Proton extrusion is an essential signalling component in the HR of epidermal single cells in the barley-powdery mildew interaction

Plant Journal

Volumn 23, Issue 2, 2000, Pages 245-254

  Zhou, Fasong ^a,b   Andersen, Claus H ^a,c   Burhenne, Kim ^a   Fischer, Pernille Hertz ^a   Collinge, David B ^a   Thordal Christensen, Hans ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b SAINSBURY LABORATORY   (United Kingdom)

^c DLF Trifolium AS   (Denmark)

Author keywords

Blumeria graminis; Fusicoccin; H2O2; Hypersensitive response; PH; Proton pump

Indexed keywords

ACIDIFICATION; APOPLAST; BARLEY; BIOCHEMICAL PATHWAY; BUFFER; CELL ACTIVATION; CELL MEMBRANE; CITRIC ACID; EPIDERMIS CELL; FUSICOCCIN; HYDROGEN PEROXIDE; HYPERSENSITIVITY REACTION; MESOPHYLL CELL; MODEL; PH; POWDERY MILDEW; SUCCINIC ACID;

ASCOMYCOTA; HORDEUM; HYDROGEN PEROXIDE; PROTON-TRANSLOCATING ATPASES; SIGNAL TRANSDUCTION;

BLUMERIA GRAMINIS; ERYSIPHALES; FUNGI; HORDEUM VULGARE SUBSP. VULGARE;

EID: 0033898236     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2000.00777.x     Document Type: Article

References (58)

1. Aarts, N., Metz, M., Holub, E., Staskawicz, B.J., Daniels, M.J. and Parker, J.E. (1998) Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc. Natl Acad. Sci. USA, 95, 10306-10311.
2. Abad, M.S., Hakimi, S.M., Kaniewski, W.K., Rommens, C.M., Shulaev, V., Lam, E. and Shah, D.M. (1997) Characterization of acquired resistance in lesion-mimic transgenic potato expressing bacterio-opsin. Mol. Plant-Microbe Interact. 10, 635-645.
3. Aist, J.R. and Bushnell, W.R. (1991) Invasion of plants by powdery mildew fungi and cellular mechanisms of the resistance. In The Fungal Spore and Disease Initiation in Plants and Animals (Cole, G.T. and Hoch, H.C., eds). New York: Plenum Press, pp. 321-345.
4. Aist, J.R. and Israel, H.W. (1977) Papilla formation: timing and significance during penetration of barley coleoptiles by Erysiphe graminis hordei. Phytopathology, 67, 455-461.
5. Alvarez, M.E., Pennell, R.I., Meijer, P.J., Ishikawa, A., Dixon, R.A. and Lamb, C. (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell, 92, 773-784.
6. +-ATPase to generate a fusicoccin binding complex and a fusicoccin responsive system. Plant J. 13, 661-671.
7. Boyd, L.A., Smith, P.H., Foster, E.M. and Brown, J.K.M. (1995) The effects of allelic variation at the Mla resistance locus in barley on the early development of Erysiphe graminis f.sp. hordei and host responses. Plant J. 7, 959-968.
8. Brandt, J., Thordal-Christensen, H., Vad, K., Gregersen, P.L. and Collinge, D.B. (1992) A pathogen-induced gene of barley encodes a protein showing high similarity to a protein kinase regulator. Plant J. 2, 815-820.
9. Bushnell, W.R. (1981) Incompatibility conditioned by the Mla gene in powdery mildew of barley: the halt in cytoplasmic streaming. Phytopathology, 71, 1062-1066.
10. Century, K.S., Shapiro, A.D., Repetti, P.P., Dahlbeck, D., Holub, E. and Staskawicz, B.J. (1997) NDR1, a pathogen-induced component required for Arabidopsis disease resistance. Science, 278, 1963-1965.
11. Dangl, J.L., Dietrich, R.A. and Richberg, M.H. (1996) Death don't have no mercy: cell death programs in plant-microbe interactions. Plant Cell, 8, 1793-1807.
12. Delaney, T.P., Uknes, S., Vernooij, B. et al. (1994) A central role of salicylic acid in plant disease resistance. Science, 266, 1247-1250.
13. Delledonne, M., Xia, Y., Dixon, R.A. and Lamb, C. (1998) Nitric oxide functions as a signal in plant disease resistance. Nature, 394, 585-588.
14. - generating system in plasma membrane-rich fraction of potato tuber tissues by treatment with an elicitor from Phytophthora infestans or with digetonin. Physiol. Mol. Plant Pathol. 46, 17-28.
15. Dumas, B., Freyssinet, G. and Pallett, K.E. (1995) Tissue-specific expression of germin-like oxalate oxidase during development and fungal infection of barley seedlings. Plant Physiol. 107, 1091-1096.
16. Falk, A., Feys, B.J., Frost, L.N., Jones, J.D., Daniels, M.J. and Parker, J.E. (1999) EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proc. Natl Acad. Sci. USA, 96, 3292-3297.
17. Faris, J.D., Li, W.L., Liu, D.J., Chen, P.D. and Gill, B.S. (1999) Candidate gene analysis of quantitative disease resistance in wheat. Theor. Appl. Genet. 98, 219-225.
18. Görg, R., Hollricher, K. and Schulze-Lefert, P. (1993) Functional analysis and RFLP mapping of the Mlg resistance gene in barley. Plant J. 3, 857-866.
19. Gregersen, P.L., Thordal-Christensen, H., Förster, H. and Collinge, D.B. (1997) Differential gene transcript accumulation in barley leaf epidermis and mesophyll in response to attack by Blumeria graminis f.sp. hordei. Physiol. Mol. Plant Pathol. 51, 85-97.
20. Hammond-Kosack, K.E., Tang, S., Harrison, K. and Jones, J.D. (1998) The tomato Cf-9 disease resistance gene functions in tobacco and potato to confer responsiveness to the fungal avirulence gene product avr 9. Plant Cell, 10, 1251-1266.
21. Heath, M.C. (1998a) Apoptosis, programmed cell death and the hypersensitive response. Eur. J. Plant Pathol. 104, 117-124.
22. Heath, M.C. (1998b) Involvement of reactive oxygen species in the response of resistant (hypersensitive) or susceptible cowpeas to the cowpea rust fungus. New Phytol. 138, 251-263.
23. Higgins, V.J., Lu, H., Xing, T., Gelli, A. and Blumwald, E. (1998) The gene-for-gene concept and beyond: interactions and signals. Can. J. Plant Pathol. 20, 150-157.
24. Hurkman, W.J. and Tanaka, C.K. (1996) Germin gene expression is induced in wheat leaves by powdery mildew infection. Plant Physiol. 111, 735-739.
25. Jabs, T. (1999) Reactive oxygen intermediates as mediators of programmed cell death in plants and animals. Biochem. Pharmacol. 57, 231-245.
26. Kato, T., Shiraishi, T., Toyoda, K., Saitoh, K., Satoh, Y., Tahara, M., Yamada, T. and Oku, H. (1993) Inhibition of ATPase activity in pea plasma membrane by fungal suppressors from Mycosphaerella pinodes and their peptide moieties. Plant Cell Physiol. 34, 439-445.
27. Kawasaki, T., Henmi, K., Ono, E., Hatakeyama, S., Iwano, M., Satoh, H. and Shimamoto, K. (1999) The small GTP-binding protein rac is a regulator of cell death in plants. Proc. Natl Acad. Sci. USA, 96, 10922-10926.
28. Knogge, W. (1996) Fungal infection of plants. Plant Cell, 8, 1711-1722.
29. Koga, H., Zeyen, R.J., Bushnell, W.R. and Ahlstrand, G.G. (1988) Hypersensitive cell death, autofluorescence and insoluble silicon accumulation in barley leaf epidermal cells under attack by Erysiphe graminis f.sp. hordei. Physiol. Mol. Plant Pathol. 32, 395-409.
30. Kotsira, V.P. and Clonis, Y.D. (1997) Oxalate oxidase from barley roots: purification to homogeneity and study of some molecular, catalytic and binding properties. Arch. Biochem. Biophys. 340, 239-249.
31. Kølster, P., Munk, L., Stølen, O. and Løhde, J. (1986) Nearisogenic barley lines with genes for resistance to powdery mildew. Crop Sci. 26, 903-907.
32. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 583-593.
33. Levine, A., Pennell, R.I., Alvarez, M.E., Palmer, R. and Lamb, C. (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol. 6, 427-437.
34. Low, P.S. and Merida, J.R. (1996) The oxidative burst in plant defence: function and signal transduction. Physiol. Plant, 96, 533-542.
35. Mittler, R., Shulaev, V. and Lam, E. (1995) Coordinated activation of programmed cell death and defence mechanisms in transgenic tobacco plants expressing a bacterial proton pump. Plant Cell, 7, 29-42.
36. Mittler, R., Herr, E.H., Orvar, B.L., van Camp, W., Willekens, H., Inze, D. and Ellis, B.E. (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc. Natl Acad. Sci. USA 96, 14165-14170.
37. Pike, S.M., Ádám, A.L., Pu, X.A., Hoyos, M.E., Laby, R., Beer, S.V. and Novacky, A. (1998) Effects of Erwinia amylovora harpin on tobacco leaf cell membranes are related to leaf necrosis and electrolyte leakage and distinct from perturbations caused by inoculated E. amylovora. Physiol. Mol. Plant Pathol. 53, 39-60.
38. Roberts, M.R. and Bowles, D.J. (1999) Fusicoccin, 14-3-3 proteins and defence responses in tomato plants. Plant Physiol. 119, 1243-1250.
39. Romeis, T., Piedras, P., Zhang, S., Klessig, D.F., Hirt, H. and Jones, J.D.G. (1999) Rapid Avr 9-and Cf-9-dependent activation of MAP kinases in tobacco cell cultures and leaves: convergence of resistance gene, elicitor, wound, and salicylate responses. Plant Cell, 11, 273-288.
40. Rushton, P.J. and Somssich, I.E. (1999) Transcriptional regulation of plant genes responsive to pathogens and elicitors. In Plant-Microbe Interactions, Vol. 4 (Stacey, G. and Keen, N.T., eds). St Paul, Minnesota: APS Press, pp. 251-274.
41. +-ATPase activity differentially activates wound and pathogen defence responses in tomato plants. Plant Cell, 11, 263-272.
42. Schiffer, R., Gorg, R., Jarosch, B., Beckhove, U., Bahrenberg, G., Kogel, K.-H. and Schulze-Lefert, P. (1997) Tissue dependence and differential cordycepin sensitivity of race-specific resistance responses in the barley-powdery mildew interaction. Mol. Plant-Microbe Interact. 10, 830-839.
43. Scofield, S.R., Tobias, C.M., Rathjen, J.P., Chang, J.H., Lavelle, D.T., Michelmore, R.W. and Staskawicz, B.J. (1996) Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science, 274, 2063-2065.
44. Sessa, G., D'Ascenzo, M. and Martin, G.B. (2000) The major site of the pti1 kinase phosphorylated by the pto kinase is located in the activation domain and is required for pto-pti1 physical interaction. Eur. J. Biochem. 267, 171-178.
45. Shirasu, K., Lahaye, T., Tan, M.W., Zhou, F., Azevedo, C. and Schulze-Lefert, P. (1999) A novel class of eukaryotic zinc-binding proteins is required for disease resistance signaling in barley and development in C. elegans. Cell, 99, 355-366.
46. Simon-Plas, F., Rusterucci, C., Milat, M.L., Humbert, C., Montillet, J.L. and Blein, J.P. (1997) Active oxygen species production in tobacco cells elicited by cryptogein. Plant Cell Environ. 20, 1573-1579.
47. Sugiura, M., Yamamura, H., Hirano, K., Sasaki, M., Morikawa, M. and Tsuboi, M. (1979) Purification and properties of oxalate oxidase from barley seedlings. Chem. Pharm. Bull. 27, 2003-2007.
48. Tang, X., Frederick, R.D., Zhou, J., Halterman, D.A., Jia, Y. and Martin, G.B. (1996) Initiation of plant disease resistance by physical interaction of avrPto and Pto kinase. Science, 274, 2060-2063.
49. Tang, X., Xie, M., Kim, Y.J., Zhou, J., Klessig, D.F. and Martin, G.B. (1999) Overexpression of Pto activates defence responses and confers broad resistance. Plant Cell, 11, 15-30.
50. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
51. Trewavas, A. and Gilroy, S. (1991) Signal transduction in plant cells. Trends Genet. 7, 356-361.
52. +-ATPase by elicitor-induced enzyme dephosphorylation. Plant Physiol. 104, 209-215.
53. +-ATPase by phytotoxic peptides from the fungal pathogen Rhynchosporium secalis. Plant Physiol. 101, 297-301.
54. Wright, A.J. and Heale, J.B. (1988) Host responses to fungal penetration in Erysiphe graminis f.sp. hordei infections in barley. Plant Pathol. 37, 131-140.
55. +-ATPase. Plant Cell, 8, 555-564.
56. 2-producing enzyme, accumulates in barley attacked by the powdery mildew fungus. Plant J. 8, 139-145.
57. Zhou, J., Loh, Y.T., Bressan, R.A. and Martin, G.B. (1995) The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell, 83, 925-935.
58. Zhou, F., Zhang, Z., Gregersen, P.L., Mikkelsen, J.D., de Neergaard, E., Collinge, D.B. and Thordal-Christensen, H. (1998) Molecular characterization of the oxalate oxidase involved in the response of barley to the powdery mildew fungus. Plant Physiol. 117, 33-41.