Host cell entry of powdery mildew is correlated with endosomal transport of antagonistically acting VvPEN1 and VvMLO to the papilla

Molecular Plant-Microbe Interactions

Volumn 26, Issue 10, 2013, Pages 1138-1150

  Feechan, A ^a   Jermakow, A M ^a   Ivancevic, A ^a   Godfrey, D ^a   Pak, H ^a   Panstruga, R ^b   Dry, I B ^a  

^a CSIRO   (Australia)

^b RWTH AACHEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; PEN1 PROTEIN, ARABIDOPSIS; SYNTAXIN; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; ASCOMYCETES; CELL WALL; ENDOSOME; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PLANT DISEASE; PLANT IMMUNITY; PROTEIN TRANSPORT; TRANSGENIC PLANT; VITIS;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; CELL WALL; ENDOSOMES; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANT IMMUNITY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PROTEIN TRANSPORT; QA-SNARE PROTEINS; SEQUENCE DELETION; VITIS;

EID: 84884810388     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-04-13-0091-R     Document Type: Article

References (52)

1. Assaad, F. F., Qiu, J. L., Youngs, H., Ehrhardt, D., Zimmerli, L., Kalde, M., Wanner, G., Peck, S. C., Edwards, H., Ramonell, K., Somerville, C. R., and Thordal-Christensen, H. 2004. The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol. Biol. Cell 15:5118-5129.
2. 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 broadspectrum antifungal defense. Science 323:101-106.
3. Benschop, J. J., Mohammed, S., O'Flaherty, M., Heck, A. J. R., Slijper, M., and Menke, F. L. H. 2007. Quantitative phosphoproteomics of early elicitor signaling in Arabidopsis. Mol. Cell. Proteomics 6:1198-1214.
4. 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. U.S.A. 102:3135-3140.
5. 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.
6. Clough, S. J., and Bent, A. F. 1998. Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16:735-743.
7. 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.
8. 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.
9. Consonni, C., Bednarek, P., Humphry, M., Francocci, F., Ferrari, S., Harzen, A., Ver Loren van Themaat, E., and Panstruga, R. 2010.Tryptophanderived metabolites are required for antifungal defense in the Arabidopsis mlo2 mutant. Plant Physiol. 152 1544-1561.
10. Devoto, A., Piffanelli, P., Nilsson, I., Wallin, E., Panstruga, R., von Heijne, G., and Schulze-Lefert, P. 1999. Topology, subcellular localization, and sequence diversity of the Mlo family in plants. J. Biol. Chem. 274:34993-35004.
11. Devoto, A., Hartmann, H. A., Piffanelli, P., Elliott, C., Simmons, C., Taramino, G., Goh, C. S., Cohen, F. E., Emerson, B. C., Schulze-Lefert, P., and Panstruga, R. 2003. Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. J. Mol. Evol. 56:77-88.
12. 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.
13. Elliott, C., Zhou, F., Spielmeyer, W., Panstruga, R., and Schulze-Lefert, P. 2002. Functional conservation of wheat and rice Mlo orthologs in defense modulation to the powdery mildew fungus. Mol. Plant-Microbe Interact. 15:1069-1077.
14. 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.
15. Feechan, A., Kabbara, S., and Dry, I.B. 2011. Mechanisms of powdery mildew resistance in the Vitaceae family. Mol. Plant Pathol. 12:263-274.
16. 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.
17. Gleave, A. P. 1992. A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol. Biol. 20:1203-1207.
18. Godfrey, D., Zhang, Z., Saalbach, G., and Thordal-Christensen, H. 2009. A proteomics study of barley powdery mildew haustoria. Proteomics 9:3222-3232.
19. Haseloff, J., Siemering, K. R., Prasher, D. C., and Hodge, S. 1997. Removal of a cryptic intron and subcellular localization of green fluorescent protein are required to mark transgenic Arabidopsis plants brightly. Proc. Natl. Acad. Sci. U.S.A. 94:2122-2127.
20. Ito, E., Fujimoto, M., Ebine, K., Uemura, T., Ueda, T., and Nakano, A. 2012. Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging. Plant J. 69:204-216.
21. 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.
22. Jaillon, O., Aury, J. M., Noel, B., Policriti, A., Clepet, C., Casagrande, A., Choisne, N., Aubourg, S., Vitulo, N., Jubin, C., Vezzi, A., Legeai, F., Hugueney, P., Dasilva, C., Horner, D., Mica, E., Jublot, D., Poulain, J., Bruyere, C., Billault, A., Segurens, B., Gouyvenoux, M., Ugarte, E., Cattonaro, F., Anthouard, V., Vico, V., Del Fabbro, C., Alaux, M., Di Gaspero, G., Dumas, V., Felice, N., Paillard, S., Juman, I., Moroldo, M., Scalabrin, S., Canaguier, A., Le Clainche, I., Malacrida, G., Durand, E., Pesole, G., Laucou, V., Chatelet, P., Merdinoglu, D., Delledonne, M., Pezzotti, M., Lecharny, A., Scarpelli, C., Artiguenave, F., Pe, M. E., Valle, G., Morgante, M., Caboche, M., Adam-Blondon, A. F., Weissenbach, J., Quetier, F., and Wincker, P. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463-467.
23. 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.
24. 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.
25. Koch, E., and Slusarenko, A. 1990. Arabidopsis is susceptible to infection by a downy mildew fungus. Plant Cell 2:437-445.
26. Kwaaitaal, M., Keinath, N. F., Pajonk, S., Biskup, C., and Panstruga, R. 2010. Combined bimolecular fluorescence complementation (BiFC) and Förster resonance energy transfer (FRET) reveals ternary SNARE complex formation in living plant cells. Plant Physiol. 152:1135-1147.
27. Kwon, C., Neu, C., Pajonk, S., Yun, H. S., Lipka, U., Humphry, M., Bau, S., Straus, M., Kwaaitaal, M., Rampelt, H., El Kasmi, F., Jürgens, G., Parker, J., Panstruga, R., Lipka, V., and Schulze-Lefert, P. 2008. Co-option of a default secretory pathway for plant immune responses. Nature 451:835-U810.
28. Lewis, J. D., Wan, J., Ford, R., Gong, Y., Fung, P., Nahal, H., Wang, P. W., Desveaux, D., and Guttman, D. S. 2012. Quantitative interactor screening with next-generation sequencing (QIS-Seq) identifies Arabidopsis thaliana MLO2 as a target of the Pseudomonas syringae type III effector HopZ2. BMC Genomics 13:8.
29. 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.
30. Lipka, V., Kwon, C., and Panstruga, R. 2007. SNARE-ware: The role of SNARE-domain proteins in plant biology. Annu. Rev. Cell Dev. Biol. 23:147-174.
31. 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.
32. Miklis, M., Consonni, C., Bhat, R. A., Lipka, V., Schulze-Lefert, P., and Panstruga, R. 2007. Barley MLO modulates actin-dependent and actinindependent antifungal defense pathways at the cell periphery. Plant Physiol. 144:1132-1143.
33. 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. U.S.A. 104:19613-19618.
34. Nakagawa, T., Suzuki, T., Murata, S., Nakamura, S., Hino, T., Maeo, K., Tabata, R., Kawai, T., Tanaka, K., Niwa, Y., Watanabe, Y., Nakamura, K., Kimura, T., and Ishiguro, S. 2007. Improved gateway binary vectors: High-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71:2095-2100.
35. Nielsen, M. E., Feechan, A., Bohlenius, H., Ueda, T., and Thordal-Christensen, H. 2012. Arabidopsis ARF-GTP exchange factor, GNOM, mediates transport required for innate immunity and focal accumulation of syntaxin PEN1. Proc. Natl. Acad. Sci. U.S.A. 109:11443-11448.
36. Nühse, T. S., Boller, T., and Peck, S. C. 2003. A plasma membrane syntaxin is phosphorylated in response to the bacterial elicitor flagellin. J. Biol. Chem. 278:45248-45254.
37. Pajonk, S., Kwon, C., Clemens, N., Panstruga, R., and Schulze-Lefert, P. 2008. Activity determinants and functional specialization of Arabidopsis PEN1 syntaxin in innate immunity. J. Biol. Chem. 283:26974-26984.
38. Panstruga, R. 2005. Serpentine plant MLO proteins as entry portals for powdery mildew fungi. Biochem. Soc. Trans. 33:389-392.
39. Pedersen, C., Ver Loren van Themaat, E., McGuffin, L. J., Abbott, J. C., Burgis, T. A., Barton, G., Bindschedler, L. V., Lu, X., Maekawa, T., Wessling, R., Cramer, R., Thordal-Christensen, H., Panstruga, R., and Spanu, P. D. 2012. Structure and evolution of barley powdery mildew effector candidates. BMC Genomics 13:694.
40. Pratelli, R., Sutter, J. U., and Blatt, M. R. 2004. A new catch in the SNARE. Trends Plant Sci. 9:187-195.
41. Robatzek, S., Chinchilla, D., and Boller, T. 2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20:537-542.
42. Saitou, N., and Nei, M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
43. Satiat-Jeunemaitre, B., Cole, L., Bourett, T., Howard, R., and Hawes, C. 1996. Brefeldin A effects in plant and fungal cells: Something new about vesicle trafficking? J. Microsc. 181:162-177.
44. Spanu, P. D., Abbott, J. C., Amselem, J., Burgis, T. A., Soanes, D. M., Stuber, K., Ver Loren van Themaat, E., Brown, J. K., Butcher, S. A., Gurr, S. J., Lebrun, M. H., Ridout, C. J., Schulze-Lefert, P., Talbot, N. J., Ahmadinejad, N., Ametz, C., Barton, G. R., Benjdia, M., Bidzinski, P., Bindschedler, L. V., Both, M., Brewer, M. T., Cadle-Davidson, L., Cadle-Davidson, M. M., Collemare, J., Cramer, R., Frenkel, O., Godfrey, D., Harriman, J., Hoede, C., King, B. C., Klages, S., Kleemann, J., Knoll, D., Koti, P. S., Kreplak, J., Lopez-Ruiz, F. J., Lu, X., Maekawa, T., Mahanil, S., Micali, C., Milgroom, M.G., Montana, G., Noir, S., O'Connell, R. J., Oberhaensli, S., Parlange, F., Pedersen, C., Quesneville, H., Reinhardt, R., Rott, M., Sacristan, S., Schmidt, S. M., Schon, M., Skamnioti, P., Sommer, H., Stephens, A., Takahara, H., Thordal-Christensen, H., Vigouroux, M., Wessling, R., Wicker, T., and Panstruga, R. 2010. Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330:1543-1546.
45. 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.
46. Teh, O. K., and Moore, I. 2007. An ARF-GEF acting at the Golgi and in selective endocytosis in polarized plant cells. Nature 448:493-496.
47. Thompson, J. D., Higgins, D. G., and Gibson, T. J. 1994. CLUSTALW: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
48. Thordal-Christensen, H. 2003. Fresh insights into processes of nonhost resistance. Curr. Opin. Plant Biol. 6:351-357.
49. Tucker, M. R., Okada, T., Hu, Y. K., Scholefield, A., Taylor, J. M., and Koltunow, A. M. G. 2012. Somatic small RNA pathways promote the mitotic events of megagametogenesis during female reproductive development in Arabidopsis. Development 139:1399-1404.
50. Underwood, W., and Somerville, S. C. 2008. Focal accumulation of defences at sites of fungal pathogen attack. J. Exp. Bot. 59:3501-3508.
51. 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.
52. 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.