  • Hossain MA, Henriquez-Valencia C, Gomez-Paez M, Medina J, Orellana A, Vicente-Carbajosa J, Zouhar J (2016) Identification of novel components of the unfolded protein response in Arabidopsis. Front Plant Sci 7:650

    PubMed  PubMed Central  Google Scholar 

  • Jiang JJ, Ma SH, Ye NH, Jiang M, Cao JS, Zhang JH (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59:86–101

    CAS  PubMed  Google Scholar 

  • Ju L, Jing Y, Shi P, Liu J, Chen J, Yan J et al (2019) JAZ proteins modulate seed germination through interaction with ABI5 in bread wheat and Arabidopsis. New Phytol 223:246–260

    CAS  PubMed  Google Scholar 

  • Kazan K, Manners JM (2012) JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 17:22–31

    CAS  PubMed  Google Scholar 

  • Lackman P, Gonzalez-Guzman M, Tilleman S, Carqueijeiro I, Perez AC, Moses T et al (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci USA 108:5891–5896

    CAS  PubMed  Google Scholar 

  • Li C, He X, Luo XY, Xu L, Liu LL, Min L et al (2014) Cotton WRKY1 Mediates the plant defense-to-development transition during infection of cotton by Verticillium dahliae by activating JASMONATE ZIM-DOMAIN1 expression. Plant Physiol 166:2179–2194

    PubMed  PubMed Central  Google Scholar 

  • Liu H, Ding YD, Zhou YQ, Jin WQ, Xie KB, Chen LL (2017) CRISPR-P 2.0: an improved CRISPR-Cas9 tool for genome editing in plants. Mol Plant 10:530–532

    CAS  PubMed  Google Scholar 

  • Liu Q, Wang C, Jiao XZ, Zhang HW, Song LL, Li YX et al (2019) Hi-TOM: a platform for high-throughput tracking of mutations induced by CRISPR/Cas systems. Sci China Life Sci 62:1–7

    PubMed  Google Scholar 

  • Long L, Yang WW, Liao P, Guo YW, Kumar A, Gao W (2019) Transcriptome analysis reveals differentially expressed ERF transcription factors associated with salt response in cotton. Plant Sci 281:72–81

    CAS  PubMed  Google Scholar 

  • Luo X, Bai X, Sun XL, Zhu D, Liu BH, Ji W et al (2013) Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. J Exp Bot 64:2155–2169

    CAS  PubMed  Google Scholar 

  • Meyer K, Leube MP, Grill E (1994) A Protein Phosphatase 2C involved in ABA signal-transduction in Arabidopsis thaliana. Science 264:1452–1455

    CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970

    CAS  PubMed  Google Scholar 

  • Ou B, Yin KQ, Liu SN, Yang Y, Gu T, Hui JMW et al (2011) A high-throughput screening system for arabidopsis transcription factors and its application to Med25-dependent transcriptional regulation. Mol Plant 4:546–555

    CAS  PubMed  Google Scholar 

  • Parihar P, Singh S, Singh R, Singh VP, Prasad SM (2015) Effect of salinity stress on plants and its tolerance strategies: a review. Environ Sci Pollut R 22:4056–4075

    CAS  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL Family of START proteins. Science 324:1068–1071

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    CAS  PubMed  Google Scholar 

  • Ranjan A, Sawant S (2015) Genome-wide transcriptomic comparison of cotton (Gossypium herbaceum) leaf and root under drought stress. 3 Biotech 5:585–596

    PubMed  Google Scholar 

  • Ranjan A, Pandey N, Lakhwani D, Dubey NK, Pathre UV, Sawant SV (2012) Comparative transcriptomic analysis of roots of contrasting Gossypium herbaceum genotypes revealing adaptation to drought. BMC Genom 13:680

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Sah SK, Reddy KR, Li JX (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571

    PubMed  PubMed Central  Google Scholar 

  • Shao HB, Wang HY, Tang XL (2015) NAC transcription factors in plant multiple abiotic stress responses: progress and prospects. Front Plant Sci 6:902

    PubMed  PubMed Central  Google Scholar 

  • Shi WN, Hao LL, Li J, Liu DD, Guo XQ, Li H (2014) The Gossypium hirsutum WRKY gene GhWRKY39-1 promotes pathogen infection defense responses and mediates salt stress tolerance in transgenic Nicotiana benthamiana. Plant Cell Rep 33:483–498

    CAS  PubMed  Google Scholar 

  • Singh D, Laxmi A (2015) Transcriptional regulation of drought response: a tortuous network of transcriptional factors. Front Plant Sci 6:895

    PubMed  PubMed Central  Google Scholar 

  • Song Y, Chen LG, Zhang LP, Yu DQ (2010) Overexpression of OsWRKY72 gene interferes in the abscisic acid signal and auxin transport pathway of Arabidopsis. J Biosciences 35:459–471

    CAS  Google Scholar 

  • Ullah A, Sun H, Yang XY, Zhang XL (2017) Drought coping strategies in cotton: increased crop per drop. Plant Biotechnol J 15:271–284

    CAS  PubMed  PubMed Central  Google Scholar 

  • Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86

    PubMed  PubMed Central  Google Scholar 

  • Wan Y, Mao M, Wan D, Liu J, Wang G, Li G, Wang R (2018) Caragana intermedia WRKY75 Altered Arabidopsis thaliana tolerance to salt stress and ABA. Acta Bot Boreali-Occidential Sinica 38:17–25

    Google Scholar 

  • Wang PC, Zhang J, Sun L, Ma YZ, Xu J, Liang SJ et al (2018) High efficient multisites genome editing in allotetraploid cotton (Gossypium hirsutum) using CRISPR/Cas9 system. Plant Biotechnol J 16:137–150

    CAS  PubMed  Google Scholar 

  • Xu L, Jin L, Long L, Liu LL, He X, Gao W et al (2012) Overexpression of GbWRKY1 positively regulates the Pi starvation response by alteration of auxin sensitivity in Arabidopsis. Plant Cell Rep 31:2177–2188

    CAS  PubMed  Google Scholar 

  • Zhang SC, Li C, Wang R, Chen YX, Shu S, Huang RH et al (2017) The Arabidopsis mitochondrial protease FtSH4 is involved in leaf senescence via regulation of WRKY-dependent salicylic acid accumulation and signaling. Plant Physiol 173:2294–2307

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang LL, Cheng J, Sun XM, Zhao TT, Li MJ, Wang QF et al (2018a) Overexpression of VaWRKY14 increases drought tolerance in Arabidopsis by modulating the expression of stress-related genes. Plant Cell Re 37:1159–1172

    CAS  Google Scholar 

  • Zhang LP, Chen LG, Yu DQ (2018b) Transcription factor WRKY75 interacts with DELLA proteins to affect flowering. Plant Physiol 176:790–803

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Prof. Keith Lindsey (Durham University) for critical suggestions on manuscript revision. We are grateful to Huazhi Song and De Zhu (National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University) for confocal imaging, and Pengcheng Wang (National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University) for providing the CRISPR vector. We thank Prof. Sheng Luan and Dr. Congcong Hou (University of California, Berkeley) for providing pDONR221-P1P4, pDONR221-P3P2, pBIFCt-2in1-NN, and pFRETgc-2in1-NN plasmids.

Funding

This work was financially supported by the National Natural Science Foundation of China (31471541) and the National Key Project of Research and Development (2018YFD0100403).

Author information

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, Hubei, China

    Xiangyin Luo, Chao Li, Xin He, Xianlong Zhang & Longfu Zhu

Authors
  1. Xiangyin Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xin He
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xianlong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Longfu Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XZ, LZ, and XL conceived and designed research. XL conducted experiments and wrote the manuscript. CL generated GbWRKY1 transgenic materials. XH gave constructive suggestions on stress experiments. LZ revised the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Longfu Zhu.

Ethics declarations

Conflicts of interest

The authors have no conflicts of interest to declare.

Additional information

Communicated by Chun-Hai Dong.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 361 kb)

Supplementary material 2 (XLSX 10 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luo, X., Li, C., He, X. et al. ABA signaling is negatively regulated by GbWRKY1 through JAZ1 and ABI1 to affect salt and drought tolerance. Plant Cell Rep 39, 181–194 (2020). https://doi.org/10.1007/s00299-019-02480-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-019-02480-4

Keywords

Search

Navigation