Skip to main content
Log in

Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinase (MAPK) cascades play a remarkably crucial role in plants. It has been studied intensively in model plants Arabidopsis, tobacco and rice. However, the function of MAPKs in maize (Zea mays L.) has not been well documented. ZmSIMK1 (Zea mays salt-induced mitogen-activated protein kinase 1) is a previously identified MAPK gene in maize. In this research, we charactered ZmSIMK1 and showed that ZmSIMK1 was involved in Arabidopsis salt stress. The genomic organization of ZmSIMK1 gene and its expression in maize have been analyzed. In order to investigate the function of ZmSIMK1, we generated transgenic Arabidopsis constitutively overexpressing ZmSIMK1. Ectopic expression of ZmSIMK1 in Arabidopsis resulted in increased resistance against salt stress. Importantly, ZmSIMK1-overexpressing Arabidopsis exhibited constitutive expression of stress-responsive marker genes, RD29A and P5CS1. Furthermore, RD29A and P5CS1 were upregulated under salt stress. These results suggest that ZmSIMK1 may play an important role in plant salt stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Ai J, Wang Y, Tan K, Deng Y, Luo N, Yuan W, Wang Z, Li Y, Wang Y, Mo X, Zhu C, Yin Z, Liu M, Wu X (2008) A human homolog of mouse Lbh gene, hLBH, expresses in heart and activates SRE and AP-1 mediated MAPK signaling pathway. Mol Biol Rep 35:179–187

    Article  CAS  PubMed  Google Scholar 

  2. Mishra NS, Tuteja R, Tuteja N (2006) Signaling through MAP kinase networks in plants. Arch Biochem Biophys 452:55–68

    Article  CAS  PubMed  Google Scholar 

  3. Colcombet J, Hirt H (2008) Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochem J 413:217–226

    Article  CAS  PubMed  Google Scholar 

  4. Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  CAS  PubMed  Google Scholar 

  5. Xu H, Li K, Yang F, Shi Q, Wang X (2009) Overexpression of CsNMAPK in tobacco enhanced seed germination under salt and osmotic stresses. Mol Biol Rep. doi: 10.1007/s11033-009-9895-6

  6. Ghawana S, Kumar S, Ahuja PS (2010) Early low-temperature responsive mitogen activated protein kinases RaMPK1 and RaMPK2 from Rheum australe D. Don respond differentially to diverse stresses. Mol Biol Rep 37:933–938

    Article  CAS  PubMed  Google Scholar 

  7. Peng S, Zhang Y, Zhang J, Wang H, Ren B (2009) Effect of ketamine on ERK expression in hippocampal neural cell and the ability of learning behavior in minor rats. Mol Biol Rep. doi: 10.1007/s11033-009-9892-9

  8. Zhu N, Shao Y, Xu L, Yu L, Sun L (2009) Gadd45-alpha and Gadd45-gamma utilize p38 and JNK signaling pathways to induce cell cycle G2/M arrest in Hep-G2 hepatoma cells. Mol Biol Rep 36:2075–2085

    Article  CAS  PubMed  Google Scholar 

  9. Agarwal PK, Gupta K, Jha B (2010) Molecular characterization of the Salicornia brachiata SbMAPKK gene and its expression by abiotic stress. Mol Biol Rep 37:981–986

    Article  CAS  PubMed  Google Scholar 

  10. Group MAPK (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    Article  Google Scholar 

  11. Duerr B, Gawienowski M, Ropp T, Jacobs T (1993) MsERK1: a mitogen-activated protein kinase from a flowering plant. Plant Cell 5:87–96

    Article  CAS  PubMed  Google Scholar 

  12. Reyna NS, Yang Y (2006) Molecular analysis of the rice MAP kinase gene family in relation to Magnaporthe grisea infection. Mol Plant Microbe Interact 19:530–540

    Article  CAS  PubMed  Google Scholar 

  13. Nicole MC, Hamel LP, Morency MJ, Beaudoin N, Ellis BE, Seguin A (2006) MAP-ping genomic organization and organ-specific expression profiles of poplar MAP kinases and MAP kinase kinases. BMC Genomics 7:223

    Article  PubMed  Google Scholar 

  14. Zhang T, Liu Y, Yang T, Zhang L, Xu S, Xue L, An L (2006) Diverse signals converge at MAPK cascades in plant. Plant Physiol Biochem 44:274–283

    Article  CAS  PubMed  Google Scholar 

  15. Berberich T, Sano H, Kusano T (1999) Involvement of a MAP kinase, ZmMPK5, in senescence and recovery from low-temperature stress in maize. Mol Gen Genet 262:534–542

    Article  CAS  PubMed  Google Scholar 

  16. Lalle M, Visconti S, Marra M, Camoni L, Velasco R, Aducci P (2005) ZmMPK6, a novel maize MAP kinase that interacts with 14-3-3 proteins. Plant Mol Biol 59:713–722

    Article  CAS  PubMed  Google Scholar 

  17. Wang Q, Zhai S, Zhang Y, Yin X, Zhang J (2005) Cloning and molecular characterization of a gene encoding MAP kinase from maize and its expression in E. coli. High Technol Lett 11:315–319

    CAS  Google Scholar 

  18. Zong XJ, Li DP, Gu LK, Li DQ, Liu LX, Hu XL (2009) Abscisic acid and hydrogen peroxide induce a novel maize group C MAP kinase gene, ZmMPK7, which is responsible for the removal of reactive oxygen species. Planta 229:485–495

    Article  CAS  PubMed  Google Scholar 

  19. Zhang A, Jiang M, Zhang J, Tan M, Hu X (2006) Mitogen-activated protein kinase is involved in abscisic acid-induced antioxidant defense and acts downstream of reactive oxygen species production in leaves of maize plants. Plant Physiol 141:475–487

    Article  CAS  PubMed  Google Scholar 

  20. Zhang A, Jiang M, Zhang J, Ding H, Xu S, Hu X, Tan M (2007) Nitric oxide induced by hydrogen peroxide mediates abscisic acid-induced activation of the mitogen-activated protein kinase cascade involved in antioxidant defense in maize leaves. New Phytol 175:36–50

    Article  CAS  PubMed  Google Scholar 

  21. Ding H, Zhang A, Wang J, Lu R, Zhang H, Zhang J, Jiang M (2009) Identity of an ABA-activated 46 kDa mitogen-activated protein kinase from Zea mays leaves: partial purification, identification and characterization. Planta 230:239–251

    Article  CAS  PubMed  Google Scholar 

  22. Lin F, Ding H, Wang J, Zhang H, Zhang A, Zhang Y, Tan M, Dong W, Jiang M (2009) Positive feedback regulation of maize NADPH oxidase by mitogen-activated protein kinase cascade in abscisic acid signalling. J Exp Bot 60:3221–3238

    Article  CAS  PubMed  Google Scholar 

  23. Alexandrov NN, Brover VV, Freidin S, Troukhan ME, Tatarinova TV, Zhang H, Swaller TJ, Lu YP, Bouck J, Flavell RB, Feldmann KA (2009) Insights into corn genes derived from large-scale cDNA sequencing. Plant Mol Biol 69:179–194

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  25. Mizoguchi T, Irie K, Hirayama T, Hayashida N, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K (1996) A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold, and water stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 93:765–769

    Article  CAS  PubMed  Google Scholar 

  26. Ichimura K, Mizoguchi T, Irie K, Morris P, Giraudat J, Matsumoto K, Shinozaki K (1998) Isolation of ATMEKK1 (a MAP kinase kinase kinase)-interacting proteins and analysis of a MAP kinase cascade in Arabidopsis. Biochem Biophys Res Commun 253:532–543

    Article  CAS  PubMed  Google Scholar 

  27. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24:655–665

    Article  CAS  PubMed  Google Scholar 

  28. Teige M, Scheikl E, Eulgem T, Doczi R, Ichimura K, Shinozaki K, Dangl JL, Hirt H (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15:141–152

    Article  CAS  PubMed  Google Scholar 

  29. Ulm R, Ichimura K, Mizoguchi T, Peck SC, Zhu T, Wang X, Shinozaki K, Paszkowski J (2002) Distinct regulation of salinity and genotoxic stress responses by Arabidopsis MAP kinase phosphatase 1. EMBO J 21:6483–6493

    Article  CAS  PubMed  Google Scholar 

  30. Liu L, Hu X, Song J, Zong X, Li DP, Li D (2009) Over-expression of a Zea mays L. protein phosphatase 2C gene (ZmPP2C) in Arabidopsis thaliana decreases tolerance to salt and drought. J Plant Physiol 166:531–542

    Article  CAS  PubMed  Google Scholar 

  31. Xu Y, Li DP, Gu L, Hu X, Zong X, Li D (2005) Cloning and expression characteristics of protein phosphatase gene ZmPP2C of Zea mays roots. J Plant Physiol Mol Biol 31:183–189

    CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  33. Koo SC, Yoon HW, Kim CY, Moon BC, Cheong YH, Han HJ, Lee SM, Kang KY, Kim MC, Lee SY, Chung WS, Cho MJ (2007) Alternative splicing of the OsBWMK1 gene generates three transcript variants showing differential subcellular localizations. Biochem Biophys Res Commun 360:188–193

    Article  CAS  PubMed  Google Scholar 

  34. Liu H, He R, Zhang H, Huang Y, Tian M, Zhang J (2010) Analysis of synonymous codon usage in Zea mays. Mol Biol Rep 37:677–684

    Article  CAS  PubMed  Google Scholar 

  35. Lai J, Dey N, Kim CS, Bharti AK, Rudd S, Mayer KF, Larkins BA, Becraft P, Messing J (2004) Characterization of the maize endosperm transcriptome and its comparison to the rice genome. Genome Res 14:1932–1937

    Article  PubMed  Google Scholar 

  36. Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk LA, Lamkemeyer T, Fladerer C, Madlung J, Barbazuk B, Nordheim A, Nettleton D, Schnable PS, Hochholdinger F (2007) Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol 145:575–588

    Article  CAS  PubMed  Google Scholar 

  37. Gao L, Xiang CB (2008) The genetic locus At1g73660 encodes a putative MAPKKK and negatively regulates salt tolerance in Arabidopsis. Plant Mol Biol 67:125–134

    Article  CAS  PubMed  Google Scholar 

  38. Cao Z, Jia Z, Liu Y, Wang M, Zhao J, Zheng J, Wang G (2010) Constitutive expression of ZmsHSP in Arabidopsis enhances their cytokinin sensitivity. Mol Biol Rep 37:1089–1097

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Many thanks to Professor Juren Zhang for providing helpful suggestions. This work was supported by the National Natural Science Foundation of China (Nos. 30471052, 30871457) and the State Key Basic Research and Development Plan of China (No. 2009CB118500), and also was supported by the Program for Changjiang Scholars and Innovative Research Team in University (No. IRT0635).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to De-Quan Li.

Additional information

Lingkun Gu and Yukun Liu have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 775 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gu, L., Liu, Y., Zong, X. et al. Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Mol Biol Rep 37, 4067–4073 (2010). https://doi.org/10.1007/s11033-010-0066-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-010-0066-6

Keywords

Navigation