Skip to main content
SpringerLink
Log in

The Arabidopsis kinase-associated protein phosphatase KAPP, interacting with protein kinases SnRK2.2/2.3/2.6, negatively regulates abscisic acid signaling

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

The kinase-associated protein phosphatase, KAPP, is negatively involved in abscisic acid (ABA) signaling. KAPP interacts physically with SnRK2.2, SnRK2.3 and SnRK2.6, and functionally acts upstream of SnRK2.2 and SnRK2.3.

Abstract

The kinase-associated protein phosphatase (KAPP) has been reported to be involved in the regulation of many developmental and signaling events, but it remains unknown whether KAPP is involved in ABA signaling. Here, we report that KAPP is negatively involved in ABA-mediated seed germination and early seedling growth in Arabidopsis thaliana. The two loss-of-function mutants of KAPP, kapp-1 and kapp-2, exhibit increased ABA sensitivity in ABA-induced seed germination inhibition and post-germination growth arrest. The three closely-related protein kinase, (SNF1)-related protein kinase SnRK2.2, SnRK2.3 and SnRK2.6, which play critical roles in ABA signaling, interact and co-localize with KAPP. Genetic evidence showed that the ABA-hypersensitive phenotypes caused by KAPP mutation were suppressed by the double mutation of SnRK2.2 and SnRK2.3, indicating that KAPP functions upstream of SnRK2.2 and SnRK2.3 in ABA signaling. RNA-sequencing analysis revealed that KAPP mutation affects expression of multiple ABA-responsive genes. These results demonstrated that KAPP is negatively involved in plant response to ABA, which help to understand the complicated ABA signaling mechanism.

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

Similar content being viewed by others

References

  • Acharya BR, Jeon BW, Zhang W, Assmann SM (2013) Open Stomata 1 (OST1) is limiting in abscisic acid responses of Arabidopsis guard cells. New Phytol 200:1049–1063

    CAS  PubMed  Google Scholar 

  • Bi C, Ma Y, Jiang SC, Mei C, Wang XF, Zhang DP (2019) Arabidopsis translation initiation factors eIFiso4G1/2 link repression of mRNA cap-binding complex eIFiso4F assembly with RNA-binding protein SOAR1-mediated ABA signaling. New Phytol 223:1388–1406

    CAS  PubMed  Google Scholar 

  • Braun DM, Stone JM, Walker JC (1997) Interaction of the maize and Arabidopsis kinase interaction domains with a subset of receptor-like protein kinases: implications for transmembrane signaling in plants. Plant J 12:83–95

    CAS  PubMed  Google Scholar 

  • Chen H, Zou Y, Shang Y, Lin H, Wang Y, Cai R, Zhou JM (2008) Firefly luciferase complementation imaging assay for protein-protein interactions in plants. Plant Physiol 146:368–376

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    CAS  PubMed  Google Scholar 

  • Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis Dev Cell 32:278–289

    CAS  PubMed  Google Scholar 

  • Ding Z, Wang H, Liang X, Morris ER, Gallazzi F, Pandit S, Van Doren SR (2007) Phosphoprotein and phosphopeptide interactions with the FHA domain from Arabidopsis kinase-associated protein phosphatase. Biochemistry 46:2684–2696

    CAS  PubMed  Google Scholar 

  • Dong T, Park Y, Hwang I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays Biochem 58:29–48

    PubMed  Google Scholar 

  • Feng CZ, Chen Y, Wang C, Kong YH, Wu WH, Chen YF (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80:654–668

    CAS  PubMed  Google Scholar 

  • Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci USA 106:8380–8385

    CAS  PubMed  Google Scholar 

  • Fujii H, Verslues PE, Zhu JK (2007) Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis Plant Cell 19:485–494

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Yamaguchi-Shinozaki K (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis Plant Cell 17:3470–3488

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Gomez L, Bauer Z, Boller T (2001) Both the extracellular leucine-rich repeat domain and the kinase activity of FSL2 are required for flagellin binding and signaling in Arabidopsis Plant Cell 13:1155–1163

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gramegna G, Modesti V, Savatin DV, Sicilia F, De Cervone F (2016) GRP-3 and KAPP, encoding interactors of WAK1, negatively affect defense responses induced by oligogalacturonides and local response to wounding. J Exp Bot 67:1715–1729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guo J, Zeng Q, Emami M, Ellis BE, Chen JG (2008) The GCR2 gene family is not required for ABA control of seed germination and early seedling development in Arabidopsis PLoS ONE 3:e2982

    PubMed  PubMed Central  Google Scholar 

  • Hirayama T, Shinozaki K (2007) Perception and transduction of abscisic acid signals: keys to the function of the versatile plant hormone ABA. Trends Plant Sci 12:343–351

    CAS  PubMed  Google Scholar 

  • Huang Y, Feng CZ, Ye Q, Wu WH, Chen YF (2016) Arabidopsis WRKY6 transcription factor acts as a positive regulator of abscisic acid signaling during seed germination and early seedling development. PLoS Genet 12:e1005833

    PubMed  PubMed Central  Google Scholar 

  • Kong L, Cheng J, Zhu Y, Ding Y, Meng J, Chen Z, Gong Z (2015) Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases. Nat Commun 6:8630

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krzywinska E, Bucholc M, Kulik A, Ciesielski A, Lichocka M, Dębski J, Dobrowolska G (2016) Phosphatase ABI1 and okadaic acid-sensitive phosphoprotein phosphatases inhibit salt stress-activated SnRK2.4 kinase. BMC Plant Biol 16:136

  • Kuromori T, Seo M, Shinozaki K (2018) ABA transport and plant water stress responses. Trends Plant Sci 23:513–522

    CAS  PubMed  Google Scholar 

  • Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60

    CAS  PubMed  Google Scholar 

  • Leung J, Merlot S, Giraudat J (1997) The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9:759–771

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Smith GP, Walker JC (1999) Kinase interaction domain of kinase-associated protein phosphatase, a phosphoprotein-binding domain. Proc Natl Acad Sci USA 96:7821–7826

    CAS  PubMed  Google Scholar 

  • Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328

    CAS  PubMed  Google Scholar 

  • Lu K, Liang S, Wu Z, Bi C, Yu YT, Wang XF, Zhang DP (2016) Overexpression of an Arabidopsis cysteine-rich receptor-like protein kinase, CRK5, enhances abscisic acid sensitivity and confers drought tolerance. J Exp Bot 67:5009–5027

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ma XL, Zhang QY, Zhu QL, Liu W, Chen Y, Qiu R, Liu YG (2015) A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol Plant 8:1274–1284

    CAS  PubMed  Google Scholar 

  • Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324:1064–1068

    CAS  PubMed  Google Scholar 

  • Manabe Y, Bressan RA, Wang T, Li F, Koiwa H, Sokolchik I, Maggio A (2008) The Arabidopsis kinase-associated protein phosphatase regulates adaptation to Na+ stress. Plant Physiol 146:612–622

    CAS  PubMed  PubMed Central  Google Scholar 

  • Merlot S, Gosti F, Guerrier D, Vavasseur A, Giraudat J (2001) The ABI1 and ABI2 protein phosphatases 2C act in a negative feedback regulatory loop of the abscisic acid signalling pathway. Plant J 25:295–303

    CAS  PubMed  Google Scholar 

  • Nee G, Kramer K, Nakabayashi K, Yuan B, Xiang Y, Miatton E, Finkemeier I (2017) DELAY OF GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nat Commun 8:72

    PubMed  PubMed Central  Google Scholar 

  • Pandey S, Nelson DC, Assmann SM (2009) Two novel GPCR-type G proteins are abscisic acid receptors in Arabidopsis Cell 136:136–148

    CAS  PubMed  Google Scholar 

  • Park SY, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Cutler SR (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 

  • Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20:2729–2745

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saez A, Apostolova N, Gonzalez-Guzman M, Gonzalez-Garcia MP, Nicolas C, Lorenzo O, Rodriguez PL (2004) Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling. Plant J 37:354–369

    CAS  PubMed  Google Scholar 

  • Schweighofer A, Hirt H, Meskiene I (2004) Plant PP2C phosphatases: emerging functions in stress signaling. Trends Plant Sci 9:236–243

    CAS  PubMed  Google Scholar 

  • Shah K, Russinova E, Gadella TW Jr, Willemse J, De Vries SC (2002) The Arabidopsis kinase-associated protein phosphatase controls internalization of the somatic embryogenesis receptor kinase 1. Genes Dev 16:1707–1720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shang Y, Yan L, Liu ZQ, Cao Z, Mei C, Xin Q, Zhang DP (2010) The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell 22:1909–1935

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shen YY, Wang XF, Wu FQ, Du SY, Cao Z, Shang Y, Zhang DP (2006) The Mg-chelatase H subunit is an abscisic acid receptor. Nature 443:823–826

    CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    CAS  PubMed  Google Scholar 

  • Skubacz A, Daszkowska-Golec A, Szarejko I (2016) The role and regulation of ABI5 (ABA-insensitive 5) in plant development, abiotic stress responses and phytohormone crosstalk. Front Plant Sci 7:1884

    PubMed  PubMed Central  Google Scholar 

  • Singh A, Pandey A, Srivastava AK, Tran LS, Pandey GK (2016) Plant protein phosphatases 2C: from genomic diversity to functional multiplicity and importance in stress management. Crit Rev Biotechnol 36:1023–1035

    CAS  PubMed  Google Scholar 

  • Sirichandra C, Davanture M, Turk BE, Zivy M, Valot B, Leung J, Merlot S (2010) The Arabidopsis ABA-activated kinase OST1 phosphorylates the bZIP transcription factor ABF3 and creates a 14-3-3 binding site involved in its turnover. PLoS ONE 5:e13935

    PubMed  PubMed Central  Google Scholar 

  • Stone JM, Collinge MA, Smith RD, Horn MA, Walker JC (1994) Interaction of a protein phosphatase with an Arabidopsis serine-threonine receptor kinase. Science 266:793–795

    CAS  PubMed  Google Scholar 

  • Stone JM, Trotochaud AE, Walker JC, Clark SE (1998) Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Plant Physiol 117:1217–1225

    CAS  PubMed  PubMed Central  Google Scholar 

  • Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y, Dohmae N, Shinozaki K (2018) A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556:235–238

    CAS  PubMed  Google Scholar 

  • Tichtinsky G, Vanoosthuyse V, Cock JM, Gaude T (2003) Making inroads into plant receptor kinase signalling pathways. Trends Plant Sci 8:231–237

    CAS  PubMed  Google Scholar 

  • Trotochaud AE, Hao T, Wu G, Yang Z, Clark SE (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11:393–406

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuzuki T, Takahashi K, Inoue S, Okigaki Y, Tomiyama M, Hossain MA, Shimazaki K, Murata Y, Kinoshita T (2011) Mg-chelatase H subunit affects ABA signaling in stomatal guard cells, but is not an ABA receptor in Arabidopsis thaliana J Plant Res 124:527–538

    CAS  PubMed  PubMed Central  Google Scholar 

  • Umezawa T, Sugiyama N, Mizoguchi M, Hayashi S, Myouga F, Yamaguchi-Shinozaki K, Shinozaki K (2009) Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis Proc Natl Acad Sci USA 106:17588–17593

    CAS  PubMed  Google Scholar 

  • Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 8:161

    PubMed  PubMed Central  Google Scholar 

  • Wang X (2002) Phospholipase D in hormonal and stress signaling. Curr Opin Plant Biol 5:408–414

    CAS  PubMed  Google Scholar 

  • Wang P, Xue L, Batelli G, Lee S, Hou YJ, Van Oosten MJ, Zhu JK (2013) Quantitative phosphoproteomics identifies SnRK2 protein kinase substrates and reveals the effectors of abscisic acid action. Proc Natl Acad Sci USA 110:11205–11210

    CAS  PubMed  Google Scholar 

  • Williams RW, Wilson JM, Meyerowitz EM (1997) A possible role for kinase-associated protein phosphatase in the Arabidopsis CLAVATA1 signaling pathway. Proc Natl Acad Sci USA 94:10467–10472

    CAS  PubMed  Google Scholar 

  • Yang W, Zhang W, Wang X (2017) Post-translational control of ABA signalling: the roles of protein phosphorylation and ubiquitination. Plant Biotechnol J 15:4–14

    CAS  PubMed  Google Scholar 

  • Zhang XF, Jiang T, Yu YT, Wu Z, Jiang SC, Lu K, Feng XJ, Liang S, Lu YF, Wang XF, Zhang DP (2014) Arabidopsis co-chaperonin CPN20 antagonizes Mg-chelatase H subunit to derepress ABA responsive WRKY40 transcription repressor. Sci China Life Sci 57:11–21

    CAS  PubMed  Google Scholar 

  • Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis Plant Physiol 124:941–948

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Natural Science Foundation of China (Grant No. 31700229), the Jiangsu Provincial Natural Science Foundation (Grant No. BK20170594), the Key Research and Development Projects of Jiangsu Province (Grant No. BE2016370) and the National Key Technology Support Program Project (Grant No. 2015BAD01B00). We thank Dr. Yaoguang Liu for providing vectors for gene editing, and the staffs of Genepioneer Biotechnologies Co., Ltd., Nanjing, China for their help on bioinformatics analysis. The T-DNA insertion line was provided by ABRC.

Author information

Author notes

  1. Kai Lu and Ya-Dong Zhang contributed equally to this work.

Authors and Affiliations

  1. Institute of Food Crops, Provincial Key Laboratory of Agrobiology, Jiangsu Academy of Agricultural Sciences/ Jiangsu High Quality Rice Research and Development Center / Nanjing Branch of China National Center for Rice Improvement, Nanjing, 210014, China

    Kai Lu, Ya-Dong Zhang, Chun-Fang Zhao, Li-Hui Zhou, Qing-Yong Zhao, Tao Chen & Cai-Lin Wang

Authors
  1. Kai Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ya-Dong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chun-Fang Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Li-Hui Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qing-Yong Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Tao Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Cai-Lin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cai-Lin Wang.

Additional information

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 (XLSX 86.2 kb)

Supplementary material 2 (DOCX 4643.8 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lu, K., Zhang, YD., Zhao, CF. et al. The Arabidopsis kinase-associated protein phosphatase KAPP, interacting with protein kinases SnRK2.2/2.3/2.6, negatively regulates abscisic acid signaling. Plant Mol Biol 102, 199–212 (2020). https://doi.org/10.1007/s11103-019-00941-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-019-00941-8

Keywords

Search

Navigation