Skip to main content
SpringerLink
Log in

Overexpression of ZmMAPK1 enhances drought and heat stress in transgenic Arabidopsis thaliana

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinase (MAPK) signal transduction cascades play a crucial role in the response to extracellular stimuli in eukaryotes. A number of MAPK family genes have been isolated in plants, but the maize MAPK genes have been little studied. Here, we studied the role of maize MAP kinase 1 (ZmMAPK1) using gene expression, protein subcellular localization, transformation in Arabidopsis, expression patterns of the stress-responsive genes and physiological parameter analysis. Our physiological parameter analysis suggested that over-expression ZmMAPK1 can increase proline content and decrease malondialdehyde content under drought, and prevent chlorophyll loss and the production of scavenger reactive oxygen species under heat stress. The resistance characteristics of the over-expression of ZmMAPK1 were associated with a significant increase in survival rate. These results suggest that ZmMAPK1 plays a positive role in response to drought and heat stress in Arabidopsis, and provide new insights into the mechanisms of action of MAPK in response to abiotic stress 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
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

ABA:

Abscisic acid

CaMV:

Cauliflower mosaic virus

MDA:

Malondialdehyde

ROS:

Reactive oxygen species

MAPK:

Mitogen-activated protein kinase

ORF:

Open reading frame

SOD:

Superoxide dismutase

GFP:

Green fluorescent protein

References

  • Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M, Innan H, Cano L, Kamoun S, Terauchi R (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bao Y, Wang CT, Jiang CM, Pan J, Zhang GB, Liu H, Zhang HX (2014) The tumor necrosis factor receptor-associated factor (TRAF)-like family protein SEVEN IN ABSENTIA2 (SINA2) promotes drought tolerance in an ABA-dependent manner in Arabidopsis. New Phytol 202:174–187

    Article  CAS  PubMed  Google Scholar 

  • Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–220

    Article  CAS  Google Scholar 

  • Bechtold N, Pelletier G (1998) In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods Mol Biol 82:259–266

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cai G, Wang G, Wang L, Pan J, Liu Y, Li D (2014) ZmMKK1, a novel group A mitogen-activated protein kinase gene in maize, conferred chilling stress tolerance and was involved in pathogen defense in transgenic tobacco. Plant Sci 214:57–73

    Article  CAS  PubMed  Google Scholar 

  • Cheng MC, Liao PM, Kuo WW, Lin TP (2013) The Arabidopsis ETHYLENE RESPONSE FACTOR1regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 145:890–904

    Article  CAS  PubMed Central  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  CAS  PubMed  Google Scholar 

  • Ding Y, Cao J, Ni L, Zhu Y, Zhang A, Tan M, Jiang M (2013) ZmCPK11 is involved in abscisic acid-induced antioxidant defence and functions upstream of ZmMPK5 in abscisic acid signalling in maize. J Exp Bot 64:871–884

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frey A, Effroy D, Lefebvre V, Seo M, Perreau F, Berger A, Sechet J, To A, North HM, Marion-Poll A (2012) Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70:501–512

    Article  CAS  PubMed  Google Scholar 

  • Fu SF, Chou WC, Huang DD, Huang HJ (2002) Transcriptional regulation of a rice mitogen-activated proteined kinase gene, OsMAPK4, in response to environmental stresses. Plant Cell Physiol 43:958–963

    Article  CAS  PubMed  Google Scholar 

  • Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74:840–851

    Article  CAS  PubMed  Google Scholar 

  • Hartung W, Schraut D, Jiang F (2005) Physiology of abscisic acid (ABA) in roots under stress—a review of the relationship between root ABA and radial water and ABA flows. Crop Pasture Sci 56:1253–1259

    Article  CAS  Google Scholar 

  • Herskowitz I (1995) MAP kinase pathways in yeast: formating and more. Cell 80:187–197

    Article  CAS  PubMed  Google Scholar 

  • Jin YM, Jung J, Jeon H, Won SY, Feng Y, Kang JS, Lee SY, Cheong JJ, Koiwa H, Kim M (2011) AtCPL5, a novel Ser-2-specific RNA polymerase II C-terminal domain phosphatase, positively regulates ABA and drought responses in Arabidopsis. New Phytol 190:57–74

    Article  CAS  PubMed  Google Scholar 

  • Kosetsu K, Matsunaga S, Nakagami H, Colcombet J, Sasabe M, Soyano T, Takahashi Y, Hirt H, Machida Y (2010) The MAP kinase MPK4is required for cytokinesis in Arabidopsis thaliana. Plant Cell 22:3778–3790

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Larkindale J, Hall JD, Knight MR, Vierling E (2005) Heat stress phenotypes of Arabidopsis mutants implicate multiple signaling pathways in the acquisition of thermotolerance. Plant Physiol 138:882–897

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lei L, Li Y, Wang Q, Xu J, Chen YF, Yang HL, Ren DT (2014) Activation of MKK9-MPK3/MPK6 enhances phosphate acquisition in Arabidopsis thaliana. New Phytol 203:1146–1160

    Article  CAS  PubMed  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  CAS  PubMed  Google Scholar 

  • Lim CW, Lee SC (2014) Functional roles of the pepper MLO protein gene, CaMLO2, in abscisic acid signaling and drought sensitivity. Plant Mol Biol 85:1–10

    Article  CAS  PubMed  Google Scholar 

  • Lim S, Baek W, Lee SC (2014) Identification and functional roles of CaDIN1 in abscisic acid signaling and drought sensitivity. Plant Mol Biol 86:513–525

    Article  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu P, Xu ZS, Pan-Pan L, Hu D, Chen M, Li LC, Ma YZ (2013a) A wheat PI4 K gene whose product possesses threonine autophophorylation activity confers tolerance to drought and salt in Arabidopsis. J Exp Bot 64:2915–2927

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu YK, Wang L, Zhang D, Li D (2013b) Expression analysis of segmentally duplicated ZmMPK3-1 and ZmMPK3-2 genes in maize. Plant Mol Bio Rep 31:457–463

    Article  CAS  Google Scholar 

  • Luo X, Bai X, Sun X, Zhu D, Liu B, Ji W, Cai H, Cao L, Wu J, Hu M, Liu X, Tang L, Zhu Y (2013) Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signaling. J Exp Bot 64:2155–2169

    Article  CAS  PubMed  Google Scholar 

  • Lv WT, Lin B, Zhang M, Hua XJ (2011) Proline accumulation is inhibitory to Arabidopsis seedlings during heat stress. Plant Physiol 156:1921–1933

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Macková H, Hronková M, Dobrá J, Turečková V, Novák O, Lubovská Z, Motyka V, Haisel D, Hájek T, Prášil IT, Gaudinová A, Štorchová H, Ge E, Werner T, Schmülling T, Vanková R (2013) Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokine in oxidase/dehydrogenase gene expression. J Exp Bot 64:2805–2815

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10:339–346

    Article  CAS  PubMed  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  CAS  PubMed Central  PubMed  Google Scholar 

  • Pan J, Zhang M, Kong X, Xing X, Liu Y, Zhou Y, Liu Y, Sun L, Li D (2012) ZmMAPK17, a novel maize group D MAP kinase gene, is involved in multiple stress responses. Planta 235:661–676

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Hirt H (2006) Mitogen-activated protein kinase and reactive oxygen species signaling in plants. Plant Physiol 141:351–356

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pitzschke A, Hirt H (2009) Disentangling the complexity of mitogen-activated protein kinases and reactive oxygen species signaling. Plant Physiol 149:606–615

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sharma S, Villamor JG, Verslues PE (2011) Essential role of tissue-specific proline synthesis and catabolism in growth and redox balance at low water potential. Plant Physiol 157:292–304

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen X, Yuan B, Liu H, Li X, Xu C, Wang S (2010) Opposite functions of a rice mitogen-activated protein kinase during the process of resistance against Xanthomonas oryzae. Plant J 64:86–99

    CAS  PubMed  Google Scholar 

  • Sudhakar C, Lakshmi A, Giridarakumar S (2001) Changes in the antioxidant enzyme efficacy in two high yielding genotypes of mulberry (Morusalba L.) under NaCl salinity. Plant Sci 161:613–619

    Article  CAS  Google Scholar 

  • Thomas G (1992) MAP kinase by any other name smells just as sweet. Cell 68:3–6

    Article  CAS  PubMed  Google Scholar 

  • Tian S, Mao X, Zhang H, Chen S, Zhai C, Yang S, Jing R (2013) Cloning and characterization of TaSnRK2.3, a novel SnRK2 gene in common wheat. J Exp Bot 64:2063–2080

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Volkov RA, Panchuk II, Mullineaux PM, Schöffl F (2006) Heat stress-induced H2O2 is required for effective expression of heat shock genes in Arabidopsis. Plant Mol Bio 61:733–746

    Article  CAS  Google Scholar 

  • Wang NN, Shih MC, Li N (2005) The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J Exp Bot 56:909–920

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Ding H, Zhang A, Ma F, Cao J, Jiang M (2010) A novel mitogen-activated protein kinase gene in maize (Zea mays), ZmMPK3, is involved in response to diverse environmental cues. J Integr Plant Biol 52:442–452

    CAS  PubMed  Google Scholar 

  • Wang LC, Wu JR, Chang WL, Yeh CH, Ke YT, Lu CA, Wu SJ (2013) Arabidopsis HIT4 encodes a novel chromocentre-localized protein involved in the heat reactivation of transcriptionally silent loci and is essential for heat tolerance in plants. J Exp Bot 64:1689–1701

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Liu Y, Cai G, Jiang S, Pan J, Li D (2014) Ectopic expression of ZmSIMK1 leads to improved drought tolerance and activation of systematic acquired resistance in transgenic tobacco. J Biotechnol 172:18–29

    Article  CAS  PubMed  Google Scholar 

  • Wei KF, Wang YM, Zhong XJ, Pan S (2014) Protein kinase structure, expression and regulation in maize drought signaling. Mol Breeding 34:583–602

    Article  CAS  Google Scholar 

  • Wu LJ, Wang XT, Wu LC, Wang PA, Chen YH (2011a) Molecular cloning and expression analysis of an HINT1 homologue from maize (Zea mays L.). Plant Mol Biol Rep 29:1006–1012

    Article  CAS  Google Scholar 

  • Wu T, Kong XP, Zong XJ, Li DP, Li DQ (2011b) Expression analysis of five maize MAP kinase genes in response to various abiotic stresses and signal molecules. Mol Biol Rep 38:3967–3975

    Article  CAS  PubMed  Google Scholar 

  • Yoo CY, Pence HE, Jin JB, Miura K, Gosney MJ, Hasegawa PM, Mickelbart MV (2010) The Arabidopsis GTL1 transcription factor regulates water use efficiency and drought tolerance by modulating stomatal density via transrepression of SDD1. Plant Cell 22:4128–4141

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zeng Q, Chen JG, Ellis BE (2011) AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant J 67:895–906

    Article  CAS  PubMed  Google Scholar 

  • Zhang A, Zhang J, Ye N, Cao J, Tan M, Zhang J, Jiang M (2010) ZmMPK5 is required for the NADPH oxidase-mediated self-propagation of apoplastic H2O2 in brassinosteroid-induced antioxidant defence in leaves of maize. J Exp Bot 61:4399–4411

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang M, Pan J, Kong X, Zhou Y, Liu Y, Sun L, Li D (2012) ZmMKK3, a novel maize group B mitogen-activated protein kinase kinase gene, mediates osmotic stress and ABA signal responses. J Plant Physiol 169:1501–1510

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Jiang S, Pan J, Kong X, Zhou Y, Liu Y, Li D (2014) The overexpression of a maize mitogen-activated protein kinase gene (ZmMPK5) confers salt stress tolerance and induces defence responses in tobacco. Plant Biol (Stuttg) 16:558–570

    Article  CAS  Google Scholar 

  • Zhou W, Zhou T, Li MX, Zhao CL, Jia N, Wang XX, Sun YZ, Li GL, Xu M, Zhou RG, Li B (2012a) The Arabidopsis J-protein AtDjB1 facilitates thermotolerance by protecting cells against heat-induced oxidative damage. New Phytol 194:364–378

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Zhang D, Pan J, Kong X, Liu Y, Sun L, Wang L, Li D (2012b) Overexpression of a multiple stress-responsive gene, ZmMPK4, enhances tolerance to low temperature in transgenic tobacco. Plant Physiol Biochem 58:174–181

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu JK, Hasegawa PM, Bressan RA, Bohnert HJ (1997) Molecular aspects of osmotic stress in plants. Crit Rev Plant Sci 16:253–277

    Article  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  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Prof. Zhankuan Chen (Henan Academy of Agricultural Sciences) for providing plasmid pCAMBIA1304. We also thank Prof. Hairong Zhang (Henan Agricultural University) for kind help in the Arabidopsis transformation work. This research was supported by grants from the National Nature Science Foundation of China (No. 31471503) and the National Basic Research Program of China (973 Program, No. 2011CB111500).

Author information

Author notes

    Authors and Affiliations

    1. Henan Agricultural University, Synergetic Innovation Center of Henan Grain Crops, 63 Nongye Road, Zhengzhou, 450002, People’s Republic of China

      Liuji Wu, Xiaofeng Zu, Huimin Zhang, Liancheng Wu, Zhangying Xi & Yanhui Chen

    2. Key Laboratory of Physiological Ecology and Genetic Improvement of Food Crops in Henan Province, Zhengzhou, 450002, People’s Republic of China

      Liuji Wu, Xiaofeng Zu, Huimin Zhang, Liancheng Wu, Zhangying Xi & Yanhui Chen

    Authors
    1. Liuji Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Xiaofeng Zu
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Huimin Zhang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Liancheng Wu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Zhangying Xi
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Yanhui Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Yanhui Chen.

    Additional information

    Liuji Wu and Xiaofeng Zu have contributed equally to this work.

    Electronic supplementary material

    Below is the link to the electronic supplementary material.

    Supplementary material 1 (DOCX 860 kb)

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Wu, L., Zu, X., Zhang, H. et al. Overexpression of ZmMAPK1 enhances drought and heat stress in transgenic Arabidopsis thaliana . Plant Mol Biol 88, 429–443 (2015). https://doi.org/10.1007/s11103-015-0333-y

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s11103-015-0333-y

    Keywords

    Search

    Navigation