A comprehensive mutational analysis of the arabidopsis resistance protein RPW8.2 reveals key amino acids for defense activation and protein targeting

Plant Cell

Volumn 25, Issue 10, 2013, Pages 4242-4261

  Wang, Wenming ^a,b   Zhang, Yi ^b   Wen, Yingqiang ^b,c   Berkey, Robert ^b   Ma, Xianfeng ^a,b   Pan, Zhiyong ^b,d   Bendigeri, Dipti ^b   King, Harlan ^b   Zhang, Qiong ^b   Xiao, Shunyuan ^b,e  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

^b UNIVERSITY OF MARYLAND BIOTECHNOLOGY INSTITUTE   (United States)

^c NORTHWEST A F UNIVERSITY   (China)

^d HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^e UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; ERYSIPHALES; GOLOVINOMYCES CICHORACEARUM;

AMINO ACID; ARABIDOPSIS PROTEIN; PLANT DNA; RPW8.2 PROTEIN, ARABIDOPSIS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ASCOMYCETES; CYTOLOGY; DISEASE RESISTANCE; GENETICS; IMMUNOLOGY; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT DISEASE; PLANT IMMUNITY; PLANT LEAF; SITE DIRECTED MUTAGENESIS; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMINO ACIDS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ASCOMYCOTA; DISEASE RESISTANCE; DNA MUTATIONAL ANALYSIS; DNA, PLANT; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PLANT DISEASES; PLANT IMMUNITY; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED;

EID: 84888419593     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.117226     Document Type: Article

References (72)

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. Bhattacharjee, S., Halane, M.K., Kim, S.H., and Gassmann, W. (2011). Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science 334: 1405-1408.
3. Bonfante, P., and Genre, A. (2010). Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1: 48.
4. Brueggeman, R., Rostoks, N., Kudrna, D., Kilian, A., Han, F., Chen, J., Druka, A., Steffenson, B., and Kleinhofs, A. (2002). The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc. Natl. Acad. Sci. USA 99: 9328-9333.
5. Caplan, J.L., Mamillapalli, P., Burch-Smith, T.M., Czymmek, K., and Dinesh-Kumar, S.P. (2008). Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell 132: 449-462.
6. Chisholm, S.T., Coaker, G., Day, B., and Staskawicz, B.J. (2006). Host-microbe interactions: Shaping the evolution of the plant immune response. Cell 124: 803-814.
7. Collins, N.C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J.L., Hückelhoven, 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. Feys, B.J., Wiermer, M., Bhat, R.A., Moisan, L.J., Medina-Escobar, N., Neu, C., Cabral, A., and Parker, J.E. (2005). Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell 17: 2601-2613.
9. Frye, C.A., Tang, D., and Innes, R.W. (2001). Negative regulation of defense responses in plants by a conserved MAPKK kinase. Proc. Natl. Acad. Sci. USA 98: 373-378.
10. Fu, Z.Q., Yan, S., Saleh, A., Wang, W., Ruble, J., Oka, N., Mohan, R., Spoel, S.H., Tada, Y., Zheng, N., and Dong, X. (2012). NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486: 228-232.
11. Halterman, D., Zhou, F., Wei, F., Wise, R.P., and Schulze-Lefert, P. (2001). The MLA6 coiled-coil, NBS-LRR protein confers AvrMla6-dependent resistance specificity to Blumeria graminis f. sp. hordei in barley and wheat. Plant J. 25: 335-348.
12. Hardham, A.R., Jones, D.A., and Takemoto, D. (2007). Cytoskeleton and cell wall function in penetration resistance. Curr. Opin. Plant Biol. 10: 342-348.
13. Heidrich, K., Wirthmueller, L., Tasset, C., Pouzet, C., Deslandes, L., and Parker, J.E. (2011). Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science 334: 1401-1404.
14. Hückelhoven, R., and Panstruga, R. (2011). Cell biology of the plantpowdery mildew interaction. Curr. Opin. Plant Biol. 14: 738-746.
15. Humphry, M., Bednarek, P., Kemmerling, B., Koh, S., Stein, M., Göbel, U., Stüber, K., Pislewska-Bednarek, M., Loraine, A., Schulze-Lefert, P., Somerville, S., and Panstruga, R. (2010). A regulon conserved in monocot and dicot plants defines a functional module in antifungal plant immunity. Proc. Natl. Acad. Sci. USA 107: 21896-21901.
16. Isakoff, S.J., Cardozo, T., Andreev, J., Li, Z., Ferguson, K.M., Abagyan, R., Lemmon, M.A., Aronheim, A., and Skolnik, E.Y. (1998). Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J. 17: 5374-5387.
17. Israel, H.W., Wilson, R.G., Aist, J.R., and Kunoh, H. (1980). Cell wall appositions and plant disease resistance: Acoustic microscopy of papillae that block fungal ingress. Proc. Natl. Acad. Sci. USA 77: 2046-2049.
18. Jones, J.D., and Dangl, J.L. (2006). The plant immune system. Nature 444: 323-329.
19. Kinkema, M., Fan, W., and Dong, X. (2000). Nuclear localization of NPR1 is required for activation of PR gene expression. Plant Cell 12: 2339-2350.
20. Koh, S., André, A., Edwards, H., Ehrhardt, D., and Somerville, S. (2005). Arabidopsis thaliana subcellular responses to compatible Erysiphe cichoracearum infections. Plant J. 44: 516-529.
21. Köhler, R.H., Cao, J., Zipfel, W.R., Webb, W.W., and Hanson, M.R. (1997). Exchange of protein molecules through connections between higher plant plastids. Science 276: 2039-2042.
22. Kosugi, S., Hasebe, M., Matsumura, N., Takashima, H., Miyamoto-Sato, E., Tomita, M., and Yanagawa, H. (2009). Six classes of nuclear localization signals specific to different binding grooves of importin α. J. Biol. Chem. 284: 478-485.
23. Krattinger, S.G., Lagudah, E.S., Spielmeyer, W., Singh, R.P., Huerta-Espino, J., McFadden, H., Bossolini, E., Selter, L.L., and Keller, B. (2009). A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323: 1360-1363.
24. Krenz, B., Jeske, H., and Kleinow, T. (2012). The induction of stromule formation by a plant DNA-virus in epidermal leaf tissues suggests a novel intra-and intercellular macromolecular trafficking route. Front. Plant Sci. 3: 291.
25. Kutateladze, T.G. (2006). Phosphatidylinositol 3-phosphate recognition and membrane docking by the FYVE domain. Biochim. Biophys. Acta 1761: 868-877.
26. Kwon, C., et al. (2008). Co-option of a default secretory pathway for plant immune responses. Nature 451: 835-840.
27. Lawrence, G.J., Finnegan, E.J., Ayliffe, M.A., and Ellis, J.G. (1995). The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell 7: 1195-1206.
28. Lemmon, M.A. (2008). Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9: 99-111.
29. Li, H.Y., and Chye, M.L. (2003). Membrane localization of Arabidopsis acyl-CoA binding protein ACBP2. Plant Mol. Biol. 51: 483-492.
30. Lipka, V., et al. (2005). Pre-and postinvasion defenses both contribute to nonhost resistance in Arabidopsis. Science 310: 1180-1183.
31. Lu, Y.J., Schornack, S., Spallek, T., Geldner, N., Chory, J., Schellmann, S., Schumacher, K., Kamoun, S., and Robatzek, S. (2012). Patterns of plant subcellular responses to successful oomycete infections reveal differences in host cell reprogramming and endocytic trafficking. Cell. Microbiol. 14: 682-697.
32. Meder, V.S., Boeglin, M., de Murcia, G., and Schreiber, V. (2005). PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J. Cell Sci. 118: 211-222.
33. 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.
34. 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.
35. Misra, S., Miller, G.J., and Hurley, J.H. (2001). Recognizing phosphatidylinositol 3-phosphate. Cell 107: 559-562.
36. Mosher, R.A., Durrant, W.E., Wang, D., Song, J., and Dong, X. (2006). A comprehensive structure-function analysis of Arabidopsis SNI1 defines essential regions and transcriptional repressor activity. Plant Cell 18: 1750-1765.
37. Müller, C., Bremer, A., Schreiber, S., Eichwald, S., and Calkhoven, C.F. (2010). Nucleolar retention of a translational C/EBPalpha isoform stimulates rDNA transcription and cell size. EMBO J. 29: 897-909.
38. Nelson, B.K., Cai, X., and Nebenführ, A. (2007). A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51: 1126-1136.
39. O'Connell, R.J., and Panstruga, R. (2006). Tête à tête inside a plant cell: Establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytol. 171: 699-718.
40. Orgil, U., Araki, H., Tangchaiburana, S., Berkey, R., and Xiao, S. (2007). Intraspecific genetic variations, fitness cost and benefit of RPW8, a disease resistance locus in Arabidopsis thaliana. Genetics 176: 2317-2333.
41. Parker, J.E., Coleman, M.J., Szabò, V., Frost, L.N., Schmidt, R., van der Biezen, E.A., Moores, T., Dean, C., Daniels, M.J., and Jones, J.D. (1997). The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 9: 879-894.
42. Periyannan, S., et al. (2013). The gene Sr33, an ortholog of barley Mla genes, encodes resistance to wheat stem rust race Ug99. Science 341: 786-788.
43. Price, D.C., et al. (2012). Cyanophora paradoxa genome elucidates origin of photosynthesis in algae and plants. Science 335: 843-847.
44. Pumplin, N., Zhang, X., Noar, R.D., and Harrison, M.J. (2012). Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proc. Natl. Acad. Sci. USA 109: E665-E672.
45. Rairdan, G.J., Collier, S.M., Sacco, M.A., Baldwin, T.T., Boettrich, T., and Moffett, P. (2008). The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell 20: 739-751.
46. Saintenac, C., Zhang, W., Salcedo, A., Rouse, M.N., Trick, H.N., Akhunov, E., and Dubcovsky, J. (2013). Identification of wheat gene Sr35 that confers resistance to Ug99 stem rust race group. Science 341: 783-786.
47. Sattarzadeh, A., Krahmer, J., Germain, A.D., and Hanson, M.R. (2009). A myosin XI tail domain homologous to the yeast myosin vacuole-binding domain interacts with plastids and stromules in Nicotiana benthamiana. Mol. Plant 2: 1351-1358.
48. Schattat, M., Barton, K., Baudisch, B., Klösgen, R.B., and Mathur, J. (2011). Plastid stromule branching coincides with contiguous endoplasmic reticulum dynamics. Plant Physiol. 155: 1667-1677.
49. 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.
50. Scott, M., Boisvert, F.M., Vieyra, D., Johnston, R.N., Bazett-Jones, D.P., and Riabowol, K. (2001). UV induces nucleolar translocation of ING1 through two distinct nucleolar targeting sequences. Nucleic Acids Res. 29: 2052-2058.
51. Shen, Q.H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., Seki, H., Ulker, B., Somssich, I.E., and Schulze-Lefert, P. (2007). Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science 315: 1098-1103.
52. Song, J., Bradeen, J.M., Naess, S.K., Raasch, J.A., Wielgus, S.M., Haberlach, G.T., Liu, J., Kuang, H., Austin-Phillips, S., Buell, C.R., Helgeson, J.P., and Jiang, J. (2003). Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl. Acad. Sci. USA 100: 9128-9133.
53. Spoel, S.H., Mou, Z., Tada, Y., Spivey, N.W., Genschik, P., and Dong, X. (2009). Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137: 860-872.
54. Stein, M., Dittgen, J., Sánchez-Rodríguez, 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.
55. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11: 1187-1194.
56. Vallejo, A.N., Pogulis, R.J., and Pease, L.R. (2003). Mutagenesis and synthesis of novel recombinant genes using PCR. In PCR Primer: A Laboratory Manual, C.W. Dieffenbach and G.S. Dveksler, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 467-474.
57. Wang, W., Berkey, R., Wen, Y., and Xiao, S. (2010). Accurate and adequate spatiotemporal expression and localization of RPW8.2 is key to activation of resistance at the host-pathogen interface. Plant Signal. Behav. 5: 1002-1005.
58. Wang, W., Devoto, A., Turner, J.G., and Xiao, S. (2007). Expression of the membrane-associated resistance protein RPW8 enhances basal defense against biotrophic pathogens. Mol. Plant Microbe Interact. 20: 966-976.
59. Wang, W., Wen, Y., Berkey, R., and Xiao, S. (2009). Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. Plant Cell 21: 2898-2913.
60. Waters, M.T., Fray, R.G., and Pyke, K.A. (2004). Stromule formation is dependent upon plastid size, plastid differentiation status and the density of plastids within the cell. Plant J. 39: 655-667.
61. Wen, Y., Wang, W., Feng, J., Luo, M.C., Tsuda, K., Katagiri, F., Bauchan, G., and Xiao, S. (2011). Identification and utilization of a sow thistle powdery mildew as a poorly adapted pathogen to dissect post-invasion non-host resistance mechanisms in Arabidopsis. J. Exp. Bot. 62: 2117-2129.
62. Wilson, I.A., Haft, D.H., Getzoff, E.D., Tainer, J.A., Lerner, R.A., and Brenner, S. (1985). Identical short peptide sequences in unrelated proteins can have different conformations: A testing ground for theories of immune recognition. Proc. Natl. Acad. Sci. USA 82: 5255-5259.
63. Xiao, S., Brown, S., Patrick, E., Brearley, C., and Turner, J.G. (2003). Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1 and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. Plant Cell 15: 33-45.
64. Xiao, S., Calis, O., Patrick, E., Zhang, G., Charoenwattana, P., Muskett, P., Parker, J.E., and Turner, J.G. (2005). The atypical resistance gene, RPW8, recruits components of basal defence for powdery mildew resistance in Arabidopsis. Plant J. 42: 95-110.
65. Xiao, S., Ellwood, S., Calis, O., Patrick, E., Li, T., Coleman, M., and Turner, J.G. (2001). Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291: 118-120.
66. Xiao, S., Ellwood, S., Findlay, K., Oliver, R.P., and Turner, J.G. (1997). Characterization of three loci controlling resistance of Arabidopsis thaliana accession Ms-0 to two powdery mildew diseases. Plant J. 12: 757-768.
67. Xiao, S., Emerson, B., Ratanasut, K., Patrick, E., O'Neill, C., Bancroft, I., and Turner, J.G. (2004). Origin and maintenance of a broad-spectrum disease resistance locus in Arabidopsis. Mol. Biol. Evol. 21: 1661-1672.
68. Yahiaoui, N., Srichumpa, P., Dudler, R., and Keller, B. (2004). Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. Plant J. 37: 528-538.
69. Yang, X., Wang, W., Coleman, M., Orgil, U., Feng, J., Ma, X., Ferl, R., Turner, J.G., and Xiao, S. (2009). Arabidopsis 14-3-3 lambda is a positive regulator of RPW8-mediated disease resistance. Plant J. 60: 539-550.
70. Yoon, H.S., Nakayama, T., Reyes-Prieto, A., Andersen, R.A., Boo, S.M., Ishida, K., and Bhattacharya, D. (2009). A single origin of the photosynthetic organelle in different Paulinella lineages. BMC Evol. Biol. 9: 98.
71. Yuan, H., Michelsen, K., and Schwappach, B. (2003). 14-3-3 dimers probe the assembly status of multimeric membrane proteins. Curr. Biol. 13: 638-646.
72. 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.