Regulation of basal resistance by a powdery mildew-induced cysteine-rich receptor-like protein kinase in barley

Molecular Plant Pathology

Volumn 13, Issue 2, 2012, Pages 135-147

  Rayapuram, Cbgowda ^a   Jensen, Michael K ^a   Maiser, Fabian ^a   Shanir, Johanna Vikgren ^a   Hornshøj, Henrik ^a,b   Rung, Jesper H ^a,d   Gregersen, Per L ^a,b   Schweizer, Patrick ^c   Collinge, David B ^a   Lyngkjær, Michael F ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b AARHUS UNIVERSITY   (Denmark)

^c LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

^d NOVOZYMES A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; COMPLEMENTARY DNA; CYSTEINE; HYDROGEN PEROXIDE; MESSENGER RNA; PROTEIN KINASE; SALICYLIC ACID; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; ASCOMYCETES; CELL FRACTIONATION; CHEMICAL PHENOMENA; CHEMISTRY; DISEASE RESISTANCE; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HORDEUM; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ASCOMYCOTA; CYSTEINE; DISEASE RESISTANCE; DNA, COMPLEMENTARY; GENE EXPRESSION REGULATION, PLANT; GENE SILENCING; HORDEUM; HYDROGEN PEROXIDE; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PLANT LEAVES; PLANT PROTEINS; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECEPTORS, CELL SURFACE; RNA, MESSENGER; SALICYLIC ACID; SUBCELLULAR FRACTIONS;

BLUMERIA GRAMINIS; ERYSIPHALES; HORDEUM; HORDEUM VULGARE;

EID: 84855739838     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2011.00736.x     Document Type: Article

References (57)

1. Acharya, B.R., Raina, S., Maqbool, S.B., Jagadeeswaran, G., Mosher, S.L., Appel, H.M., Schultz, J.C., Klessig, D.F. and Raina, R. (2007) Overexpression of CRK13, an Arabidopsis cysteine-rich receptor-like kinase, results in enhanced resistance to Pseudomonas syringae. Plant J. 50, 488-499.
2. 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.
3. Brandizzi, F., Frangne, N., Marc-Martin, S., Hawes, C., Neuhaus, J.M. and Paris, N. (2002) The destination for single-pass membrane proteins is influenced markedly by the length of the hydrophobic domain. Plant Cell, 14, 1077-1092.
4. Bretscher, M.S. and Munro, S. (1993) Cholesterol and the Golgi-apparatus. Science, 261, 1280-1281.
5. Buschges, 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.
6. Carver, T.L.W., Zeyen, R.J., Robbins, M.P., Vance, C.P. and Boyles, D.A. (1994) Suppression of host cinnamyl alcohol-dehydrogenase and phenylalanine ammonia-lyase increases oat epidermal-cell susceptibility to powdery mildew penetration. Physiol. Mol. Plant Pathol. 44, 243-259.
7. Chen, K.G., Du, L.Q. and Chen, Z.X. (2003) Sensitization of defense responses and activation of programmed cell death by a pathogen-induced receptor-like protein kinase in Arabidopsis. Plant Mol. Biol. 53, 61-74.
8. Chen, K.G., Fan, B.F., Du, L.Q. and Chen, Z.X. (2004) Activation of hypersensitive cell death by pathogen-induced receptor-like protein kinases from Arabidopsis. Plant Mol. Biol. 56, 271-283.
9. Chen, Z.X. (2001) A superfamily of proteins with novel cysteine-rich repeats. Plant Physiol. 126, 473-476.
10. Collinge, D.B., Gregersen, P.L. and Thordal-Christensen, H. (2002) The nature and role of defence response genes in cereals. In: The Powdery Mildews: A Comprehensive Treatise (Belanger, R.R., Bushnell, W.R., Dik, A.J. and Carver, T.L.W., eds), pp. 146-160. St. Paul, MN: American Phytopathological Society Press.
11. 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.
12. Dievart, A. and Clark, S.E. (2004) LRR-containing receptors regulating plant development and defense. Development, 131, 251-261.
13. Dong, W.B., Nowara, D. and Schweizer, P. (2006) Protein polyubiquitination plays a role in basal host resistance of barley. Plant Cell, 18, 3321-3331.
14. Douchkov, D., Nowara, D., Zierold, U. and Schweizer, P. (2005) A high-throughput gene-silencing system for the functional assessment of defense-related genes in barley epidermal cells. Mol. Plant-Microbe Interact. 18, 755-761.
15. Du, L.Q. and Chen, Z.X. (2000) Identification of genes encoding receptor-like protein kinases as possible targets of pathogen- and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J. 24, 837-847.
16. Dykema, P.E., Sipes, P.R., Marie, A., Biermann, B.J., Crowell, D.N. and Randall, S.K. (1999) A new class of proteins capable of binding transition metals. Plant Mol. Biol. 41, 139-150.
17. Earley, K.W., Haag, J.R., Pontes, O., Opper, K., Juehne, T., Song, K.M. and Pikaard, C.S. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J. 45, 616-629.
18. Glazebrook, J. (2001) Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr. Opin. Plant Biol. 4, 301-308.
19. Gregersen, P.L. and Collinge, D.B. (2001) Penetration attempts by the powdery mildew fungus into barley leaves are accompanied by increased gene transcript accumulation in the epidermal cell layer. In 5th Congress of the European Foundation for Plant Pathology. J. Plant Pathol. 82, 257-260. Edizioni/ETS.
20. Gregersen, P.L., Thordal-Christensen, H., Forster, 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 (syn. Erysiphe graminis f.sp. hordei). Physiol. Mol. Plant Pathol. 51, 85-97.
21. Horton, P., Park, K.J., Obayashi, T., Fujita, N., Harada, H., Adams-Collier, C.J. and Nakai, K. (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res. 35, W585-W587.
22. Huckelhoven, R., Fodor, J., Preis, C. and Kogel, K.H. (1999) Hypersensitive cell death and papilla formation in barley attacked by the powdery mildew fungus are associated with hydrogen peroxide but not with salicylic acid accumulation. Plant Physiol. 119, 1251-1260.
23. Ihlow, A., Schweizer, P. and Seiffert, U. (2008) A high-throughput screening system for barley/powdery mildew interactions based on automated analysis of light micrographs. BMC Plant Biol. 8, Article 6.
24. Jensen, M.K., Rung, J.H., Gregersen, P.L., Gjetting, T., Fuglsang, A.T., Hansen, M., Joehnk, N., Lyngkjaer, M.F. and Collinge, D.B. (2007) The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis. Plant Mol. Biol. 65, 137-150.
25. Jiang, J.F., Li, J.H., Xu, Y.Y., Han, Y., Bai, Y., Zhou, G.X., Lou, Y.G., Xu, Z.H. and Chong, K. (2007) RNAi knockdown of Oryza sativa root meander curling gene led to altered root development and coiling which were mediated by jasmonic acid signalling in rice. Plant Cell Environ. 30, 690-699.
26. Johrde, A. and Schweizer, P. (2008) A class III peroxidase specifically expressed in pathogen-attacked barley epidermis contributes to basal resistance. Mol. Plant Pathol. 9, 687-696.
27. Jørgensen, J.H. (1994) Genetics of powdery mildew resistance in barley. Crit. Rev. Plant Sci. 13, 97-119.
28. 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, 447-450.
29. 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.
30. Kyte, J. and Doolittle, R.F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132.
31. Lassmann, T., Frings, O. and Sonnhammer, E.L.L. (2009) Kalign2: high-performance multiple alignment of protein and nucleotide sequences allowing external features. Nucleic Acids Res. 37, 858-865.
32. Lehti-Shiu, M.D., Zou, C., Hanada, K. and Shiu, S.H. (2009) Evolutionary history and stress regulation of plant receptor-like kinase/Pelle genes. Plant Physiol. 150, 12-26.
33. +-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol. 7, e100013.
34. Lyngkjaer, M.F., Newton, A.C., Atzema, J.L. and Baker, S.J. (2000) The barley mlo-gene: an important powdery mildew resistance source. Agronomie, 20, 745-756.
35. Michelsen, K., Schmid, V., Metz, J., Heusser, K., Liebel, U., Schwede, T., Spang, A. and Schwappach, B. (2007) Novel cargo-binding site in the beta and delta subunits of coatomer. J. Cell Biol. 179, 209-217.
36. Overmyer, K., Brosche, M. and Kangasjarvi, J. (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci. 8, 335-342.
37. Panstruga, R. and Schulze-Lefert, P. (2003) Corruption of host seven-transmembrane proteins by pathogenic microbes: a common theme in animals and plants? Microb. Infect. 5, 429-437.
38. Perriere, G. and Gouy, M. (1996) WWW-query: an on-line retrieval system for biological sequence banks. Biochimie, 78, 364-369.
39. Pfaffl, M.W., Horgan, G.W. and Dempfle, L. (2002) Relative expression software tool (REST (c)) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36.
40. Piffanelli, P., Zhou, F.S., 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.
41. Prats, E., Mur, L.A.J., Sanderson, R. and Carver, T.L.W. (2005) Nitric oxide contributes both to papilla-based resistance and the hypersensitive response in barley attacked by Blumeria graminis f. sp hordei. Mol. Plant Pathol. 6, 65-78.
42. Ren, X.R., Reiter, E., Ahn, S., Kim, J., Chen, W. and Lefkowitz, R.J. (2005) Different G protein-coupled receptor kinases govern G protein and beta-arrestin-mediated signaling of V2 vasopressin receptor. Proc. Natl. Acad. Sci. USA, 102, 1448-1453.
43. Runions, J., Brach, T., Kuhner, S. and Hawes, C. (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. J. Exp. Bot. 57, 43-50.
44. Schultz, J., Copley, R.R., Doerks, T., Ponting, C.P. and Bork, P. (2000) SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res. 28, 231-234.
45. 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.
46. Seeholzer, S., Tsuchimatsu, T., Jordan, T., Bieri, S., Pajonk, S., Yang, W.X., Jahoor, A., Shimizu, K.K., Keller, B. and Schulze-Lefert, P. (2010) Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Mol. Plant-Microbe Interact. 23, 497-509.
47. Shiu, S., Karlowski, W.M., Mayer, K.F.X., Pan, R., Tzeng, Y. and Li, W. (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis thaliana and rice. Plant Cell, 2004, 1220-1234.
48. Shiu, S.H. and Bleecker, A.B. (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc. Natl. Acad. Sci. USA, 98, 10763-10768.
49. Singh, K.B., Foley, R.C. and Onate-Sanchez, L. (2002) Transcription factors in plant defense and stress responses. Curr. Opin. Plant Biol. 5, 430-436.
50. Szczesna-Skorupa, E. and Kemper, B. (2000) Endoplasmic reticulum retention determinants in the transmembrane and linker domains of cytochrome P4502C1. J. Biol. Chem. 275, 19409-19415.
51. Teasdale, R.D. and Jackson, M.R. (1996) Signal-mediated sorting of membrane proteins between the endoplasmic reticulum and the Golgi apparatus. Annu. Rev. Cell Dev. Biol. 12, 27-54.
52. Thomas, C.L., Bayer, E.M., Ritzenthaler, C., Fernandez-Calvino, L. and Maule, A.J. (2008) Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol. 6, 180-190.
53. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25, 4876-4882.
54. 2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. Plant J. 11, 1187-1194.
55. Tichtinsky, G., Vanoosthuyse, V., Cock, J.M. and Gaude, T. (2003) Making inroads into plant receptor kinase signalling pathways. Trends Plant Sci. 8, 231-237.
56. Wrzaczek, M., Brosche, M., Salojarvi, J., Kangasjarvi, S., Idanheimo, N., Mersmann, S., Robatzek, S., Karpinski, S., Karpinska, B. and Kangasjarvi, J. (2010) Transcriptional regulation of the CRK/DUF26 group of receptor-like protein kinases by ozone and plant hormones in Arabidopsis. BMC Plant Biol. 10(95), 1-19.
57. Zeyen, R.J., Carver, T.L.W. and Lyngkjaer, M.F. (2002) Epidermal cell papillae. In: The Powdery Mildews: A Comprehensive Treatise (Belanger, R.R., Bushnell, W.R., Dik, A.J. and Carver, T.L.W., eds), pp. 107-125. St. Paul, MN: American Phytopathological Society Press.