Skip to main content
SpringerLink
Log in

ZmMKK4 regulates osmotic stress through reactive oxygen species scavenging in transgenic tobacco

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

Abstract

Mitogen-activated protein kinase kinase (MAPKKs) are important components of MAPK cascades, which are universal signal transduction modules and play important role in regulating both plant development and biotic or abiotic stress responses. In this study, we identified the group C MAPKK gene, ZmMKK4, in maize (Zea mays L.). Overexpression of ZmMKK4 in tobacco enhanced tolerance to osmotic stress by increased proline content and antioxidant enzyme (POD) activities compared with wild-type plants. RT-PCR revealed that one peroxidase (POX) gene, NtPOX1, was higher in ZmMKK4-overexpressing plants than in the wild-type plants. In addition, the accumulation of reactive oxygen species (ROS) in ZmMKK4-overexpressing plants is much less than that of wild-type plants. These results suggest that ZmMKK4 may be involved in ROS signaling. Taken together, these results indicate that ZmMKK4 is a positive regulator of osmotic stress by regulating scavenging of ROS in plants.

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

Similar content being viewed by others

References

  • Andreasson E, Ellis B (2010) Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci 15:106–113

    Article  PubMed  CAS  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signaling cascade in Arabidopsis innate immunity. Nature 415:977–983

    Article  PubMed  CAS  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Beck M, Komis G, Muller J, Menzel D, Samaj J (2010a) Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell 22:755–771

    Article  PubMed  CAS  Google Scholar 

  • Beck M, Komis G, Ziemann A, Menzel D, Samaj J (2010b) Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol 189:1069–1083

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Fiil BK, Petersen K, Petersen M, Mundy J (2009) Gene regulation by MAP kinase cascades. Curr Opin Plant Biol 12:615–621

    Article  PubMed  CAS  Google Scholar 

  • Gao M, Liu J, Bi D, Zhang Z, Cheng F, Chen S, Zhang Y (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res 18:1190–1198

    Article  PubMed  CAS  Google Scholar 

  • Gu L, Liu Y, Zong X, Liu L, Li DP, Li DQ (2010) Overexpression of maize mitogen-activated protein kinase gene, ZmSIMK1 in Arabidopsis increases tolerance to salt stress. Mol Biol Rep 37:4067–4073

    Article  PubMed  CAS  Google Scholar 

  • Hamel LP, Nicole MC, Sritubtim S, Morency MJ, Ellis M, Ehlting J, Beaudoin N, Barbazuk B, Klessig D, Lee J, Martin G, Mundy J, Ohashi Y, Scheel D, Sheen J, Xing T, Zhang S, Seguin A, Ellis BE (2006) Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. Trends Plant Sci 11:192–198

    Article  PubMed  CAS  Google Scholar 

  • Horsch RB, Fry JE, Hoffmann NL, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227:1229–1231

    Article  CAS  Google Scholar 

  • Hwa CM, Yang XC (2008) The AtMKK3 pathway mediates ABA and salt signaling in Arabidopsis. Acta Physiol Plant 30:277–286

    Article  CAS  Google Scholar 

  • Ichimura K, Shinozaki K, Tena G et al (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    Article  CAS  Google Scholar 

  • Jiang M, Zhang J (2001) Effect of abscisic acid on active oxygen species, antioxidative defence system and oxidative damage in leaves of maize seedlings. Plant Cell Physiol 42:1265–1273

    Article  PubMed  CAS  Google Scholar 

  • Kong X, Pan J, Zhang M, Xing X, Zhou Y, Liu Y, Li D, Li D (2011) ZmMKK4, a novel group C MAPK kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell Environ. doi:10.1111/j.1365-3040.2011.02329.x

  • Lampard GR, Lukowitz W, Ellis BE, Bergmann DC (2009) Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 21:3506–3517

    Article  PubMed  CAS  Google Scholar 

  • Lampard GR, Macalister CA, Bergmann DC (2008) Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–1116

    Article  PubMed  CAS  Google Scholar 

  • Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20:2238–2251

    Article  PubMed  CAS  Google Scholar 

  • 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 signaling. J Exp Bot 60:3221–3238

    Article  PubMed  CAS  Google Scholar 

  • Liu J, Zhu JK (1997) Proline accumulation and salt-stress-induced gene expression in a salt-hypersensitive mutant of Arabidopsis. Plant Physiol 114:591–596

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Ren D, Pike S, Pallardy S, Gassmann W, Zhang S (2007) Chloroplast-generated reactive oxygen species are involved in hypersensitive response-like cell death mediated by a mitogen-activated protein kinase cascade. Plant J 51:941–954

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Ning J, Li X, Hicks LM, Xiong L (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152:876–890

    Article  PubMed  CAS  Google Scholar 

  • Pitzschke A, Djamei A, Bitton F, Hirt H (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant 2:120–137

    Article  PubMed  CAS  Google Scholar 

  • Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M (2008a) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221

    Article  PubMed  CAS  Google Scholar 

  • Qiu JL, Zhou L, Yun BW, Nielsen HB, Fiil BK, Petersen K, Mackinlay J, Loake GJ, Mundy J, Morris PC (2008b) Arabidopsis mitogen-activated protein kinase kinases MKK1 and MKK2 have overlapping functions in defense signaling mediated by MEKK1, MPK4, and MKS1. Plant Physiol 148:212–222

    Article  PubMed  CAS  Google Scholar 

  • Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559–565

    Article  PubMed  CAS  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogen-activated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  PubMed  CAS  Google Scholar 

  • Scarpeci TE, Zanor MI, Carrillo N, Mueller-Roeber B, Valle EM (2008) Generation of superoxide anion in chloroplasts of Arabidopsis thaliana during active photosynthesis: a focus on rapidly induced genes. Plant Mol Biol 66:361–378

    Article  PubMed  CAS  Google Scholar 

  • Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y (2010) HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol 51:1766–1776

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19:63–73

    Article  PubMed  Google Scholar 

  • Xing Y, Jia W, Zhang J (2008) AtMKK1 mediates ABA-induced CAT1 expression and H2O2 production via AtMPK6-coupled signaling in Arabidopsis. Plant J 54:440–451

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Xu J, Li Y, Wang Y, Liu H, Lei L, Yang H, Liu G, Ren D (2008) Activation of MAPK kinase 9 induces ethylene and camalexin biosynthesis and enhances sensitivity to salt stress in Arabidopsis. J Biol Chem 283:26996–27006

    Article  PubMed  CAS  Google Scholar 

  • Yoo SD, Cho YH, Tena G, Xiong Y, Sheen J (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signaling. Nature 451:789–795

    Article  PubMed  CAS  Google Scholar 

  • Zhang A, Jiang M, Zhang J, Tan M, Hu X (2006a) 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Dai Y, Xiong Y, DeFraia C, Li J, Dong X, Mou Z (2007) Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance. Plant J 52:1066–1079

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

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Funding for this research was provided by the Grants from the Nation Natural Science Foundation of China (Nos. 30871457, 31071337) and the State Key Basic Research and Development Plan of China (No. 2009CB118500).

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an, 271018, Shandong, China

    Xiangpei Kong, Yan Zhou, Maoying Zhang, Yang Liu, Jiaowen Pan & Dequan Li

  2. Taishan Medical University, Tai’an, 271000, Shandong, China

    Liping Sun

Authors
  1. Xiangpei Kong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liping Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maoying Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jiaowen Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dequan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dequan Li.

Additional information

Communicated by K. Chong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 1383 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kong, X., Sun, L., Zhou, Y. et al. ZmMKK4 regulates osmotic stress through reactive oxygen species scavenging in transgenic tobacco. Plant Cell Rep 30, 2097–2104 (2011). https://doi.org/10.1007/s00299-011-1116-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-011-1116-9

Keywords

Search

Navigation