Tropical Plant Pathology

, Volume 41, Issue 1, pp 15–23 | Cite as

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

  • Y. Gao
  • J. Stebbing
  • K. Tubei
  • L. N. Tian
  • X. Q. Li
  • T. Xing
Original Article

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.

Keywords

Fusarium head blight Leaf rust MAPKKK Plant defense Wheat 

References

  1. Alsaiari S (2012) Functional analysis of FLRS and TaFLR in wheat during abiotic stresses. MSc Thesis, Carleton University. OttawaGoogle Scholar
  2. 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 415:977–983CrossRefPubMedGoogle Scholar
  3. Baker B, Zambryski P, Staskawicz B, Dinesh-Kumar SP (1997) Signaling in plant-microbe interactions. Science 276:726–733CrossRefPubMedGoogle Scholar
  4. 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 6:1198–1214CrossRefGoogle Scholar
  5. 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 42:567–585CrossRefPubMedGoogle Scholar
  6. 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 141:407–418CrossRefGoogle Scholar
  7. Cvetkovska M, Rampitsch C, Bykova N, Xing T (2005) Genomic analysis of MAP kinase cascades in Arabidopsis defense responses. Plant Mol Biol Report 23:331–343CrossRefGoogle Scholar
  8. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833CrossRefPubMedGoogle Scholar
  9. 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 23:3072–3082PubMedCentralCrossRefPubMedGoogle Scholar
  10. 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 31:407–414CrossRefGoogle Scholar
  11. 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
  12. Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947–956PubMedCentralCrossRefPubMedGoogle Scholar
  13. 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 98:373–378PubMedCentralCrossRefPubMedGoogle Scholar
  14. 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 9:436–442CrossRefPubMedGoogle Scholar
  15. 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 131:643–651CrossRefGoogle Scholar
  16. 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 415–455CrossRefGoogle Scholar
  17. Heath MC (1997) Signalling between pathogenic rust fungi and resistant or susceptible host plants. Ann Bot 80:713–720CrossRefGoogle Scholar
  18. Hoch HC, Staples RC (1987) Structural and chemical changes among the rust fungi during appressorium development. Annu Rev Phytopathol 25:231–247CrossRefGoogle Scholar
  19. Ichimura K, Mizoguchi T, Shinozaki K (1997) ATMRK1, an Arabidopsis protein kinase related to mammal mixed-lineage kinases and Raf protein kinases. Plant Sci 130:171–179CrossRefGoogle Scholar
  20. Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K (2000) Various abiotic stresses rapidly activated Arabidopsis MAP kinases AtMPK4 and AtMPK6. Plant J 24:655–665CrossRefPubMedGoogle Scholar
  21. 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 3:291–297CrossRefPubMedGoogle Scholar
  22. Jonak C, Okresz L, Bogre L, Hirt H (2002) Complexity, cross talk and integration of plant MAP kinase signaling. Curr Opin Plant Biol 5:415–424CrossRefPubMedGoogle Scholar
  23. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329CrossRefPubMedGoogle Scholar
  24. 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–S232CrossRefGoogle Scholar
  25. 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 109:19486–19491PubMedCentralCrossRefPubMedGoogle Scholar
  26. 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 72:427–441CrossRefPubMedGoogle Scholar
  27. Kolmer JA (1996) Genetics of resistance to wheat leaf rust. Annu Rev Phytopathol 34:435–455CrossRefPubMedGoogle Scholar
  28. 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 279:22440–22448CrossRefPubMedGoogle Scholar
  29. 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 38:800–809CrossRefPubMedGoogle Scholar
  30. 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 20:1604–1615CrossRefGoogle Scholar
  31. 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 125:313–317CrossRefGoogle Scholar
  32. Melech-Bonfil S, Sessa G (2010) Tomato MAPKKKepsilon is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J 64:379–391CrossRefPubMedGoogle Scholar
  33. Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266CrossRefPubMedGoogle Scholar
  34. 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 16:897–907PubMedCentralCrossRefPubMedGoogle Scholar
  35. Nakagami H, Pitzschke A, Hirt H (2005) Emerging MAP kinase pathways in plant stress signaling. Trends Plant Sci 10:339–346CrossRefPubMedGoogle Scholar
  36. 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 22:260–272PubMedCentralCrossRefPubMedGoogle Scholar
  37. Peck SC (2003) Early phosphorylation events in biotic stress. Curr Opin Plant Biol 6:334–338CrossRefPubMedGoogle Scholar
  38. 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 13:1467–1475PubMedCentralCrossRefPubMedGoogle Scholar
  39. 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 74:18–26CrossRefGoogle Scholar
  40. 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 338:390–393PubMedCentralCrossRefPubMedGoogle Scholar
  41. 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 17:139–153PubMedCentralCrossRefPubMedGoogle Scholar
  42. 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 147:802–815PubMedCentralCrossRefPubMedGoogle Scholar
  43. Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning—a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  44. Stubbs RW, Prescott JM, Saari EE, Dubin HJ (1986) Cereal disease methodology manual. CIMMYT, Mexico CityGoogle Scholar
  45. 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 144:1481–1494PubMedCentralCrossRefPubMedGoogle Scholar
  46. 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 28:2731–2739PubMedCentralCrossRefPubMedGoogle Scholar
  47. 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 138:1018–1026PubMedCentralCrossRefPubMedGoogle Scholar
  48. 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 25:4876–4882PubMedCentralCrossRefPubMedGoogle Scholar
  49. 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 117:107–119CrossRefGoogle Scholar
  50. 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 14:197PubMedCentralCrossRefPubMedGoogle Scholar
  51. Xing T, Laroche A (2011) Revealing plant defense signaling—getting more sophisticated with phosphoproteomics. Plant Signal Behav 6:1–6CrossRefGoogle Scholar
  52. 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 46:109–120CrossRefPubMedGoogle Scholar
  53. Xing T, Ouellet T, Miki BL (2002) Towards genomic and proteomic studies of protein phosphorylation in plant-pathogen interactions. Trends Plant Sci 7:224–230CrossRefPubMedGoogle Scholar
  54. 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 62:209–217CrossRefGoogle Scholar
  55. 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 73:33–39CrossRefGoogle Scholar

Copyright information

© Sociedade Brasileira de Fitopatologia 2015

Authors and Affiliations

  • Y. Gao
    • 1
  • J. Stebbing
    • 2
  • K. Tubei
    • 1
  • L. N. Tian
    • 3
  • X. Q. Li
    • 4
  • T. Xing
    • 1
  1. 1.Department of Biology and Institute of BiochemistryCarleton UniversityOttawaCanada
  2. 2.Cereal Research Centre, Agriculture and Agri-Food CanadaWinnipegCanada
  3. 3.Southern Crop Protection and Food Research CentreAgriculture and Agri-Food CanadaLondonCanada
  4. 4.Fredericton Research and Development CentreAgriculture and Agri-Food CanadaFrederictonCanada

Personalised recommendations