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Molecular cloning and functional characterization of MdSOS2 reveals its involvement in salt tolerance in apple callus and Arabidopsis

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Abstract

Plants respond to various environmental stresses by activating “stress genes”. CIPKs (CBL-interacting protein kinases) family genes play an important role in the process of stress response. In this study, a CIPK gene MdSOS2 was isolated from apple (Malus × Domestica). Sequence alignment and phylogenetic analysis showed that it is highly similar with Arabidopsis AtSOS2 and contained the conserved domains and motifs. Expression analysis demonstrated that MdSOS2 expressed in all tested organs at different levels, and positively in response to salt stress. Furthermore, the ectopic expression of MdSOS2 complemented the function of Arabidopsis sos2 mutant, and conferred enhanced salt tolerance to the transgenic Arabidopsis. Yeast two-hybrid assay indicated that the N-terminal of MdSOS2 protein physically interacted with MdSOS3 and AtSOS3, respectively, suggesting that SOS pathway operates in apple tree. Finally, MdSOS2 overexpression enhanced, while its suppression reduced the tolerance to salt in transgenic apple calluses, indicating that MdSOS2 acts as a positive regulator in response to salt stress in apple.

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References

  • Batelli G, Verslues PE, Agius F, Qiu Q, Fujii H, Pan SQ, Schumaker K, Grillo S, Zhu JK (2007) SOS2 promotes salt tolerance in part by interacting with the vacuolar H+-ATPase and upregulating its transport activity. Mol Cell Biol 27:7781–7790

    Article  PubMed  CAS  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  PubMed  CAS  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • D’Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schultke S, Albrecht V, Ehlert B, Schulz B, Harter K (2006) Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid dependent and independent stress responses in Arabidopsis. Plant J 48:857–872

    Article  PubMed  Google Scholar 

  • Ghassemi F, Jakeman A, Nix H (1995) Salinization of land and water resources: human causes extent management and case studies. University of South Wales Press, Sydney

    Google Scholar 

  • Halfter U, Ishitani M, Zhu JK (2000) The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci USA 97:3735–3740

    Article  PubMed  CAS  Google Scholar 

  • Hwang YH, Bethke PC, Cheong YH, Chang HS, Zhu T, Jones RL (2005) A gibberellin-regulated calcineurin B in rice localizes to the tonoplast and is implicated in vacuole function. Plant Physiol 138:1347–1358

    Article  PubMed  CAS  Google Scholar 

  • Ishitani M, Liu J, Halfter U, Kim C-S, Shi W, Zhu J-K (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium-binding. Plant Cell 12:1667–1677

    Article  PubMed  CAS  Google Scholar 

  • Kim KN, Cheong YH, Grant JJ, Pandey GK, Luan S (2003a) CIPK3, a calcium sensor-associated protein kinase that regulates abscisic acid and cold signal transduction in Arabidopsis. Plant Cell 15:411–423

    Article  PubMed  CAS  Google Scholar 

  • Kim KN, Lee JS, Han H, Ah Choi S, Joo Go S, Sun Yoon I (2003b) Isolation and characterization of a novel rice Ca2+-regulated protein kinase gene involved in responses to diverse signals including cold, light, cytokinins, sugars and salts. Plant Mol Biol 52:1191–1202

    Article  PubMed  CAS  Google Scholar 

  • Knight H (2000) Calcium signaling during abiotic stress in plants. Int Rev Cytol 195:269–324

    Article  PubMed  CAS  Google Scholar 

  • Kurusu T, Hamada J, Nokajima H, Kitagawa Y, Kiyoduka M, Takahashi A, Hanamata S, Ohno R, Hayashi T, Okada K (2010) Regulation of microbe-associated molecular pattern-induced hypersensitive cell death, phytoalexin production, and defense gene expression by calcineurin B-like protein-interacting protein kinases, OsCIPK14/15, in rice cultured cells. Plant Physiol 153:678–689

    Article  PubMed  CAS  Google Scholar 

  • Li DD, Shi W, Deng XX (2002) Agrobacterium-mediated transformation of embryogenic calluses of Ponkan mandarin and the regeneration of plants containing the chimeric ribonuclease gene. Plant Cell Rep 21:153–156

    Article  CAS  Google Scholar 

  • Liu J, Ishitani M, Halfter U, Kim C-S, Zhu J-K (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97:3730–3734

    Article  PubMed  CAS  Google Scholar 

  • Mahajan S, Sopory SK, Tuteja N (2006) Cloning and characterization of CBL-CIPK signaling components from a legume (Pisum sativum). FEBS J 273:907–925

    Article  PubMed  CAS  Google Scholar 

  • Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471:146–158

    Article  PubMed  CAS  Google Scholar 

  • Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681

    Article  PubMed  CAS  Google Scholar 

  • Ohta Masaru, Guo Yan, Halfter Ursula, Zhu Jian-Kang (2003) A novel domain in the protein kinase SOS2 mediates interaction with the protein phosphatase 2C ABI2. Proc Natl Acad Sci USA 100:11771–11776

    Article  PubMed  CAS  Google Scholar 

  • Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046

    Article  PubMed  CAS  Google Scholar 

  • Pauly N, Knight MR, Thuleau P, van der Luit AH, Moreau M, Trewavas AJ, Ranjeva R, Mazars C (2000) Control of free calcium in plant cell nuclei. Nature 405:754–755

    Article  PubMed  CAS  Google Scholar 

  • Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu J-K (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 9:8436–8441

    Article  Google Scholar 

  • Quan R, Lin H, Mendoza I, Zhang Y, Cao W, Yang Y, Shang M, Chen S, Pardo JM, Guo Y (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19:1415–1431

    Article  PubMed  CAS  Google Scholar 

  • Serrano R, Rodriguez-Navarro A (2001) Ion homeostasis during salt stress in plants. Curr Opin Cell Biol 13:399–404

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Ishitani M, Kim C, Zhu J-K (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Quintero FJ, Pardo JM, Zhu J-K (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477

    Article  PubMed  CAS  Google Scholar 

  • Shi H, Lee B, Wu S-J, Zhu J-K (2003) Overexpression of a plasma membrane Na1/H1 antiporter improves salt tolerance in Arabidopsis. Nat Biotechnol 21:81–85

    Article  PubMed  CAS  Google Scholar 

  • Tang ZC (1999) Modern experiment protocols in plant physiology. Science Press, Beijing, pp 302–308

  • Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D (2009a) CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant J 58:778–790

    Article  PubMed  CAS  Google Scholar 

  • Tripathi V, Syed N, Laxmi A, Chattopadhyay D (2009b) Role of CIPK6 in root growth and auxin transport. Plant Signal Behav 4:663–672

    Article  PubMed  CAS  Google Scholar 

  • Verslues PE, Batelli G, Grillo S, Agius F, Kim YS, Zhu J, Agarwal M, Katiyar-Agarwal S, Zhu JK (2007) Interaction of SOS2 with nucleoside diphosphate kinase 2 and catalases reveals a point of connection between salt stress and H2O2 signaling in Arabidopsis thaliana. Mol Cell Biol 27:7771–7780

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Gu D, Liu T et al (2007) Overexpression of a putative maize calcineurin B-like protein in Arabidopsis confers salt tolerance. Plant Mol Biol 65(6):733–746

    Article  PubMed  CAS  Google Scholar 

  • Weinl S, Kudla J (2009) The CBL-CIPK Ca2+-decoding signaling network: function and perspectives. New Phytol 184:517–528

    Article  PubMed  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu J-K (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14(suppl):S165–S183

    PubMed  CAS  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  PubMed  CAS  Google Scholar 

  • Yang W, Kong Z, Omo-Ikerodah E, Xu W, Li Q, Xue Y (2008) Calcineurin B-like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.). J Genet Genomics 35:531–543 (S531–S532)

    Article  PubMed  CAS  Google Scholar 

  • Yao YX, Li M, Liu Z, Hao YJ, Zhai H (2007) A novel gene, screened by cDNA-AFLP approach, contributes to lowering the acidity of fruit in apple. Plant Physiol Biochem 45:139–145

    Article  PubMed  CAS  Google Scholar 

  • Zhang HX, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19:765–768

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Sun Z, Zheng J, Guo X, Dong Z, Huai J, Gou M, He J, Jin Y, Wang J, Wang G (2009) Cloning and characterization of a novel CBL-interacting protein kinase from maize. Plant Mol Biol 69:661–674

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2001) Cell signaling under salt, water and cold stresses. Curr Opin Plant Biol 4:401–406

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhu JK (2003) Regulation of ion homeostasis under salt stress. Curr Opin Plant Biol 6:441–445

    Article  PubMed  CAS  Google Scholar 

  • Zhu Jian-Kang, Liu Ji-ping, Xiong Li-ming (1998a) Genetic analysis of salt tolerance in Arabidopsis: evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191

    Article  PubMed  CAS  Google Scholar 

  • Zhu J-K, Xiong L, Ishitani M, Liu J, Lee H, Stevenson B, Shi W (1998b) Identification of genes important for environmental stress tolerance in plants. In: Sato Y (ed) In breeding and biotechnology of environmental stress in rice. Hokkaido National Agricultural Experiment Station, Sapporo, pp 105–113

    Google Scholar 

Download references

Acknowledgments

We thank Dr. Jian-Kang Zhu for providing Arabidopsis sos2 mutant. This work was supported by the National High Technology Research and Development Program of China, 948 Project from Ministry of Agriculture (2011-G21), and “Taishan Scholar” project from Shandong Province of China.

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Correspondence to Yu-Jin Hao.

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Communicated by J. R. Liu.

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Hu, DG., Li, M., Luo, H. et al. Molecular cloning and functional characterization of MdSOS2 reveals its involvement in salt tolerance in apple callus and Arabidopsis . Plant Cell Rep 31, 713–722 (2012). https://doi.org/10.1007/s00299-011-1189-5

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  • DOI: https://doi.org/10.1007/s00299-011-1189-5

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