Skip to main content
Springer Nature Link
Log in

Characterization and expression analysis of mitogen-activated protein kinase cascade genes in wheat subjected to phosphorus and nitrogen deprivation, high salinity, and drought

  • Original Article
  • Published:
Journal of Plant Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinase (MAPK) cascades are conserved signal-transducing modules that have important functions in plant growth and development as well as in diverse biotic and abiotic stress responses. In this study, six MAP kinase kinase kinase genes, two MAP kinase kinase genes, and 11 MAP kinase genes in wheat were characterized. The MAPK cascade members of wheat were named based on their homologs in Brachypodium distachyon and Arabidopsis. The polypeptides translated from these MAPK cascade genes share conserved domains similar to those reported in B. distachyon and Arabidopsis, and such domains are involved in protein interaction and phosphorylation. Expression analysis results of the MAPK cascade members revealed that some of the selected genes were involved in responses to phosphorus (P; ten genes) and nitrogen (N; five genes) deprivation, salinity (five genes), and drought (three genes). Such genes were either upregulated or downregulated. Temporal expression profile analysis of the stress-responsive MAPK members indicated that all of these genes were progressively regulated by stress and exhibited typical recovery responses when these genes were exposed again to normal growth conditions. Two MAPK members, TaMPK6 and TaMPK16, responded to four stress factors, including deprivations of P and N as well as salt and drought stress. TaMPK4, TaMPK12;1, TaMPK14, and TaMPK17 were responsive to two stress factors. These results suggested that various MAPK cascade members in wheat are involved in mediating signal transductions by transcriptionally regulating P and N deprivations, high salinity, and drought. TaMPK6 and TaMPK16, together with TaMPK4, TaMPK12;1, TaMPK14, and TaMPK17 have potential functions in mediating plant responses and tolerance to two or more stress factors by distinct MAPK cascade modules. Our data have provided information about MAPK modules and put further insight into their biological functions in abiotic stress response of wheat.

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

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

MAPK:

Mitogen-activated protein kinase

MAPKK:

Mitogen-activated protein kinase kinase

MAPKKK:

Mitogen-activated protein kinase kinase kinase

PEG:

polyethylene glycol

CK:

Control group

Pi:

Inorganic phosphate

RT-PCR:

Reverse transcriptase-polymerase chain reactions

pI:

Isoelectric points

ER:

Endoplasmic reticulum

References

  • Agrawal GK, Rakwal R, Iwahashi H (2002) Isolation of novel rice (Oryza sativa L.) multiple stress responsive MAP kinase gene, OsMSRMK2, whose mRNA accumulates rapidly in response to environmental cues. Biochem Biophys Res Commun 294:1009–1016

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cardinale F, Meskiene I, Ouaked F, Hirt H (2002) Convergence and divergence of stress-induced mitogen-activated protein kinase signaling pathways at the level of two distinct mitogen-activated protein kinase kinases. Plant Cell 14:703–711

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chen L, Hu W, Tan S, Wang M, Ma Z, Zhou S, Deng X, Zhang Y, Huang C, Yang G, He G (2012) Genome-wide identification and analysis of MAPK and MAPKK gene families in Brachypodium distachyon. PLoS One 7(10):e46744

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • Ding HD, Zhang XH, Xu SC, Sun LL, Jiang MY, Zhang AY, Jin YG (2009) Induction of protection against paraquat-induced oxidative damage by abscisic acid in maize leaves is mediated through mitogen-activated protein kinase. J Integr Plant Biol 51:961–972

    Article  CAS  PubMed  Google Scholar 

  • Dóczi R, Brader G, Pettkó-Szandtner A, Rajh I, Djamei A, Pitzschke A, Teige M, Hirt H (2007) The Arabidopsis mitogen-activated protein kinase kinase MKK3 is upstream of group C mitogen-activated protein kinases and participates in pathogen signaling. Plant Cell 19:3266–3279

    Article  PubMed Central  PubMed  Google Scholar 

  • Droillard M, Boudsocq M, Barbier-Brygoo H, Laurière C (2002) Different protein kinase families are activated by osmotic stresses in Arabidopsis thaliana cell suspensions. Involvement of the MAP kinases AtMPK3 and AtMPK6. FEBS Lett 527:43–50

    Article  CAS  PubMed  Google Scholar 

  • Droillard MJ, Boudsocq M, Barbier-Brygoo H, Lauriere C (2004) Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of A. thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 574:42–48

    Article  CAS  PubMed  Google Scholar 

  • Dutta A, Sen J, Deswal R (2013) New evidences about stritosidine synthase (Str) regulation by salinity, cold stress and nitric oxide in Cathatranthus roseus. J Plant Biochem Biotechnol 22(1):124–131

    Article  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Gupta M, Sharma P, Sarin NB, Sinha AK (2009) Differential response of arsenic stress in two varieties of Brassica juncea L. Chemosphere 74:1201–1208

    Article  CAS  PubMed  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(4):192–198

    Article  CAS  PubMed  Google Scholar 

  • Huang X-S, Luo T, Fu X-Z, Fan Q-J, Liu J-H (2011) Cloning and molecular characterization of a mitogen-activated protein kinase gene from Poncirus trifoliata whose ectopic expression confers dehydration/drought tolerance in transgenic tobacco. J Exp Bot 62(14):5191–5206

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jonak C, Okrész L, Bögre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signalling. Curr Opin Plant Biol 5:415–424

    Article  CAS  PubMed  Google Scholar 

  • Jonak C, Nakagami H, Hirt H (2004) Heavy metal stress. Activation of distinct mitogen-activated protein kinase pathways by copper and cadmium. Plant Physiol 136:3276–3283

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Karin M (1998) Mitogen-activated protein kinase cascades as regulators of stress responses. Ann N Y Acad Sci 851:139–146

    Article  CAS  PubMed  Google Scholar 

  • Kong X, Sun L, Zhou Y, Zhang M, Liu Y, Pan J, Li D (2011) ZmMKK4 regulates osmotic stress through reactive oxygen species scavenging in transgenic tobacco. Plant Cell Rep 30:2097–2104

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔC T method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Mészáros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G, Bardóczy V, Teige M, Koncz C, Peck S, Bögre L (2006) The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J 48:485–498

    Article  PubMed  Google Scholar 

  • 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 

  • 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 U S A 93:765–769

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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 

  • Poyraz I (2013) Molecular cloning and characterization of a mitogen-activated protein kinase kinase (OoMAPKK1) in Origanum omits L. (Lamiaceae). J Plant Biochem Biotechnol. doi:10.1007/s13562-013-0238-2

    Google Scholar 

  • Qiu JL et al (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rao KP, Richa T, Kumar K, Raghuram B, Sinha AK (2010a) In silico analysis reveals 75 members of mitogen-activated protein kinase kinase kinase gene family in rice. DNA Res 17(3):139–153

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rao KP, Vani G, Kumar K, Wankhede DP, Mishra M, Gupta M, Sinha AK (2010b) Arsenic stress activates MAP kinase in rice roots and leaves. Arch Biochem Biophys 506:73–82

    Article  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 

  • Shi J, An HL, Zhang L, Gao Z, Guo XQ (2010) GhMPK7, a novel multiple stress-responsive cotton group C MAPK gene, has a role in broad spectrum disease resistance and plant development. Plant Mol Biol 74:1–17

    Article  CAS  PubMed  Google Scholar 

  • Singh A, Pandey GK (2012) Protein phosphotases: a genomic outlook to understand their function in plants. J Plant Biochem Biotechnol. doi:10.1007/s13562-012-0150-1

    PubMed Central  PubMed  Google Scholar 

  • Sinha AK, Jaggi M, Raghuram B, Tuteja N (2011) Mitogen-activated protein kinase signaling in plants under abiotic stress. Plant Signal Behav 6(2):196–203

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sun Z-H, Ding C-H, Li X-M, Xiao K (2012) Molecular characterization and expression analysis of TaZFP15, a C2H2– type zinc finger transcription factor gene in wheat (Triticum aestivum L.). J Integr Agric 11(1):31–42

    Article  CAS  Google Scholar 

  • Takabe T (2012) Engineering of betaine biosynthesis and transport for abiotic stress tolerance in plants. J Plant Biochem Biotechnol 21(Suppl 1):S58–S62

    Article  Google Scholar 

  • Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2007) The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19:805–818

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Teige M, Scheikl E, Eulgem T, Dóczi 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 

  • Tena G, Asai T, Chiu WL, Sheen J (2001) Plant mitogen-activated protein kinase signaling cascades. Curr Opin Plant Biol 4:392–400

    Article  CAS  PubMed  Google Scholar 

  • The International Brachypodium Initiative (2010) Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463(7282):763–768

    Article  Google Scholar 

  • Wang C, Song W (2013) ZmCK3, a maize calcium-dependent protein kinase gene, endows tolerance to drought and heat stresses in transgenic Arabidopsis. J Plant Biochem Biotechnol. doi:10.1007/s13562-013-0208-8

    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 Central  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 

  • Whitmarsh AJ, Davis RJ (1998) Structural organization of MAP-kinase signaling modules by scaffold proteins in yeast and mammals. Trends Biochem Sci 23:481–485

    Article  CAS  PubMed  Google Scholar 

  • Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yeh CM, Hsiao LJ, Huang HJ (2004) Cadmium activates a mitogen-activated protein kinase gene and MBP kinases in rice. Plant Cell Physiol 45:1306–1312

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Zhang L, Li Y, Lu W, Meng F, Wu C, Guo X (2012) Cotton GhMKK5 affects disease resistance, induces HR-like cell death, and reduces the tolerance to salt and drought stress in transgenic Nicotiana benthamiana. J Exp Bot 63(10):3935–3951

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao X, Liu X, Guo C, Gu J, Xiao K (2013) Identification and characterization of microRNAs from wheat (Triticum aestivum L.) under phosphorus deprivation. J Plant Biochem Biotechnol 22(1):113–123

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Science Foundation of China (grant nos. 31201674 and 31371618), the National Transgenic Major Program (grant no. 2011ZX08008), and Key Laboratory of Crop Growth Regulation of Hebei Province. The authors thank two anonymous reviewers and the editor whose detailed comments and careful work helped to improve the manuscript.

Author information

Authors and Affiliations

  1. College of Agronomy, Agricultural University of Hebei, Baoding, 071001, People’s Republic of China

    Chengjin Guo, Chunying Ma, Weiwei Duan & Kai Xiao

  2. College of Life Sciences, Agricultural University of Hebei, Baoding, 071001, People’s Republic of China

    Yanli Wen, Xiaojuan Li & Wenjing Lu

Authors
  1. Yanli Wen
    View author publications

    Search author on:PubMed Google Scholar

  2. Xiaojuan Li
    View author publications

    Search author on:PubMed Google Scholar

  3. Chengjin Guo
    View author publications

    Search author on:PubMed Google Scholar

  4. Chunying Ma
    View author publications

    Search author on:PubMed Google Scholar

  5. Weiwei Duan
    View author publications

    Search author on:PubMed Google Scholar

  6. Wenjing Lu
    View author publications

    Search author on:PubMed Google Scholar

  7. Kai Xiao
    View author publications

    Search author on:PubMed Google Scholar

Corresponding authors

Correspondence to Wenjing Lu or Kai Xiao.

Additional information

Yanli Wen and Xiaojuan Li contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online Supplemental Table 1

(DOC 50 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wen, Y., Li, X., Guo, C. et al. Characterization and expression analysis of mitogen-activated protein kinase cascade genes in wheat subjected to phosphorus and nitrogen deprivation, high salinity, and drought. J. Plant Biochem. Biotechnol. 24, 184–196 (2015). https://doi.org/10.1007/s13562-014-0256-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13562-014-0256-8

Keywords