Skip to main content
SpringerLink
Log in

Response of TaFLR MAPKKK to wheat leaf rust and Fusarium head blight and the activation of downstream components

  • Original Article
  • Published:
Tropical Plant Pathology Aims and scope Submit manuscript

Abstract

Mitogen-activated protein kinase pathways form a key network in plant defense responses. Gene array analysis has indicated that many members of the MAPK pathway in host plants are regulated in response to pathogen attack. TaFLR (wheat Fusarium and Leaf Rust Response, a wheat MAP kinase kinase kinase gene) was transcriptionally up-regulated during the early interactions of wheat and the leaf rust pathogen, Puccinia triticina. Infection with Fusarium graminearum also activated this kinase gene. Analysis of the background transcript levels in sixteen different wheat cultivars showed no correlation between the transcriptional level of TaFLR and the resistance phenotypes to Fusarium head blight. Transient expression of TaFLR in protoplasts activated pathogenesis-related genes β-1,3-glucanase and chitinase. While the level of TaFLRS gene (wheat Fusarium and Leaf Rust Sensitive, a wheat MAP kinase) remained unchanged at the translational level, the kinase protein was highly phosphorylated. Ectopic expression of TaFLR in tomato plants enhanced resistance against the bacterial pathogen Pseudomonas syringae pv. tomato. Our findings suggest that TaFLR may activate defense response pathways and this activation could involve the phosphorylation of TaFLRS.

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

Similar content being viewed by others

References

  • Alsaiari S (2012) Functional analysis of FLRS and TaFLR in wheat during abiotic stresses. MSc Thesis, Carleton University. Ottawa

  • 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 

  • Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276:726–733

    Article  CAS  PubMed  Google Scholar 

  • Benschop JJ, Mohammed S, O’Flaherty M, Heck AJ, Slijper M, Menke FL (2007) Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Molec Cell Proteomics 6:1198–1214

    Article  CAS  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  CAS  PubMed  Google Scholar 

  • Chetouhi C, Bonhomme L, Lecomte P, Cambon F, Merlino M, Biron DG, Langin T (2015) A proteomics survey on wheat susceptibility to Fusarium head blight during grain development. Europ J Plant Pathol 141:407–418

    Article  CAS  Google Scholar 

  • Cvetkovska M, Rampitsch C, Bykova N, Xing T (2005) Genomic analysis of MAP kinase cascades in Arabidopsis defense responses. Plant Mol Biol Report 23:331–343

    Article  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  CAS  PubMed  Google Scholar 

  • del Pozo O, Pedley KF, Martin GB (2004) MAPKKKalpha is a positive regulator of cell death associated with both plant immunity and disease. EMBO J 23:3072–3082

    Article  PubMed Central  PubMed  Google Scholar 

  • Fan T, Gao Y, Al-Shammari A, Wang XJ, Xing T (2009) Yeast two-hybrid screening of MAP kinase cascade identifies cytosolic glutamine synthetase 1b as a tMEK2 interactive protein in wheat. Can J Plant Pathol 31:407–414

    Article  CAS  Google Scholar 

  • Fofana B, Banks TW, McCallum B et al. (2007) Temporal gene expression profiling of the wheat leaf rust pathosystem using cDNA microarray reveals differences in compatible and incompatible defence pathways. Int J Plant Genom 17542. doi: 10.1155/2007/17542

  • Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947–956

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frye CA, Tang D, Innes RW (2001) Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc Natl Acad Sci U S A 98:373–378

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fujita M, Fujita Y, Noutoshi Y, Takahashi F, Narusaka Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr Opin Plant Biol 9:436–442

    Article  PubMed  Google Scholar 

  • Gao Y, Liu X, Stebbing J, He D, Laroche A, Gaudet DA, Xing T (2011) TaFLRS, a novel mitogen-activated protein kinase in wheat defence responses. Eur J Plant Pathol 131:643–651

    Article  CAS  Google Scholar 

  • Gilbert J, Jordan M, Somers D, Xing T, Punja ZK (2006) Engineering plants for durable disease resistance. In: Tuzun S, Bent E (eds) Multigenic and induced systemic resistance in plants. Springer, New York, pp 415–455

    Chapter  Google Scholar 

  • Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Ann Bot 80:713–720

    Article  CAS  Google Scholar 

  • Hoch HC, Staples RC (1987) Structural and chemical changes among the rust fungi during appressorium development. Annu Rev Phytopathol 25:231–247

    Article  Google Scholar 

  • Ichimura K, Mizoguchi T, Shinozaki K (1997) ATMRK1, an Arabidopsis protein kinase related to mammal mixed-lineage kinases and Raf protein kinases. Plant Sci 130:171–179

    Article  CAS  Google Scholar 

  • Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activated Arabidopsis MAP kinases AtMPK4 and AtMPK6. Plant J 24:655–665

    Article  CAS  PubMed  Google Scholar 

  • Jin H, Axtell MJ, Dahlbeck D, Ekwenna O, Zhang S, Staskawicz B, Baker B (2002) NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants. Dev Cell 3:291–297

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jordan M, Cloutier S, Somers D, Procunier D, Rampitsch C, Xing T (2006) Beyond R genes: dissecting disease-resistance pathways using genomics and proteomics. Can J Plant Pathol 28:S228–S232

    Article  CAS  Google Scholar 

  • Ju C, Yoon GM, Shemansky JM, Lin DY, Ying ZI, Chang J, Garrett WM, Kessenbrock M, Groth G, Tucker ML, Cooper B, Kieber JJ, Chang C (2012) CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc Natl Acad Sci U S A 109:19486–19491

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kieber JJ, Rothenberg M, Roman G, Feldmann KA, Ecker JR (1993) CTR1, a negative regulator of the ethylene response pathway in Arabidopsis, encodes a member of the raf family of protein kinases. Cell 72:427–441

    Article  CAS  PubMed  Google Scholar 

  • Kolmer JA (1996) Genetics of resistance to wheat leaf rust. Annu Rev Phytopathol 34:435–455

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Rudd JJ, Macioszek VK, Scheel D (2004) Dynamic changes in the localization of MAP kinase cascade components controlling pathogenesis-related (PR) gene expression during innate immunity in parsley. J Biol Chem 279:22440–22448

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Schiff M, Dinesh-Kumar SP (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J 38:800–809

    Article  CAS  PubMed  Google Scholar 

  • Marcel TC, Aghnoum R, Durand J, Varshney RK, Niks RE (2007) Dissection of the barley 2L1.0 region carrying the ‘Laevigatum’ quantitative resistance gene to leaf rust using near-isogenic lines (NIL) and subNIL. Molec Plant-Microbe Interact 20:1604–1615

    Article  CAS  Google Scholar 

  • Mardi M, Pazouki L, Delavar H, Kazemi MB, Ghareyazie B, Steiner B, Nolz R, Lemmens M, Buerstmayr H (2006) QTL analysis of resistance to Fusarium head blight in wheat using a ‘Frontana’‐derived population. Plant Breed 125:313–317

    Article  Google Scholar 

  • Melech-Bonfil S, Sessa G (2010) Tomato MAPKKKepsilon is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J 64:379–391

    Article  CAS  PubMed  Google Scholar 

  • Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266

    Article  CAS  PubMed  Google Scholar 

  • Menke FL, van Pelt JA, Pieterse CM, Klessig DF (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16:897–907

    Article  PubMed Central  CAS  PubMed  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 

  • Oh CS, Pedley KF, Martin GB (2010) Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK α. Plant Cell 22:260–272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Peck SC (2003) Early phosphorylation events in biotic stress. Curr Opin Plant Biol 6:334–338

    Article  CAS  PubMed  Google Scholar 

  • Peck SC, Nuhse TS, Hess D, Iglesias A, Meins F, Boller T (2001) Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell 13:1467–1475

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Plett JM, Cvetkovska M, Makenson P, Xing T, Regan S (2009) Arabidopsis ethylene receptors have different roles in Fumonisin B1-induced cell death. Physiol Mol Plant Pathol 74:18–26

    Article  CAS  Google Scholar 

  • Qiao H, Shen Z, Huang SS, Schmitz RJ, Urich MA, Briggs SP, Ecker JR (2012) Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338:390–393

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rudd JJ, Keon J, Hammond-Kosack KE (2008) The wheat mitogen-activated protein kinases TaMPK3 and TaMPK6 are differentially regulated at multiple levels during compatible disease interactions with Mycosphaerella graminicola. Plant Physiol 147:802–815

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning—a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Stubbs RW, Prescott JM, Saari EE, Dubin HJ (1986) Cereal disease methodology manual. CIMMYT, Mexico City

    Google Scholar 

  • Stulemeijer IJE, Stratmann JW, Joosten M (2007) Tomato mitogen-activated protein kinases LeMPK1, LeMPK2, and LeMPK3 are activated during the Cf-4/Avr4-induced hypersensitive response and have distinct phosphorylation specificities. Plant Physiol 144:1481–1494

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tang DZ, Christiansen KM, Innes RW (2005) Regulation of plant disease resistance, stress responses, cell death, and ethylene signaling in Arabidopsis by the EDR1 protein kinase. Plant Physiol 138:1018–1026

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tregear JW, Jouannic S, Schwebel-Dugue N, Kreis M (1996) An unusual protein kinase displaying characteristics of both the serine/threonine kinase and tyrosine families is encoded by the Arabidopsis thaliana gene ATN1. Plant Sci 117:107–119

    Article  CAS  Google Scholar 

  • Xiao J, Jin X, Jia X, Wang H, Cao A, Zhao W, Pei W, Xue Z, He L, Chen Q, Wang X (2013) Transcriptome-based discovery of pathways and genes related to resistance against Fusarium head blight in wheat landrace Wangshuibai. BMC Genomics 14:197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xing T, Laroche A (2011) Revealing plant defense signaling—getting more sophisticated with phosphoproteomics. Plant Signal Behav 6:1–6

    Article  Google Scholar 

  • Xing T, Malik K, Martin T, Miki BL (2001) Activation of tomato PR and wound-related genes by a mutagenized tomato MAP kinase kinase through divergent pathways. Plant Mol Biol 46:109–120

    Article  CAS  PubMed  Google Scholar 

  • Xing T, Ouellet T, Miki BL (2002) Towards genomic and proteomic studies of protein phosphorylation in plant-pathogen interactions. Trends Plant Sci 7:224–230

    Article  CAS  PubMed  Google Scholar 

  • Xing T, Rampitsch C, Miki BL, Mauthe W, Stebbing J, Malik K, Jordan M (2003) MALDI-Qq-TOF-MS and transient gene expression analysis indicated co-enhancement of ß-1,3-glucanase and endochitinase by tMEK2 and the involvement of divergent pathways. Physiol Mol Plant Pathol 62:209–217

    Article  CAS  Google Scholar 

  • Xing T, Rampitsch C, Sun S, Romanowski A, Conroy C, Stebbing J, Wang XJ (2008) TAB2, a nucleoside diphosphate protein kinase, is a component of the tMEK2 disease resistance pathway in tomato. Physiol Mol Plant Pathol 73:33–39

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a NSERC Discovery grant, an Agriculture and Agri-Food Canada Genomics Initiative grant and an Agricultural Bioproducts Innovation Program grant to T.X. We thank Drs. Jeannie Gilbert, Brent McCallum and Thérèse Ouellet from Agriculture and Agri-Food Canada for their support. The authors declare that there are no conflicts of interest regarding the publication of this article.

Author information

Authors and Affiliations

  1. Department of Biology and Institute of Biochemistry, Carleton University, Ottawa, Canada, K1S 5B6

    Y. Gao, K. Tubei & T. Xing

  2. Cereal Research Centre, Agriculture and Agri-Food Canada, Winnipeg, MB, Canada, R3T 2M9

    J. Stebbing

  3. Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, London, ON, Canada, N5V 4T3

    L. N. Tian

  4. Fredericton Research and Development Centre, Agriculture and Agri-Food Canada, Fredericton, NB, Canada, E3B 4Z7

    X. Q. Li

Authors
  1. Y. Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Stebbing
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. K. Tubei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. N. Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. X. Q. Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. T. Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to T. Xing.

Additional information

Section Editor: F. Murilo Zerbini

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gao, Y., Stebbing, J., Tubei, K. et al. Response of TaFLR MAPKKK to wheat leaf rust and Fusarium head blight and the activation of downstream components. Trop. plant pathol. 41, 15–23 (2016). https://doi.org/10.1007/s40858-015-0063-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40858-015-0063-3

Keywords

Search

Navigation