Mechanisms of powdery mildew resistance in the Vitaceae family

Molecular Plant Pathology

Volumn 12, Issue 3, 2011, Pages 263-274

  Feechan, Angela ^a   Kabbara, Samuela ^a   Dry, Ian B ^a  

^a CSIRO   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CALLOSE; GLUCAN;

ADAPTATION; ARTICLE; ASCOMYCETES; GRAPE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; SPECIES DIFFERENCE;

ADAPTATION, PHYSIOLOGICAL; ASCOMYCOTA; GLUCANS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; PLANT DISEASES; SPECIES SPECIFICITY; VITIS;

ERYSIPHALES; ERYSIPHE NECATOR; NECATOR; VITACEAE; VITIS; VITIS VINIFERA;

EID: 79952056899     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2010.00668.x     Document Type: Article

References (68)

1. Axtell, M.J. and Staskawicz, B.J. (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell, 112, 369-377.
2. Barker, C.L., Donald, T., Pauquet, J., Ratnaparkhe, M.B., Bouquet, A., Adam-Blondon, A.F., Thomas, M.R. and Dry, I. (2005) Genetic and physical mapping of the grapevine powdery mildew resistance gene, Run1, using a bacterial artificial chromosome library. Theor. Appl. Genet. 111, 370-377.
3. Bednarek, P., Pislewska-Bednarek, M., Svatos, A., Schneider, B., Doubsky, J., Mansurova, M., Humphry, M., Consonni, C., Panstruga, R., Sanchez-Vallet, A., Molina, A. and Schulze-Lefert, P. (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science, 323, 101-106.
4. Bent, A.F. and Mackey, D. (2007) Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399-436.
5. Bhat, R.A., Miklis, M., Schmelzer, E., Schulze-Lefert, P. and Panstruga, R. (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc. Natl. Acad. Sci. USA, 102, 3135-3140.
6. Boubals, D. (1961) Etude des causes de la résistance des Vitacées a l'oidium de la vigne Uncinula necator (Schw. Burr.) et leur moed de transmission hèrèditaire. Ann. L'Amél des Plantes, 11, 401-500.
7. Büschges, R., Hollricher, K., Panstruga, R., Simons, G., Wolter, M., Frijters, A., van Daelen, R., van der Lee, T., Diergaarde, P., Groenendijk, J., Topsch, S., Vos, P., Salamini, F. and Schulze-Lefert, P. (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell, 88, 695-705.
8. Cadle-Davidson, L., Chicoine, D.R. and Consolie, N.H. (2010) Variation within and between Vitis species for foliar resistance to the powdery mildew pathogen Erysiphe necator. Plant Dis. in press.
9. Caplan, J., Padmanabhan, M. and Dinesh-Kumar, S.P. (2008) Plant NB-LRR immune receptors: from recognition to transcriptional reprogramming. Cell Host Microbe, 3, 126-135.
10. Catanzariti, A.M., Dodds, P.N., Lawrence, G.J., Ayliffe, M.A. and Ellis, J.G. (2006) Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell, 18, 243-256.
11. Clay, N.K., Adio, A.M., Denoux, C., Jander, G. and Ausubel, F.M. (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science, 323, 95-101.
12. Collins, N.C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J.L., Huckelhoven, R., Stein, M., Freialdenhoven, A., Somerville, S.C. and Schulze-Lefert, P. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature, 425, 973-977.
13. Consonni, C., Humphry, M.E., Hartmann, H.A., Livaja, M., Durner, J., Westphal, L., Vogel, J., Lipka, V., Kemmerling, B., Schulze-Lefert, P., Somerville, S.C. and Panstruga, R. (2006) Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat. Genet. 38, 716-720.
14. Dodds, P.N., Lawrence, G.J., Catanzariti, A.M., Teh, T., Wang, C.I., Ayliffe, M.A., Kobe, B. and Ellis, J.G. (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. USA, 103, 8888-8893.
15. Donald, T.M., Pellerone, F., Adam-Blondon, A.F., Bouquet, A., Thomas, M.R. and Dry, I.B. (2002) Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine. Theor. Appl. Genet. 104, 610-618.
16. Doster, M.A. and Schnathorst, W.C. (1985) Comparative susceptibility of various grapevine cultivars to the powdery mildew fungus Uncinula-necator. Am. J. Enol. Vitic. 36, 101-104.
17. Driouich, A., Zhang, G.F. and Staehelin, L.A. (1993) Effect of brefeldin A on the structure of the Golgi apparatus and on the synthesis and secretion of proteins and polysaccharides in sycamore maple (Acer pseudoplatanus) suspension-cultured cells. Plant Physiol. 101, 1363-1373.
18. Dry, I.B., Feechan, A., Anderson, C., Jermakow, A.M., Bouquet, A., Adam-Blondon, A.F. and Thomas, M.R. (2009) Molecular strategies to enhance the genetic resistance of grapevines to powdery mildew. Aust. J. Grape Wine Res. 16, 94-105.
19. Eibach, R. (1994) Investigations about the genetic-resources of grapes with regard to resistance characteristics to powdery mildew (Oidium-tuckeri). Vitis, 33, 143-150.
20. Ellis, J.G., Dodds, P.N. and Lawrence, G.J. (2007) Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions. Annu. Rev. Phytopathol. 45, 289-306.
21. Feechan, A., Jermakow, A.M., Torregrosa, L., Panstruga, R. and Dry, I.B. (2008) Identification of grapevine MLO gene candidates involved in susceptibility to powdery mildew. Funct. Plant Biol. 35, 1255-1266.
22. Feng, J., Wang, F., Liu, G., Greenshields, D., Shen, W., Kaminskyj, S., Hughes, G.R., Peng, Y., Selvaraj, G., Zou, J. and Wei, Y. (2009) Analysis of a Blumeria graminis-secreted lipase reveals the importance of host epicuticular wax components for fungal adhesion and development. Mol. Plant-Microbe Interact. 22, 1601-1610.
23. Flor, H.H. (1971) Current status of gene-for-gene concept. Annu. Rev. Phytopathol. 9, 275.
24. Frei dit Frey, N. and Robatzek, S. (2009) Trafficking vesicles: pro or contra pathogens? Curr. Opin. Plant Biol. 12, 437-443.
25. Freytag, S., Arabatzis, N., Hahlbrock, K. and Schmelzer, E. (1994) Reversible cytoplasmic rearrangements precede wall apposition, hypersensitive cell-death and defense-related gene activation in potato-Phytophthora infestans interactions. Planta, 194, 123-135.
26. Fung, R.W., Gonzalo, M., Fekete, C., Kovacs, L.G., He, Y., Marsh, E., McIntyre, L.M., Schachtman, D.P. and Qiu, W. (2008) Powdery mildew induces defense-oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol. 146, 236-249.
27. Gadoury, D.M. and Pearson, R.C. (1991) Heterothallism and pathogenic specialization in Uncinula-necator. Phytopathology, 81, 1287-1293.
28. Geldner, N., Anders, N., Wolters, H., Keicher, J., Kornberger, W., Muller, P., Delbarre, A., Ueda, T., Nakano, A. and Jurgens, G. (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell, 112, 219-230.
29. Gomez-Gomez, L., Felix, G. and Boller, T. (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J. 18, 277-284.
30. Granado, J., Felix, G. and Boller, T. (1995) Perception of fungal sterols in plants-subnanomolar concentrations of ergosterol elicit extracellular alkalinization in tomato cells. Plant Physiol. 107, 485-490.
31. Hoffmann, S., Di Gaspero, G., Kovacs, L., Howard, S., Kiss, E., Galbacs, Z., Testolin, R. and Kozma, P. (2008) Resistance to Erysiphe necator in the grapevine 'Kishmish vatkana' is controlled by a single locus through restriction of hyphal growth. Theor. Appl. Genet. 116, 427-438.
32. Jackson, C.L. and Casanova, J.E. (2000) Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol. 10, 60-67.
33. Jones, D.A. and Takemoto, D. (2004) Plant innate immunity-direct and indirect recognition of general and specific pathogen-associated molecules. Curr. Opin. Immunol. 16, 48-62.
34. Kale, S.D., Gu, B., Capelluto, D.G., Dou, D., Feldman, E., Rumore, A., Arredondo, F.D., Hanlon, R., Fudal, I., Rouxel, T., Lawrence, C.B., Shan, W. and Tyler, B. (2010) External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell, 142, 284-295.
35. Kleine-Vehn, J., Leitner, J., Zwiewka, M., Sauer, M., Abas, L., Luschnig, C. and Friml, J. (2008) Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc. Natl. Acad. Sci. USA, 105, 17812-17817.
36. 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.
37. Kobayashi, Y., Yamada, M., Kobayashi, I. and Kunoh, H. (1997) Actin microfilaments are required for the expression of nonhost resistance in higher plants. Plant Cell Physiol. 38, 725-733.
38. Koch, E. and Slusarenko, A. (1990) Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell, 2, 437-445.
39. Koh, S., Andre, A., Edwards, H., Ehrhardt, D. and Somerville, S. (2005) Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 44, 516-529.
40. Lipka, V., Dittgen, J., Bednarek, P., Bhat, R., Wiermer, M., Stein, M., Landtag, J., Brandt, W., Rosahl, S., Scheel, D., Llorente, F., Molina, A., Parker, J., Somerville, S. and Schulze-Lefert, P. (2005) Pre- and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science, 310, 1180-1183.
41. Mackey, D., Holt, B.F., 3rd, Wiig, A. and Dangl, J.L. (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell, 108, 743-754.
42. Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R. and Dangl, J.L. (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 112, 379-389.
43. Manning, V.A. and Ciuffetti, L.M. (2005) Localization of Ptr ToxA produced by Pyrenophora tritici-repentis reveals protein import into wheat mesophyll cells. Plant Cell, 17, 3203-3212.
44. 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.
45. 2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J. 29, 257-268.
46. Meyer, D., Pajonk, S., Micali, C., O'Connell, R. and Schulze-Lefert, P. (2009) Extracellular transport and integration of plant secretory proteins into pathogen-induced cell wall compartments. Plant J. 57, 986-999.
47. Miklis, M., Consonni, C., Bhat, R.A., Lipka, V., Schulze-Lefert, P. and Panstruga, R. (2007) Barley MLO modulates actin-dependent and actin-independent antifungal defense pathways at the cell periphery. Plant Physiol. 144, 1132-1143.
48. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., Narusaka, Y., Kawakami, N., Kaku, H. and Shibuya, N. (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. USA, 104, 19613-19618.
49. Peterhänsel, C., Freialdenhoven, A., Kurth, J., Kolsch, R. and Schulze-Lefert, P. (1997) Interaction analyses of genes required for resistance responses to powdery mildew in barley reveal distinct pathways leading to leaf cell death. Plant Cell, 9, 1397-1409.
50. Pratelli, R., Sutter, J.U. and Blatt, M.R. (2004) A new catch in the SNARE. Trends Plant Sci. 9, 187-195.
51. Rafiqi, M., Gan, P.H., Ravensdale, M., Lawrence, G.J., Ellis, J.G., Jones, D.A., Hardham, A.R. and Dodds, P.N. (2010) Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell, 22, 2017-2032.
52. Robatzek, S., Chinchilla, D. and Boller, T. (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537-542.
53. Robinson, D.G., Langhans, M., Saint-Jore-Dupas, C. and Hawes, C. (2008) BFA effects are tissue and not just plant specific. Trends Plant Sci. 13, 405-408.
54. Schmelzer, E. (2002) Cell polarization, a crucial process in fungal defence. Trends Plant Sci. 7, 411-415.
55. Sciaky, N., Presley, J., Smith, C., Zaal, K.J., Cole, N., Moreira, J.E., Terasaki, M., Siggia, E. and Lippincott-Schwartz, J. (1997) Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J. Cell Biol. 139, 1137-1155.
56. Staiger, C.J. (2000) Signaling to the actin cytoskeleton in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 257-288.
57. Staudt, G. (1997) Evaluation of resistance to grapevine powdery mildew (Uncinula necator [Schw.] Burr., anamorph Oidium tuckeri Berk.) in accessions of Vitis species. Vitis, 36, 151-154.
58. Stein, M., Dittgen, J., Sanchez-Rodriguez, C., Hou, B.H., Molina, A., Schulze-Lefert, P., Lipka, V. and Somerville, S. (2006) Arabidopsis PEN3/PDR8, an ATP binding cassette transporter, contributes to nonhost resistance to inappropriate pathogens that enter by direct penetration. Plant Cell, 18, 731-746.
59. Steinmann, T., Geldner, N., Grebe, M., Mangold, S., Jackson, C.L., Paris, S., Galweiler, L., Palme, K. and Jurgens, G. (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science, 286, 316-318.
60. Stergiopoulos, I. and de Wit, P.J. (2009) Fungal effector proteins. Annu. Rev. Phytopathol. 47, 233-263.
61. 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.
62. Thordal-Christensen, H. (2003) Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6, 351-357.
63. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
64. Underwood, W. and Somerville, S.C. (2008) Focal accumulation of defences at sites of fungal pathogen attack. J. Exp. Bot. 59, 3501-3508.
65. Wan, Y.Z., Schwaninger, H., He, P.C. and Wang, Y.J. (2007) Comparison of resistance to powdery mildew and downy mildew in Chinese wild grapes. Vitis, 46, 132-136.
66. Wang, J., Cai, Y., Miao, Y., Lam, S.K. and Jiang, L. (2009) Wortmannin induces homotypic fusion of plant prevacuolar compartments. J. Exp. Bot. 60, 3075-3083.
67. Winterhagen, P., Howard, S.F., Qui, W. and Kovács, L.G. (2008) Transcriptional upregulation of grapevine MLO genes in response to powdery mildew infection. Am. J. Enol. Vitic. 59, 159-168.
68. 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.