The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f.sp. hordei

Plant Journal

Volumn 41, Issue 2, 2005, Pages 291-303

  Opalski, Krystina S ^a   Schultheiss, Holger ^a   Kogel, Karl Heinz ^a   Hückelhoven, Ralph ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

Actin; MLO; Penetration resistance; Polarity; Small RAC ROP G protein; Susceptibility

Indexed keywords

CELLS; GENES; MICROORGANISMS; MUTAGENESIS; PROTEINS;

ACTIN FILAMENTS; CHEMICAL FIXATION; CYTOSKELETON; HOST PLANTS;

PLANTS (BOTANY);

ACTIN; MLO PROTEIN, HORDEUM VULGARE; RAC PROTEIN; VEGETABLE PROTEIN;

ARTICLE; BARLEY; FUNGUS; GENETICS; METABOLISM; MICROBIOLOGY; MICROFILAMENT; PATHOGENICITY; PLANT EPIDERMIS;

ACTINS; FUNGI; HORDEUM; MICROFILAMENTS; PLANT EPIDERMIS; PLANT PROTEINS; RAC GTP-BINDING PROTEINS;

BARLEY; CELLS; GENES; MICROORGANISMS; MUTATION; PROTEINS;

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

EID: 12844262457     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2004.02292.x     Document Type: Article

References (74)

1. Baluška, F., Šamaj, J., Wojtaszek, P., Volkmann, D. and Menzel, D. (2003) Cytoskeleton-plasma membrane-cell wall continuum in plants. Emerging links revisited. Plant Physiol. 133, 482-491.
2. Büschges, R., Hollricher, K., Panstruga, R. et al. (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell, 88, 695-705.
3. Bushnell, W.A. and Bergquist, S.E. (1975) Aggregation of host cytoplasm and the formation of papillae and haustoria in powdery mildew of barley. Phytopathology, 65, 310-318.
4. 2+ and GTPases. J. Exp. Bot. 54, 83-92.
5. Chen, C.Y., Cheung, A.Y. and Wu, H.M. (2003) Actin-depolymerizing factor mediates Rac/Rop GTPase-regulated pollen tube growth. Plant Cell, 15, 237-249.
6. Cheung, A.Y., Chen, C., Tao, L., Andreyeva, T., Twell, D. and Wu, H.M. (2003) Regulation of pollen tube growth by Rac-like GTP-ases. J. Exp. Bot. 54, 73-81.
7. Collins, N.C., Thordal-Christensen, H., Lipka, V. et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature, 425, 973-977.
8. Devoto, A., Piffanelli, P., Nilsson, I., Wallin, E., Panstruga, R., von Heijne, G. and Schulze-Lefert, P. (1999) Topology, subcellular localisation, and sequence diversity of the Mlo family in plants. J. Biol. Chem. 274, 34993-35004.
9. Dietrich, C. and Maiss, E. (2002) Red fluorescent protein DsRed from Discosoma sp. as a reporter protein in higher plants. Biotechniques, 32, 286, 288-290, 292-293.
10. Felle, H.H., Herrmann, A., Hanstein, S., Hückelhoven, R. and Kogel, K.-H. (2004) Apoplastic pH signalling in barley leaves attacked by the powdery mildew fungus Blumeria graminis f.sp. hordei. Mol. Plant Microbe Interact. 17, 118-123.
11. Foissner, I., Lichtscheidl, I.K. and Wasteneys, G.O. (1996) Actin-based vesicle dynamics and exocytosis during wound wall formation in Characean internodal cells. Cell. Motil. Cytoskeleton, 35, 35-48.
12. Freialdenhoven, A., Peterhänsel, C., Kurth, J., Kreuzaler, F. and Schulze-Lefert, P. (1996) Identification of genes required for the function of non-race-specific mlo resistance to powdery mildew in barley. Plant Cell, 8, 5-14.
13. Fu, Y., Li, H. and Yang, Z. (2002) The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell, 14, 777-794.
14. Furuse, K., Takemoto, D., Doke, N. and Kawakita, K. (1999) Involvement of actin filament association in hypersensitive reactions in potato cells. Physiol. Mol. Plant Pathol. 54, 51-61.
15. Genre, A. and Bonfante, P. (1998) Actin versus tubulin configuration in arbuscule-containing cells from mycorrhizal tobacco roots. New Phytol. 140, 745-752.
16. Genre, A. and Bonfante, P. (2002) Epidermal cells of a symbiosis-defective mutant of Lotus japonicus show altered cytoskeleton organisation in the presence of a mycorrhizal fungus. Protoplasma, 219, 43-50.
17. Ghosh, M., Song, X., Mouneimne, G., Sidani, M., Lawrence, D.S. and Condeelis, J.S. (2004) Cofilin promotes actin polymerization and defines the direction of cell motility. Science, 304, 743-746.
18. Gross, P., Julius, C., Schmelzer, E. and Hahlbrock, K. (1993) Translocation of cytoplasm and nucleus to fungal penetration sites is associated with depolymerization of microtubules and defense gene activation in infected, cultured parsely cells. EMBO J. 12, 1735-1744.
19. Hazen, B.E. and Bushnell, W.E. (1983) Inhibition of the hypersensitive reaction in barley to powdery mildew by heat shock and cytochalasin B. Physiol. Plant Pathol. 23, 421-438.
20. Hückelhoven, R. and Kogel, K.-H. (1998) Tissue-specific superoxide generation at interaction sites in resistant and susceptible near-isogenic barley lines attacked by the powdery mildew fungus (Erysiphe graminis f.sp. hordei). Mol. Plant Microbe Interact. 11, 292-300.
21. Hückelhoven, R. and Kogel, K.-H. (2003) Reactive oxygen intermediates in plant-microbe interactions: Who is who in powdery mildew resistance? Planta, 216, 891-902.
22. 2 but not with salicylic acid accumulation. Plant Physiol. 119, 1251-1260.
23. Hückelhoven, R., Trujillo, M. and Kogel, K.-H. (2000) Mutations in Ror1 and Ror2 genes cause modification of hydrogen peroxide accumulation in mlo-barley under attack from the powdery mildew fungus. Mol. Plant Pathol. 1, 287-292.
24. Hückelhoven, R., Dechert, C. and Kogel, K.-H. (2003) Overexpression of barley BAX inhibitor 1 induces breakdown of mlo-mediated penetration resistance to Blumeria graminis. Proc. Natl Acad. Sci. USA, 100, 5555-5560.
25. Jacobs, A.K., Lipka, V., Burton, R.A., Panstruga, R., Strizhov, N., Schulza-Lefert, P. and Fincher, G.B. (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell, 15, 2503-2513.
26. Jarosch, B., Kogel, K.-H. and Schaffrath, U. (1999) The ambivalence of the barley Mlo locus: mutations conferring resistance against powdery mildew (Blumeria graminis f.sp. hordei) enhance susceptibility to the rice blast fungus Magnaporthe grisea. Mol. Plant Microbe Interact. 12, 508-514.
27. Jones, M.A., Shen, J.-J., Fu, Y., Li, H., Yang, Z. and Grierson, C.S. (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell, 14, 763-776.
28. Jørgensen, J.H. (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica, 63, 141-152.
29. Kim, M.C., Panstruga, R., Elliott, C., Muller, J., Devoto, A., Yoon, H.W., Park, H.C., Cho, M.J. and Schulze-Lefert, P. (2002) Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature, 416, 447-451
30. Kita, N., Toyoda, H. and Shishiyama, J. (1981) Chronological analysis of cytological responses in powdery-mildewed barley leaves. Can. J. Bot. 59, 1761-1768.
31. Knodler, L.A., Celli, J. and Finlay, B.B. (2001) Pathogenic trickery: deception of host cell processes. Nat. Rev. Mol. Cell Biol. 2, 578-588.
32. Kobayashi, I. and Hakuno, H. (2003) Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta, 217, 340-345.
33. Kobayashi, I., Kobayashi, Y., Yamoka, N. and Kunoh, H. (1992) Recognition of a pathogen and a nonpathogen by barley coleoptile cells. III. Response of microtubules and actin microfilaments in barley coleoptile cells to penetration attempts. Can. J. Bot. 69, 1815-1823.
34. Kobayashi, I., Kabayashi, Y. and Hardham, A.R. (1994) Dynamic reorganization of microtubules and microfilaments in flax cells during the resistance response to flax rust infection. Planta, 195, 237-247.
35. Kobayashi, Y., Kobayashi, I., Funaki, Y., Fujimoto, S., Takemoto, T. and Kunoh, H. (1997a) Dynamic reorganization of microfilaments and microtubules is necessary for the expression of non-host resistance in barley coleoptile cells. Plant J. 11, 525-537.
36. Kobayashi, Y., Yamada, M., Kobayashi, I. and Kunoh, H. (1997b) Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant Cell Physiol. 38, 725-733.
37. Koga, H., Bushnell, W.R. and Zeyen, R.J. (1990) Specificity of cell type and timing of events associated with papilla formation and the hypersensitive reaction in leaves of Hordeum vulgare attacked by Erysiphe graminis f.sp. hordei. Can. J. Bot. 68, 2344-2352.
38. Kølster, P., Munk, L., Stølen, O. and Løhde, J. (1986) Near-isogenic barley lines with genes for resistance to powdery mildew. Crop Sci. 26, 903-907.
39. Kost, B., Lemichez, E., Spielhofer, P., Hong, Y., Tolias, K., Carpenter, C. and Chua, N.H. (1999) Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J. Cell Biol. 145, 317-330.
40. Lemichez, E., Wu, Y., Sanchez, J.P., Mettouchi, A., Mathur, J. and Chua, N.H. (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev. 15, 1808-1816.
41. Li, H., Lin, Y., Heath, R.M., Zhu, M.X. and Yang, Z. (1999) Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell, 11, 1731-1742.
42. Mathur, J. and Hülskamp, M. (2002) Microtubules and microfilaments in cell morphogenesis in higher plants. Curr. Biol. 12, R669-R676.
43. McLusky, S.R., Bennett, M.H., Beale, M.H., Lewis, M.J., Gaskin, P. and Mansfield, J.W. (1999) Cell wall alterations and localized accumulation of feruloyl-3-methoxytyramine in onion epidermis at sites of attempted penetration by Botrytis allii are associated with actin polarisation, peroxidase activity and suppression of flavonoid biosynthesis. Plant J. 17, 523-534.
44. 2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J. 29, 257-268.
45. Molendijk, A.J., Bischoff, F., Rajendrakumar, C.S.V., Friml, J., Braun, M., Gilroy, S. and Palme, K. (2001) Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J. 20, 2779-2788.
46. Nishimura, M.T., Stein, M., Hou, B.H., Vogel, J.P., Edwards, H. and Somerville, S.C. (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science, 301, 969-972.
47. Parniske, M. (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr. Opin. Plant Biol. 3, 320-328.
48. Piffanelli, P., Zhou, F., Casais, C., Orme, J., Jarosch, B., Schaffrath, U., Collins, N.C., Panstruga, R. and Schulze-Lefert, P. (2002) The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol. 129, 1076-1085
49. von Röpenack, E., Parr, A. and Schulze-Lefert, P. (1998) Structural analyses and dynamics of soluble and cell wall-bound phenolics in a broad spectrum resistance to the powdery mildew fungus in barley. J. Biol. Chem. 272, 9013-9022.
50. Schmelzer, E. (2002) Cell polarization, a crucial process in fungal defence. Trends Plant Sci. 7, 411-415.
51. Schultheiss, H., Dechert, C., Kogel, K.-H. and Hückelhoven, R. (2002) A Small GTP-binding host protein is required for entry of powdery mildew fungus into epidermal cells of barley. Plant Physiol. 128, 1447-1454.
52. Schultheiss, H., Dechert, C., Kogel, K.-H. and Hückelhoven, R. (2003) Functional analysis of barley RAC/ROP G-protein family members in susceptibility to the powdery mildew fungus. Plant J. 36, 589-601.
53. Schulze-Lefert, P. (2004) Knocking on the heaven's wall: pathogenesis of and resistance to biotrophic fungi at the cell wall. Curr. Opin. Plant Biol. 7, 377-383.
54. Schulze-Lefert, P. and Panstruga, R. (2003) Establishment of biotrophy by parasitic fungi and reprogramming of host cells for disease resistance. Annu. Rev. Phytopathol. 41, 641-667.
55. Schweizer, P., Pokorny, J., Abderhalden, O. and Dudler, R. (1999) A transient assay system for the functional assessment of defense-related genes in wheat. Mol. Plant Microbe Interact. 12, 647-654.
56. Schweizer, P., Pokorny, J., Schulze-Lefert, P. and Dudler, R. (2000) Double-stranded RNA interferes with gene function at the single-cell level in cereals. Plant J. 24, 895-903.
57. Škalamera, D. and Heath, M. (1998) Changes in the cytoskeleton accompanying infection-induced nuclear movements and the hypersensitive response in plant cells invaded by rust fungi. Plant J. 16, 191-200.
58. Škalamera, D., Jibodh, S. and Heath, M.C. (1997) Callose deposition during the interaction between cowpea (Vigna unguiculata) and the monokaryotic stage of the cowpea rust fungus (Uromyces vignae). New Phytol. 136, 511-524.
59. Staiger, C.J. (2000) Signaling to the actin cytoskeleton in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 257-288.
60. Stein, M. and Somerville, S. (2002) MLO, a novel modulator of plant defenses and cell death, binds calmodulin. Trends Plant Sci. 7, 379-380.
61. Stolzenburg, M.C., Aist, J.R. and Israel, H.W. (1984) The role of papillae in resistance to powdery mildew conditioned by the ml-o gene in barley. I Correlative evidence. Physiol. Plant Pathol. 25, 337-346.
62. Symons, M. and Rusk, N. (2003) Control of vesicular trafficking by Rho GTPases. Curr. Biol. 13, R409-R418.
63. Takemoto, D., Maeda, H., Yoshioka, H., Doke, N. and Kawakita, K. (1999) Effect of cytochalasin D on defense responses of potato tuber discs treated with hyphal wall components of Phytophthora infestans. Plant Sci. 141, 219-226.
64. Takemoto, D., Jones, D.A. and Hardham, A.R. (2003) GFP-tagging of cell components reveals the dynamics of subcellular re-organization in response to infection of Arabidopsis by oomycete pathogens. Plant J. 33, 775-792.
65. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
66. Valster, A.H., Hepler, P.K. and Chernoff, J. (2000) Plant GTPases: the Rhos in bloom. Trends Cell Biol. 10, 141-146.
67. Volkmann, D. and Baluška, F. (1999) Actin cytoskeleton in plants: from transport networks to signaling networks. Microsc. Res. Tech. 47, 135-154.
68. Vorwerk, S., Somerville, S. and Somerville, C. (2004) The role of plant cell wall polysaccharide composition in disease resistance. Trends Plant Sci. 9, 203-209.
69. Wasteneys, G.O. and Galway, M.E. (2003) Remodelling the cytoskeleton for growth and form: an overview with some new views. Annu. Rev. Plant Biol. 54, 691-722.
70. Wolter, M., Hollricher, K., Salamini, F. and Schulze-Lefert, P. (1993) The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol. Gen. Genet. 239, 122-128.
71. Xu, J.R., Staiger, C.J. and Hamer, J.E. (1998) Inactivation of the mitogen-activated protein kinase Mps1 from rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. Proc. Natl Acad. Sci. USA, 95, 12713-12718.
72. Yang, Z. (2002) Small GTPases: versatile signaling switches in plants. Plant Cell, 14 (Suppl.), 375-388.
73. Yun, B.-W., Atkinson, H.A., Gaborit, C., Greenland, A., Read, N.D., Pallas, J.A. and Loake, G.J. (2003) Loss of actin cytoskeletal function and EDS1 activity, in combination, severely compromises non-host resistance in Arabidopsis against wheat powdery mildew. Plant J. 34, 768-777.
74. Zeyen, R.J., Carver, T.L.W. and Lyngkjaer, M.F. (2002) Epidermal cell papillae. In The Powdery Mildews (Bélanger, R.R., Bushnell, W.R., Dik, A.J. and Carver, T.L.W., eds). St Paul, MN: APS Press, pp. 107-124.