Tapping into molecular conversation between oomycete plant pathogens and their hosts

Article

Abstract

Several plant pathogenic oomycetes have been under investigation using modern molecular approaches. Genome sequencing and annotations are underway or near to completion for some of the species. Pathogen-associated molecular pattern molecules (PAMPs) and effector molecules perform inter- and intracellular tasks as adaptation factors and manipulators of the defence network. Hundreds of secreted putative effectors have been discovered and conserved molecular patterns such as RXLR and EER motifs have been identified and used for classifications. PAMPs and effectors are recognized directly or indirectly by the pattern recognition receptors at the cell surface including receptor-like kinases and receptor-like proteins, and/or by nucleotide binding site–leucine rich repeat proteins within the cytoplasm. The current knowledge of effectors, immune receptors and the defence network, will help us understand the ‘intricate genetic dance’ between the oomycete pathogens and their hosts. This review concentrates on the recent findings in oomycete-plant interactions.

Keywords

PAMPs Effector Oomycete Receptor Biotrophy 

References

  1. Abramovitch, R. B., Janjusevic, R., Stebbins, C. E., & Martin, G. B. (2006). Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proceedings of the National Academy of Sciences of the United States of America, 103, 2851–2856.PubMedCrossRefGoogle Scholar
  2. Agrios, G. N. (1997). Plant pathology. San Diego: Academic.Google Scholar
  3. Allen, R. L., Bittner-Eddy, P. D., Grenville-Briggs, L. J., Meitz, J. C., Rehmany, A. P., Rose, L. E., et al. (2004). Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science, 306, 1957–1960.PubMedCrossRefGoogle Scholar
  4. Altenbach, D., & Robatzek, S. (2007). Pattern recognition receptors: From the cell surface to intracellular dynamics. Molecular PlantMicrobe Interactions, 20, 1031–1039.PubMedCrossRefGoogle Scholar
  5. Armstrong, M. R., Whisson, S. C., Pritchard, L., Bos, J. I., Venter, E., Avrova, A. O., et al. (2005). An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proceedings of the National Academy of Sciences of the United States of America, 102, 7766–7771.PubMedCrossRefGoogle Scholar
  6. Ballvora, A., Ercolano, M. R., Weiss, J., Meksem, K., Bormann, C. A., Oberhagemann, P., et al. (2002). The R1 gene for potato resistance to late blight (Phytophthora infestans) belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant Journal, 30, 361–371.PubMedCrossRefGoogle Scholar
  7. Bhattacharjee, S., Hiller, N. L., Liolios, K., Win, J., Kanneganti, T. D., Young, C., et al. (2006). The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathogens, 2, e50.PubMedCrossRefGoogle Scholar
  8. Birch, P. R., Rehmany, A. P., Pritchard, L., Kamoun, S., & Beynon, J. L. (2006). Trafficking arms: Oomycete effectors enter host plant cells. Trends in Microbiology, 14, 8–11.PubMedCrossRefGoogle Scholar
  9. Bittner-Eddy, P. D., Allen, R. L., Rehmany, A. P., Birch, P., & Beynon, J. L. (2003). Use of suppression subtractive hybridization to identify downy mildew gene expressed during infection of Arabidopsis thaliana. Molecular Plant Pathology, 4, 501–507.CrossRefGoogle Scholar
  10. Borhan, M. H., Holub, E. B., Beynon, J. L., Rozwadowski, K., & Rimmer, S. R. (2004). The Arabidopsis TIR-NB-LRR gene RAC1 confers resistance to Albugo candida (white rust) and is dependent on EDS1 but not PAD4. Molecular Plant-microbe Interactions, 17, 711–719.PubMedCrossRefGoogle Scholar
  11. Bos, J. I., Kanneganti, T. D., Young, C., Cakir, C., Huitema, E., Win, J., et al. (2006). The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant Journal, 48, 165–176.PubMedCrossRefGoogle Scholar
  12. Brunner, F., Rosahl, S., Lee, J., Rudd, J. J., Geiler, C., Kauppinen, S., et al. (2002). Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBO Journal, 21, 6681–6688.PubMedCrossRefGoogle Scholar
  13. Catanzariti, A. M., Dodds, P. N., Lawrence, G. J., Ayliffe, M. A., & Ellis, J. G. (2006). Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell, 18, 243–256.PubMedCrossRefGoogle Scholar
  14. Catanzariti, A. M., Dodds, P. N., & Ellis, J. G. (2007). Avirulence proteins from haustoria-forming pathogens. FEMS Microbiology Letters, 269, 181–188.PubMedCrossRefGoogle Scholar
  15. Chisholm, S. T., Dahlbeck, D., Krishnamurthy, N., Day, B., Sjolander, K., & Staskawicz, B. J. (2005). Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proceedings of the National Academy of Sciences of the United States of America, 102, 2087–2089.PubMedCrossRefGoogle Scholar
  16. Chisholm, S. T., Coaker, G., Day, B., & Staskawicz, B. J. (2006). Host-microbe interactions: Shaping the evolution of the plant immune response. Cell, 124, 803–814.PubMedCrossRefGoogle Scholar
  17. Cooper, A. J., Woods-Tör, A., & Holub, E. B. (2002). Albugo candida (White rust) suppresses resistance to downy mildew pathogens in Arabidopsis thaliana. Proceedings 6th Conference of EFPP, Plant Protection Science, 38 (Special issue), 474–476.Google Scholar
  18. Dangl, J. L. (2007). Plant science. Nibbling at the plant cell nucleus. Science, 315, 1088–1089.PubMedCrossRefGoogle Scholar
  19. Daxberger, A., Nemak, A., Mithofer, A., Fliegmann, J., Ligterink, W., Hirt, H., et al. (2007). Activation of members of a MAPK module in beta-glucan elicitor-mediated non-host resistance of soybean. Planta, 225, 1559–1571.PubMedCrossRefGoogle Scholar
  20. Ellis, J., Catanzariti, A. M., & Dodds, P. (2006). The problem of how fungal and oomycete avirulence proteins enter plant cells. Trends in Plant Science, 11, 61–63.PubMedCrossRefGoogle Scholar
  21. Eulgem, T., Tsuchiya, T., Wang, X. J., Beasley, B., Cuzick, A., Tör, M., et al. (2007). EDM2 is required for RPP7-dependent disease resistance in Arabidopsis and affects RPP7 transcript levels. Plant Journal, 49, 829–839.PubMedCrossRefGoogle Scholar
  22. Fritz-Laylin, L. K., Krishnamurthy, N., Tör, M., Sjolander, K. V., & Jones, J. D. (2005). Phylogenomic analysis of the receptor-like proteins of rice and Arabidopsis. Plant Physiology, 138, 611–623.PubMedCrossRefGoogle Scholar
  23. Felix, G., Duran, J. D., Volko, S., & Boller, T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant Journal, 18, 265–276.PubMedCrossRefGoogle Scholar
  24. Gaulin, E., Jauneau, A., Villalba, F., Rickauer, M., Esquerre-Tugaye, M. T., & Bottin, A. (2002). The CBEL glycoprotein of Phytophthora parasitica var nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. Journal of Cell Science, 115, 4565–4575.PubMedCrossRefGoogle Scholar
  25. Gaulin, E., Drame, N., Lafitte, C., Torto-Alalibo, T., Martinez, Y., Ameline-Torregrosa, C., et al. (2006). Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell, 18, 1766–1777.PubMedCrossRefGoogle Scholar
  26. Gouget, A., Senchou, V., Govers, F., Sanson, A., Barre, A., Rouge, P., et al. (2006). Lectin receptor kinases participate in protein–protein interactions to mediate plasma membrane–cell wall adhesions in Arabidopsis. Plant Physiology, 40, 81–90.Google Scholar
  27. Göker, M., Reithmuller, A., Voglmayr, H., Weiss, M., & Oberwinkler, F. (2004). Phylogeny of Hyaloperonospora based on nuclear ribosomal internal transcribed spacer sequences. Mycological Progress, 3, 83–94.CrossRefGoogle Scholar
  28. Grenville-Briggs, L. J., & van West, P. (2005). The biotrophic stages of oomycete-plant interactions. Advances in Applied Microbiology, 57, 217–243.PubMedCrossRefGoogle Scholar
  29. Guo, J., Jiang, R. H., Kamphuis, L. G., & Govers, F. (2006). A cDNA-AFLP based strategy to identify transcripts associated with avirulence in Phytophthora infestans. Fungal Genetics and Biology, 43, 111–123.PubMedCrossRefGoogle Scholar
  30. Guttman, D. S., Gropp, S. J., Morgan, R. L., & Wang, P. W. (2006). Diversifying selection drives the evolution of the type III secretion system pilus of Pseudomonas syringae. Molecular Biology and Evolution, 23, 2342–2354.PubMedCrossRefGoogle Scholar
  31. Hahn, M. G. (1996). Microbial elicitors and their receptors in plants. Annual Review of Phytopathology, 34, 387–412.PubMedCrossRefGoogle Scholar
  32. Hahn, M., & Mendgen, K. (2001). Signal and nutrient exchange at biotrophic plant fungus interfaces. Current Opinion in Plant Biology, 4, 322–327.PubMedCrossRefGoogle Scholar
  33. Hardham, A. R. (2007). Cell biology of plant–oomycete interactions. Cellular Microbiology, 9, 31–39.PubMedCrossRefGoogle Scholar
  34. Hiller, N. L., Bhattacharjee, S., van Ooij, C., Liolios, K., Harrison, T., Lopez-Estrano, C., et al. (2004). A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science, 306, 1934–1937.PubMedCrossRefGoogle Scholar
  35. Holub, E. B. (2001). The arms race is ancient history in Arabidopsis, the wildflower. Nature Reviews Genetics, 2, 516–527.PubMedCrossRefGoogle Scholar
  36. Holub, E. B. (2006). Evolution of parasitic symbioses between plants and filamentous microorganisms. Current Opinion in Plant Biology, 9, 397–405.PubMedCrossRefGoogle Scholar
  37. Holub, E. B. (2008). Natural history of Arabidopsis thaliana and oomycete symbioses. European Journal of Plant Pathology, (in press).Google Scholar
  38. Huang, S., van der Vossen, E. A., Kuang, H., Vleeshouwers, V. G., Zhang, N., Borm, T. J., et al. (2005). Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant Journal, 42, 251–261.PubMedCrossRefGoogle Scholar
  39. Ingle, R. A., Carstens, M., & Denby, K. J. (2006). PAMP recognition and the plant–pathogen arms race. Bioessays, 28, 880–889.PubMedCrossRefGoogle Scholar
  40. Jones, J. D., & Dangl, J. L. (2006). The plant immune system. Nature, 444, 323–329.PubMedCrossRefGoogle Scholar
  41. Kamoun, S. (2003). Molecular genetics of pathogenic oomycetes. Eukaryotic Cell, 2, 191–199.PubMedCrossRefGoogle Scholar
  42. Kamoun, S. (2006). A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology, 44, 41–60.PubMedCrossRefGoogle Scholar
  43. Kamoun, S. (2007). Groovy times: Filamentous pathogen effectors revealed. Current Opinion in Plant Biology, 10, 358–365.PubMedCrossRefGoogle Scholar
  44. Kemmerling, B., Schwedt, A., Rodriguez, P., Mazzotta, S., Frank, M., Qamar, S. A., et al. (2007). The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Current Biology, 17, 1116–1122.PubMedCrossRefGoogle Scholar
  45. Lee, S. W., Han, S. W., Bartley, L. E., & Ronald, P. C. (2006). Colloquium review. Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proceedings of the National Academy of Sciences of the United States of America, 103, 18395–18400.PubMedCrossRefGoogle Scholar
  46. Lotze, M. T., Zeh, H. J., Rubartelli, A., Sparvero, L. J., Amoscato, A. A., Washburn, N. R., et al. (2007). The grateful dead: Damage associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunological Reviews, 220, 60–82.PubMedCrossRefGoogle Scholar
  47. Medzhitov, R. (2007). Recognition of microorganisms and activation of the immune response. Nature, 449, 819–826.PubMedCrossRefGoogle Scholar
  48. Medzhitov, R., & Janeway, C. A. (2002). Decoding the patterns of self and non-self by the innate immune system. Science, 296, 298–300.PubMedCrossRefGoogle Scholar
  49. Meyers, B. C., Kozik, A., Griego, A., Kuang, H., & Michelmore, R. W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell, 15, 809–834.PubMedCrossRefGoogle Scholar
  50. Mithofer, A., Fliegmann, J., Daxberger, A., Ebel, C., Neuhaus-Url, G., Bhagwat, A. A., et al. (2001). Induction of H(2)O(2) synthesis by beta-glucan elicitors in soybean is independent of cytosolic calcium transients. FEBS Letters, 508, 191–195.PubMedCrossRefGoogle Scholar
  51. Morgan, W., & Kamoun, S. (2007). RXLR effectors of plant pathogenic oomycetes. Current Opinion in Microbiology, 10, 332–338.PubMedCrossRefGoogle Scholar
  52. Mudgett, M. B., & Staskawicz, B. J. (1998). Protein signaling via type III secretion pathways in phytopathogenic bacteria. Current Opinion in Microbiology, 1, 109–114.PubMedCrossRefGoogle Scholar
  53. Nishimura, M. T., Stein, M., Hou, B. H., Vogel, J. P., Edwards, H., & Somerville, S. C. (2003). Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science, 301, 969–972.PubMedCrossRefGoogle Scholar
  54. Nurnberger, T., Nennstiel, D., Jabs, T., Sacks, W. R., Hahlbrock, K., & Scheel, D. (1994). High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell, 78, 449–460.PubMedCrossRefGoogle Scholar
  55. O’Connell, R. J., & Panstruga, R. (2006). Tete a tete inside a plant cell. Establishing compatibility between plants and biotrophic fungi and oomycetes. New Phytologist, 171, 699–718.PubMedCrossRefGoogle Scholar
  56. Pieterse, C. M., van West, P., Verbakel, H. M., Brasse, P. W., van den Berg-Velthuis, G. C., & Govers, F. (1994). Structure and genomic organization of the ipiB and ipiO gene clusters of Phytophthora infestans. Gene, 138, 67–77.PubMedCrossRefGoogle Scholar
  57. Qutob, D., Kamoun, S., & Gijzen, M. (2002). Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant Journal, 32, 361–373.PubMedCrossRefGoogle Scholar
  58. Qutob, D., Kemmerling, B., Brunner, F., Kufner, I., Engelhardt, S., Gust, A. A., et al. (2006). Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell, 18, 3721–3744.PubMedCrossRefGoogle Scholar
  59. Rehmany, A. P., Gordon, A., Rose, L. E., Allen, R. L., Armstrong, M. R., Whisson, S. C., et al. (2005). Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell, 17, 1839–1850.PubMedCrossRefGoogle Scholar
  60. Robatzek, S. (2007). Vesicle trafficking in plant immune responses. Cellular Microbiology, 9, 1–8.PubMedCrossRefGoogle Scholar
  61. Robatzek, S., Chinchilla, D., & Boller, T. (2006). Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes and Development, 20, 537–542.PubMedCrossRefGoogle Scholar
  62. Senchou, V., Weide, R., Carrasco, A., Bouyssou, H., Pont-Lezica, R., Govers, F., et al. (2004). High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif. Cellular and Molecular Life Sciences, 61, 502–509.PubMedCrossRefGoogle Scholar
  63. Shan, W., Cao, M., Leung, D., & Tyler, B. M. (2004). The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator for avirulence on soybean plants carrying resistance gene Rps1b. Molecular PlantMicrobe Interactions, 17, 394–403.PubMedCrossRefGoogle Scholar
  64. Sharp, J. K., Valent, B., & Albersheim, P. (1984). Purification and partial characterization of a beta-glucan fragment that elicits phytoalexin accumulation in soybean. Journal of Biological Chemistry, 259, 11312–11320.PubMedGoogle Scholar
  65. Shen, Q. H., & Schulze-Lefert, P. (2007). Rumble in the nuclear jungle: Compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO Journal, 26, 4293–4301.PubMedCrossRefGoogle Scholar
  66. Shen, K. A., Chin, D. B., Arroyo-Garcia, R., Ochoa, O. E., Lavelle, D. O., Wroblewski, T., et al. (2002). Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Molecular PlantMicrobe Interactions, 15, 251–61.PubMedCrossRefGoogle Scholar
  67. Shen, Q. H., Saijo, Y., Mauch, S., Biskup, C., Bieri, S., Keller, B., et al. (2007). Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses. Science, 315, 1098–1101.PubMedCrossRefGoogle Scholar
  68. Shiu, S. H., Karlowski, W. M., Pan, R., Tzeng, Y. H., Mayer, K. F., & Li, W. H. (2004). Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell, 16, 1220–1234.PubMedCrossRefGoogle Scholar
  69. Sinapidou, E., Williams, K., Nott, L., Bahkt, S., Tör, M., Bittner-Eddy, P., et al. (2004). Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis. Plant Journal, 38, 898–909.PubMedCrossRefGoogle Scholar
  70. Sohn, K. H., Lei, R., Nemri, A., & Jones, J. D. (2007). The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell, 19, 4077–4090. DOI 10.1105/tpc.107.054262.PubMedCrossRefGoogle Scholar
  71. Takahashi, Y., Nasir, K. H., Ito, A., Kanzaki, H., Matsumura, H., Saitoh, H., et al. (2007). A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling and non-host resistance to Pseudomonas cichorii. Plant Journal, 49, 1030–1040.PubMedCrossRefGoogle Scholar
  72. Tör, M., Holub, E. B., Brose, E., Musker, R., Gunn, N., Can, C., et al. (1994). Map positions of three loci in Arabidopsis thaliana associated with isolate-specific recognition of Peronospora parasitica (downy mildew). Molecular Plant-microbe Interactions, 7, 214–222.Google Scholar
  73. Tör, M., Gordon, P., Cuzick, A., Eulgem, T., Sinapidou, E., Mert, F., et al. (2002). Arabidopsis SGT1b is required for defence signaling conferred by several downy mildew (Peronospora parasitica) resistance genes. Plant Cell, 14, 993–1003.PubMedCrossRefGoogle Scholar
  74. Tör, M., Yemm, A., & Holub, E. (2003). Role of proteolysis in R-gene mediated defence in plants. Molecular Plant Pathology, 4, 287–296.CrossRefGoogle Scholar
  75. Tyler, B. M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R. H., Aerts, A., et al. (2006). Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science, 313, 1261–1266.PubMedCrossRefGoogle Scholar
  76. Umemoto, N., Kakitani, M., Iwamatsu, A., Yoshikawa, M., Yamaoka, N., & Ishida, I. (1997). The structure and function of a soybean beta-glucan-elicitor-binding protein. Proceedings of the National Academy of Sciences of the United States of America, 94, 1029–1034.PubMedCrossRefGoogle Scholar
  77. Van Damme, M., Andel, A., Huibers, R. P., Panstruga, R., Weisbeek, P. J., & Van den Ackerveken, G. (2005). Identification of Arabidopsis loci required for susceptibility to the downy mildew pathogen Hyaloperonospora parasitica. Molecular Plant-microbe Interactions, 18, 583–592.PubMedCrossRefGoogle Scholar
  78. Van den Ackerveken, G., Marois, E., & Bonas, U. (1996). Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell. Cell, 87, 1307–1316.PubMedCrossRefGoogle Scholar
  79. van der Biezen, E. A., Juwana, H., Parker, J. E., & Jones, J. D. G. (2000). cDNA-AFLP display for the isolation of Peronospora parasitica genes expressed during infection in Arabidopsis thaliana. Molecular PlantMicrobe Interactions, 13, 895–898.PubMedCrossRefGoogle Scholar
  80. Voegele, R. T., & Mendgen, K. (2003). Rust haustoria: Nutrient uptake and beyond. New Phytologist, 159, 93–100.CrossRefGoogle Scholar
  81. Voegele, R. T, Struck, C., Hahn, M., & Mendgen K. (2001). The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proceedings of the National Academy of Sciences of the United States of America, 98, 8133–8138.PubMedCrossRefGoogle Scholar
  82. Vogel, J., & Somerville, S. (2000). Isolation and characterization of powdery mildew-resistant Arabidopsis mutants. Proceedings of the National Academy of Sciences of the United States of America, 97, 1897–1902.PubMedCrossRefGoogle Scholar
  83. Vogel, J. P., Raab, T. K., Schiff, C., & Somerville, S. C. (2002). PMR6, a pectate lyase-like gene required for powdery mildew susceptibility in Arabidopsis. Plant Cell, 14, 2095–2106.PubMedCrossRefGoogle Scholar
  84. Whisson, S. C., Boevink, P. C., Moleleki, L., Avrova, A. O., Morales, J. G., Gilroy, E. M., et al. (2007). A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature, 450, 115–118.PubMedCrossRefGoogle Scholar
  85. Win, J., Morgan, W., Bos, J., Krasileva, K. V., Cano, L. M., Chaparro-Garcia, A., et al. (2007). Adaptive evolution has targeted the C-Terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell, 19, 2349–2369.PubMedCrossRefGoogle Scholar
  86. Wroblewski, T., Piskurewicz, U., Tomczak, A., Ochoa, O., & Michelmore, R. W. (2007). Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant Journal, 51, 803–818.PubMedCrossRefGoogle Scholar
  87. Xiao, F., Giavalisco, P., & Martin, G. B. (2007). Pseudomonas syringae type III effector AvrPtoB is phosphorylated in plant cells on serine 258, promoting its virulence activity. Journal of Biological Chemistry, 282, 30737–30744.PubMedCrossRefGoogle Scholar
  88. Yamamizo, C., Kuchimura, K., Kobayashi, A., Katou, S., Kawakita, K., Jones, J. D., et al. (2006). Rewiring mitogen-activated protein kinase cascade by positive feedback confers potato blight resistance. Plant Physiology, 140, 681–692.PubMedCrossRefGoogle Scholar
  89. Zipfel, C., & Felix, G. (2005). Plants and animals: A different taste for microbes. Current Opinion in Plant Biology, 8, 353–360.PubMedCrossRefGoogle Scholar
  90. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D., Boller, T., et al. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell, 125, 749–760.PubMedCrossRefGoogle Scholar

Copyright information

© KNPV 2008

Authors and Affiliations

  1. 1.Warwick HRIUniversity of WarwickWarwickUK

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