The zig-zag-zig in oomycete-plant interactions

Molecular Plant Pathology

Volumn 10, Issue 4, 2009, Pages 547-562

  Hein, Ingo ^a   Gilroy, Eleanor M ^a   Armstrong, Miles R ^a   Birch, Paul R J ^a,b  

^a SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALGAL PROTEIN;

GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; OOMYCETES; PATHOGENICITY; PHYSIOLOGY; PLANT; REVIEW;

ALGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; OOMYCETES; PLANTS;

OOMYCETES;

EID: 67249143521     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2009.00547.x     Document Type: Review

References (131)

1. Abramovitch, R.B. and Martin, G.B. (2004) Strategies used by bacterial pathogens to suppress plant defenses. Curr. Opin. Plant Biol. 7, 356364.
2. Allen, R.L., Bittner-Eddy, P.D., Grenville-Briggs, L.J., Meitz, J.C., Rehmany, A.P., Rose, L.E. and Beynon, J.L. (2004) Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science, 306, 1957-1960.
3. Allen, R.L., Meitz, J.C., Baumber, R.E., Hall, S.A., Lee, S.C, Rose, L.E. and Beynon, J.L. (2008) Natural variation reveals key amino acids in a downy mildew effector that alters recognition specificity by an Arabidopsis resistance gene. Mol. Plant Pathol. 9, 511-523.
4. Armstrong, M.R., Whisson, S.C., Pritchard, L., Bos, J.I., Venter, E., Avrova, A.O., Rehmany, A.P., Böhme, U., Brooks, K., Cherevach, I., Hamlin, N., White, B., Fraser, A., Lord, A., Quail, M.A., Churcher, C., Hall, N., Berriman, M., Huang, S., Kamoun, S., Beynon, J.L. and Birch, P.R.J. (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. USA, 102, 7766-7771.
5. Attard, A., Gourgues, M., Galiana, E., Panabières, F., Ponchet, M. and Keller, H. (2008) Strategies of attack and defense in plant-oomycete interactions, accentuated for Phytophthora parasitica Dastur (syn. P. Nicotianae Breda de Haan) J. Plant Physiol. 165, 83-94.
6. Bailey, B.A. (1995) Purification of a protein from culture filtrates of Fusarium oxysporum that induces ethylene and necrosis in leaves of Erythroxylum coca. Phytopathology, 85, 1250-1255.
7. Bakker, E.G., Toomajian, C., Kreitman, M. and Bergelson, J. (2006) A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell, 18, 1803-1818.
8. Ballvora, A., Ercolano, M.R., Weiss, J., Meksem, K., Bormann, C.A., Oberhagemann, P., Salamini, F. and Gebhardt, C. (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 J. 30, 361-371.
9. Bartinicki-Garcia, S. and Wang, M.C (1983) Biochemical aspects of morphogenesis in Phytophthora. In: Phytophthora: Its Biology, Taxonomy, Ecology and Pathology (Bartinicki-Garcia S. and Tsao P.H., eds), pp. 121-137. St. Paul, MN: American Phytopathological Society.
10. Belkhadir, Y., Subramaniam, R. and Dangl, J.L. (2004) Plant disease resistance protein signaling: NBS-LRR proteins and their partners, Curr. Opin. Plant Biol. 7, 391-399.
11. Bergelson, J., Kreitman, M., Stahl, E.A. and Tian, D. (2001) Evolutionary dynamics of plant R-genes, Science, 292, 2281-2285.
12. Bhattacharjee, S., Hiller, N.L., Liolios, K., Win, J., Kanneganti, T.D., Young, C., Kamoun, S. and Haldar, K. (2006) The malarial hosttargeting signal is conserved in the Irish potato famine pathogen. PLoS Pathog. 2, e50.
13. van der Biezen, E.A., Freddle, C.T., Kahn, K., Parker, J.E. and Jones, J.D. (2002) Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components, Plant J. 29, 439-451.
14. van der Biezen, E.A. and Jones, J.D.G. (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23, 454456.
15. Birch, P.R.J., Boevink, P.C., Gilroy, E.M., Hein, I., Pritchard, L. and Whisson, S.C (2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr. Opin. Plant Biol. 11, 373-379.
16. Birch, P.R.J, and Cooke, D.E.L. (2004) Mechanisms of infectionoomycetes. In: Encyclopedia of Plant and Crop Science (Goodman, R.M., ed.), pp. 697-700. New York, NY: Marcel Dekker Inc.
17. Birch, P.R.J., Rehmany, A.P., Pritchard, L., Kamoun, S. and Beynon, J.L. (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol. 14, 8-11.
18. Bittner-Eddy, P.D., Crute, I.R., Holub, E.B. and Beynon, J.L. (2000) RPP13 is a simple locus in Arabidopsis thaliana for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. Plant J. 21, 177-188.
19. Blair, J.E., Coffey, M.D., Park, S-Y., Geiser, D.M. and Kang, S. (2008) A multi-locus phylogeny for Phytophthora utilizing markers from complete genome sequences. Fungal Genet. Biol. 45, 266-277.
20. Block, A., Li, G., Fu, Z.Q. and Alfano, J.R. (2008) Phytopathogen type III effector weaponry and their plant targets. Curr. Opin. Plant Biol. 11, 396-403.
21. Bos, J.L, Kanneganti, T.D., Young, C., Cakir, C., Huitema, E., Win, J., Armstrong, M.R., Birch, P.R. and Kamoun, S. (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 J. 48, 165-176.
22. Botella, M.A., Parker, J.E., Frost, L.N., Bittner-Eddy, P.D., Beynon, J.L., Daniels, M.J., Holub, E.B. and Jones, J.D.G. (1998) Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants, Plant Cell, 10, 18471860.
23. Brunner, F., Rosahl, S., Lee, J., Rudd, J.J., Geiler, C., Kauppinen, S., Rasmussen, G., Scheel, D. and Nürnberger, T. (2002) Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. EMBOJ. 21, 6681-6688.
24. Chisholm, S.T., Coaker, G., Day, B. and Staskawicz, B.J. (2006) Hostmicrobe interactions: shaping the evolution of the plant immune response. Cell, 124, 803-814.
25. Damasceno, C.M.B., Bishop, J.G., Ripoll, D.R., Win, J., Kamoun, S. and Rose, J.K.C (2008) Structure of the glucanase inhibitor protein (GIP) family from Phytophthora species suggests coevolution with plant endoß-1,3- glucanases, Mol. Plant-Microbe Interact. 21, 820-830.
26. Dangl, J.L. and Jones, J.D. (2001) Plant pathogens and integrated defence responses to infection. Nature, 411, 826-833.
27. Ding, J., Zhang, W., Jing, Z., Chen, J.Q. and Tian, D. (2007) Unique pattern of R-gene variation within populations in Arabidopsis, Mol. Gen. Genom. 277, 619-629.
28. Dou, D., Kale, S.D., Wang, X., Chen, Y., Wang, Q., Wang, X., Jiang, R.X.Y., Arredondo, F.D., Anderson, R.G., Thakur, P.B., McDowell, J.M., Wang, Y. and Tyler, B.M. (2008b) Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell, 20, 1118-1133.
29. Dou, D., Kale, S.D., Wang, X., Jiang, R.H.Y., Bruce, N.A., Arredondo, F.D., Zhang, X. and Tyler, B.M. (2008a) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery, Plant Cell, 20, 1930-1947.
30. Dumas, B., Bottin, A., Gaulin, E. and Esquerré-Tugayé, M.T. (2008) Cellulose-binding domains: cellulose associated-defensive sensing partners? Trends Plant Sci. 13, 160-164.
31. Ellis, C. and Turner, J.G. (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell, 13, 1025-1033.
32. Eulgem, T., Tsuchiya, T., Wang, X.J., Beasley, B., Cuzick, A., Tor, M., Zhu, T., McDowell, J.M., Holub, E. and Dangl, J.L. (2007) EDM2 is required for RPP7-dependent disease resistance in Arabidopsis and affects RPP7 transcript levels. Plant J. 49, 829-839.
33. Felix, G. and Boiler, T. (2003) Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco, J. Biol. Chem. 278, 6201-6208.
34. Felix, G., Duran, J.D., Volko, S. and Boiler, T. (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276.
35. Fellbrich, G., Romanski, A., Varet, A., Blume, B., Brunner, F., Engelhardt, S., Felix, G., Kemmerling, B., Krzymowska, M. and Nürnberger, T. (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J. 32, 375-390.
36. Flor, H.H. (1971) Current status of the gene-for-gene concept. Ann. Rev. Phytopathol. 9, 275-296.
37. Friedman, A.R. and Baker, B.J. (2007) The evolution of resistance genes in multi-protein plant resistance systems. Curr. Opin. Gen. Dev. 17, 493-499.
38. Gaulin, E., Draimé, N., Lafitte, C., Torto-Alallbo, T., Martinez, Y., Ameline-Torregrosa, C., Khatib, M., Mazarguil, H., VillalbaMateos, F., Kamoun, S., Mazars, C., Dumas, B., Bottin, A., EsquerréTugayé, M.T. and Rickauer, M. (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell, 18, 1766-1777.
39. Gaulin, E., Jauneau, A., Villalba, F., Rickauer, M., Esquerré- Tugayé, M.T. and Bottin, A. (2002) The CBEL glycoprotein of Phytophthora parasitica var-nicotianae is involved in cell wall deposition and adhesion to cellulosic substrates. J. Cell Sci. 115, 4565-4575.
40. Gijzen, M. and Nürnberger, T. (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry, 67, 1800-1807.
41. Göker, M., Voglmayer, H., Riethmuller, A. and Oberwinkler, F. (2006) How do obligate parasites evolve? A multi-gene phylogenetic analysis of downy mildews, Fungal Genet. Biol. 44, 105122.
42. Grant, S.R., Fisher, E.J., Chang, J.H., Mole, B.M. and Dangl, J.L. (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu. Rev. Microbiol. 60, 425-449.
43. Grouffaud, S., van West, P., Avrova, A.O., Birch, P.R.J, and Whisson, S.C. (2008) Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology, 154, 3743-3751.
44. Hardham, A.R. (2007) Cell biology of plant-oomycete interactions. Cell. Microbiol. 9, 31-39.
45. Heese, A., Hann, D.R., Gimenez-lbanez, S., Jones, A.M., He, K., Li J., Schroeder, J.I., Peck, S.C. and Rathjen, J.P. (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA, 104, 12 217-12 222.
46. Hiller, N.L., Bhattacharjee, S., van Ooij, C., Liolios, K., Harrison, T., Lopez-Estrano, C and Haldar, K. (2004) A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science, 306, 1934-1937.
47. Holub, E.B. (2001) The arms race is ancient history in Arabidopsis, the wildflower, Nat Rev. Genet. 2, 516-527.
48. van der Hoorn, R.A.L. and Kamoun, S. (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell, 20, 2009-2017.
49. Huang, S. (2005) The discovery and characterization of the major late blight resistance complex in potato-genomic structure, functional diversity, and implications. PhD Thesis. Wageningen University, The Netherlands.
50. Huang, S., Vleeshouwers, V.G., Werij, J.S., Hutten, R.C., van Eck, H.J., Visser, R.G. and Jacobsen, E. (2004) The R3 resistance to Phytophthora infestans in potato is conferred by two closely linked R genes with distinct specificities, Mol. Plant-Microbe Interact. 17, 428-435.
51. Huang, S., van der Vossen, E.A., Kuang, H., Vleeshouwers, V.G., Zhang, N., Borm, T.J., van Eck, H.J., Baker, B., Jacobsen, E. and Visser, R.G. (2005) Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J. 42, 251-261.
52. Ingle, R.A., Carstens, M. and Denby, K.J. (2006) PAMP recognition and the plant-pathogen arms race. Bioessays, 28, 880-889.
53. Jiang, R.H.Y., Tripathy, S., Govers, F. and Tyler, B.M. (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members, Proc. Natl. Acad. Sci. USA, 105, 4874-4879.
54. Jones, J.D. and Dangl, J.L. (2006) The plant immune system. Nature, 444, 323-329.
55. Kamoun, S. (2003) Molecular genetics of phytopathogenic oomycetes, Eukaryotic Cell, 2, 191-199.
56. Kamoun, S. (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annu. Rev. Phytopathol. 44, 41-60.
57. Kamoun, S. (2007) Groovy times: filamentous pathogen effectors revealed. Curr. Opin. Plant Biol. 10, 358-365.
58. Kamoun, S., Huitema, E. and Vleeshouwers, V.G. (1999) Resistance to oomycetes: a general role for the hypersensitive response? Trends Plant Sci. 4, 196-200.
59. Kanzaki, H., Saitoh, H., Ito, A., Fujisawa, S., Kamoun, S., Katou, S., Yoshioka, H. and Terauchi, R. (2003) Cytosolic HSP90 and HSP70 are essential components of INF1-mediated hypersensitive response and non-host resistance to Pseudomonas cichorii in Nicotiana benthamiana. Mol. Plant Pathol. 4, 383-391.
60. Kanzaki, H., Saitoh, H., Takahashi, Y., Berberich, T., Ito, A., Kamoun, S. and Terauchi, R. (2008) NbLRKI, a lectin-like receptor kinase protein of Nicotiana benthamiana, interacts with Phytophthora infestans INF1 elicitin and mediates INF1-induced cell death. Planta, 228, 977-987.
61. Koch, E. and Slusarenko, A. (1990) Arabidopsis is susceptible to Infection by a downy mildew fungus. Plant Cell, 2, 437-445.
62. Kuang, H., Ochoa, O.E., Nevo, E. and Michelmore, R.W. (2006) The disease resistance gene Dm3 is infrequent in natural populations of Lactuca serriola due to deletions and frequent gene conversions at the RGC2 locus. Plant J. 47, 38-48.
63. Kuang, H., Wei, F., Marano, M.R., Wirtz, U., Wang, X., Liu, J., Shum, W.P., Zaborsky, J., Talion, L.J., Rensink, W., Lobst, S., Zhang, P., Tornqvist, C.E., Tek, A., Bamberg, J., Helgeson, J., Fry, W., You, F., Luo, M.C., Jiang, J., Robin Buell, C. and Baker, B. (2005) The R1 resistance gene cluster contains three groups of independently evolving type IR1 homologues and shows substantial structural variation among haplotypes of Solanum demissum. Plant J. 44, 37-51.
64. Kuang, H., Woo, S.S., Meyers, B.C., Nevo, E. and Michelmore, R.W. (2004) Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell, 16, 2870-2894.
65. Lamour, K.H., Win, J. and Kamoun, S. (2007) Oomycete genomics: new insights and future directions. FEMS Microbiol. Lett. 274, 1-8.
66. Langston, J., Blinkovsky, A., Byun, T., Terribilini, M., Ransbarger, D. and Xu, F. (2007) Substrate specificity of Streptomyees transglutaminases. Appl. Bioehem. Biotechnol. 136, 291-308.
67. Latijnhouwers, M., de Wit, P.J. and Govers, F. (2003) Oomycetes and fungi: similar weaponry to attack plants. Trends Microbiol. 11, 462469.
68. Lehmann, P. (2002) Structure and evolution of plant disease resistance genes J. Appl. Genet. 43, 403-414.
69. Levesque, C.A. and de Cock, W.A.M. (2004) Molecular phylogeny and taxonomy of the genus Pythium. Mycol. Res. 108, 1363-1383.
70. Liu, Z., Bos, J.I.B., Armstrong, M., Whisson, S.C, da Cunha, L., Torto, T., Win, J., Avrova, A.O., Wright, F., Birch, P.R.J, and Kamoun, S. (2005) Patterns of diversifying selection in the phytotoxin-like scr74 gene family of Phytophthora infestans. Mol. Biol. Evol. 22, 659-672.
71. van Loon, L.C, Rep, M. and Pieterse, C.M.J. (2006) Significance of inducible defense-related proteins in infected plants, Annu. Rev. Phytopathol. 44, 135-162.
72. Marti, M., Good, R.T., Rug, M., Knuepfer, E. and Cowman, A.F. (2004) Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science, 306, 1930-1933.
73. Mateos, F.V., Rickauer, M. and Esquerré-Tugayé, M.T. (1997) Cloning and characterization of a cDNA encoding an elicitor of Phytophthora parasitica var. nicotianae that shows cellulose-binding and lectin-like activities. Mol. Plant-Microbe Interact. 10, 1045-1053.
74. McDowell, J.M., Dhandaydham, M., Long, T.A., Aarts, M.G.M., Goff, S., Holub, E.B. and Dangl, J.L. (1998) Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell, 10, 1861-1874.
75. McDowell, J.M. and Simon, S.A. (2006) Recent Insights into R gene evolution, Mol. Plant Pathol. 7, 437-448.
76. Medzhitov, R. and Janeway, C.A. (1997) Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9, 4-9.
77. Meyers, B.C., Chin, D.B., Shen, K.A., Sivaramakrishnan, S., Lavelle, D.O., Zhang, Z. and Michelmore, R.W. (1998b) The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell, 10, 1817-1832.
78. Meyers, B.C., Dickerman, A.W., Michelmore, R.W., Sivaramakrishnan, S., Sobral, B.W. and Young, N.D. (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 20, 317-332.
79. Meyers, B.C., Kozik, A., Griego, A., Kuang, H. and Michelmore, R.W. (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell, 15, 809-834.
80. Meyers, B.C., Shen, K.A., Rohani, P., Gaut, B.S. and Michelmore, R.W. (1998a) Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection, Plant Cell, 10, 1833-1846.
81. Michelmore, R.W. and Meyers, B.C. (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 8, 1113-1130.
82. Nei, M., Gu, X. and Sitnikova, T. (1997) Evolution by the birth-and-death process in multigene families of the vertebrate immune system, Proc. Natl. Acad. Sci. USA, 94, 7799-7806.
83. Nürnberger, T., Brunner, F., Kemmerling, B. and Plater, L. (2004) Innate immunity in plants and animals: striking similarities and obvious differences, Immunol. Rev. 198, 249-266.
84. Nürnberger, T. and Lipka, V. (2005) Non-host resistance in plants: new insights into an old phenomenon. Mol. Plant Pathol. 6, 335-345.
85. Nürnberger, T., Nennstiel, D., Jabs, T., Sacks, W.R., Hahlbrock, K. and Scheel, D. (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell, 78, 449-460.
86. Orosomando, G., Lornzi, M., Raffaelli, N., Dalla Rizza, M., Mezzetti, B. and Ruggieri, S. (2001) Phytotoxic protein PcF: purification, characterisation and cDNA sequencing of a novel hydroxyproline-containing factor secreted by the strawberry pathogen Phytophthora cactorum. J. Biol. Chem. 276, 21 575-21 584.
87. Osman, H., Vauthrin, S., Mikes, V., Milat, M.L., Panabières, F., Marais, A., Brunie, S., Maume, B., Ponchet, M. and Blein, J.P. (2001) Mediation of elicitin activity on tobacco is assumed by elicitin-sterol complexes. Mol. Biol. Cell, 12, 2825-2834.
88. Panabieres, F., Amselem, J., Galiana, E. and Le Berre, J.Y. (2005) Gene identification in the oomycete pathogen Phytophthora parasitica during in vitro vegetative growth through expressed sequence tags. Fungal Genet. Biol. 42, 611-623.
89. Parker, J.E., Coleman, M.J., Szabo, V., Frost, L.N., Schmidt, R., van der Biezen, E.A., Moores, T., Dean, C., Daniels, M.J. and Jones, J.D.G. (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.
90. Peart, J.R., Lu, R., Sadanandom, A., Malcuit, I., Moffett, P., Brice, D.C, Schauser, L., Jaggard, D.A., Xiao, S., Coleman, M.J., Dow, M., Jones, J.D., Shirasu, K. and Baulcombe, D.C. (2002) Ubiquitin ligase-associated protein SGT1 is required for host and nonhost disease resistance in plants. Proc. Natl. Acad. Sci. USA, 99, 10 86510 869.
91. Pemberton, C.L., Whitehead, N.A., Sebaihia, M., Bell, K.S., Hyman, L.J., Harris, S.J., Matlin, A.J., Robson, N.D., Birch, P.R.J., Carr, J.P., Toth, I.K. and Salmond, G.P.S. (2005) Novel quorum-sensingcontrolled genes in Erwinia carotovora subsp. carotovora: identification of a fungal elicitor homologue in a soft-rotting bacterium, Mol. PlantMicrobe. Interact. 18, 343-353.
92. Pieterse, C.M., van West, P., Verbakel, H.M., Brasse, P.W., van den Berg-Velthuls, G.C and Govers, F. (1994) Structure and genomic organization of the ipiB and ipiO gene clusters of Phytophthora infestans. Gene, 138, 67-77.
93. van Poppel, P.M.J.A., Guo, J., van de Vondervoort, P.J.I., Jung, M.W.M., Birch, P.R.J., Whisson, S.C. and Govers, F. (2008) The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector, Mol. Plant-Microbe Interact. 21, 1460-1470.
94. Qutob, D., Kamoun, S. and Gijzen, M. (2002) Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J. 32, 361-373.
95. Qutob, D., Kemmerling, B., Brunner, F., Küfner, I., Engelhardt, S., Gust, A.A., Luberacki, B., Seitz, H.U., Stahl, D., Rauhut, T., Glawischnig, E., Schween, G., Lacombe, B., Watanabe, N., Lam, E., Schlichting, R., Scheel, D., Nau, K., Dodt, G., Hubert, D., Gijzen, M. and Nürnberger, T. (2006) Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell, 18, 3721-3744.
96. Rehmany, A.P., Gordon, A., Rose, L.E., Allen, R.L., Armstrong, M.R., Whisson, S.C., Kamoun, S., Tyler, B.M., Birch, P.R. and Beynon, J.L. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines, Plant Cell, 17, 1839-1850.
97. Rentel, M.C., Leonelli, L., Dahlbeck, D., Zhao, B. and Staskawicz, B.J. (2008) Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proc. Natl. Acad. Sci. USA, 105, 1091-1096.
98. Robold, A.V. and Hardham, A.R. (2005) During attachment Phytophthora spores secrete proteins containing thrombospondin type 1 repeats. Curr. Genet. 47, 307-315.
99. Rose, J.K., Ham, K.S., Darvill, A.G. and Albersheim, P. (2002) Molecular cloning and characterization of glucanase inhibitor proteins: co-evolution of a counter-defense mechanism by plant pathogens, Plant Cell, 14, 1329-1345.
100. Rose, L.E., Bittner-Eddy, P.D., Langley, C.H., Holub, E.B., Michelmore, R.W. and Beynon, J.L. (2004) The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics, 166, 1517-1527.
101. 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.
102. Shabab, M., Shindo, T., Gu, C., Kaschani, F., Pansuriya, T., Chintha, R., Harzen, A., Colby, T., Kamoun, S. and van der Hoorn, R.A.L. (2008) Fungal effector protein AVR2 targets diversifying defense-related cys proteases of tomato. Plant Cell, 20, 1169-1183.
103. Shan, W., Cao, M., Leung, D. and Tyler, B.M. (2004) The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b Mol. Plant-Microbe interact. 17, 394-403.
104. Sharp, J.K., Valent, B. and Albersheim, P. (1984) Purification and partial characterisation of a beta-glucan fragment that elicits phytoalexin accumulation in soybean. J. Biol. Chem. 259, 11 312-11 320.
105. Shen, K.A., Chin, D.B., Arroyo-Garcia, R., Ochoa, O.E., Lavelle, D.O., Wroblewskl, T., Meyers, B.C. and Mlchelmore, R.W. (2002) Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol. Plant-Microbe Interact. 15, 251-261.
106. Sinapidou, E., Williams, K., Nott, L., Bahkt, S., Tor, M., Crute, I., Bittner-Eddy, P. and Beynon, J. (2004) Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis, Plant J. 38, 898-909.
107. Slusarenko, A.J. and Schlaich, N.L. (2003) Downy mildew of Arabidopsis thaliana caused by Hyaloperonospora parasitica (formerly Peronospora parasitica). Mol. Plant Pathol. 4, 159-170.
108. Sohn, K.H., Lei, R., Nemri, A. and Jones, D.G. (2007) The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell, 19, 4077-4090.
109. 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.
110. Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M., van der Hoorn, R. and Kamoun, S. (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defence protease Rcr3. Proc. Natl. Acad. Sci. USA, 106, 1654-1659.
111. Stahl, E.A., Dwyer, G., Mauricio, R., Kreitman, M. and Bergelson, J. (1999) Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature, 400, 667-671.
112. Takahashi, Y., Nasir, K.H., Ito, A., Kanzaki, H., Matsumura, H., Saitoh, H., Fujisawa, S., Kamoun, S. and Terauchi, R. (2007) A highthroughput 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 J. 49, 1030-1040.
113. Tian, M., Benedetti, B. and Kamoun, S. (2005) A second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato, Plant Physiol. 138, 1785-1793.
114. Tian, M., Huitema, E., da Cunha, L., Torto-Alalibo, T. and Kamoun, S. (2004) A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J. Biol. Chem. 279, 26 370-26 377.
115. Tian, M., Win, J., Song, J., van der Hoorn, R., van der Knaap, E. and Kamoun, S. (2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease, Plant Physiol. 143, 364-377.
116. Torto, T.A., Li, S., Styer, A., Huitema, E., Testa, A., Gow, N.A., van West, P. and Kamoun, S. (2003) EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Res. 13, 1675-1685.
117. Torto-Alalibo, T., Tian, M., Gajendran, K., Waugh, M.E., van West, P. and Kamoun, S. (2005) Expressed sequence tags from the oomycete fish pathogen Saprolegnia parasitica reveal putative virulence factors, BMC Microbiol. 5, 46.
118. Tyler, B.M., Tripathy, S., Zhang, X., Dehal, P., Jiang, R.H., Aerts, A., Arredondo, F.D., Baxter, L., Bensasson, D., Beynon, J.L., Chapman, J., Damasceno, C.M., Dorrance, A.E., Dou, D., Dickerman, A.W., Dubchak, I.L., Garbelotto, M., Gijzen, M., Gordon, S.G., Govers, F., Grunwald, N.J., Huang, W., Ivors, K.L., Jones, R.W., Kamoun, S., Krampis, K., Lamour, K.H., Lee, M.K., McDonald, W.H., Medina, M., Meijer, H.J., Nordberg, E.K., Maclean, D.J., Ospina-Giraldo, M.D., Morris, P.F., Phuntumart, V., Putnam, N.H., Rash, S., Rose, J.K., Sakihama, Y., Salamov, A.A., Savidor, A., Scheuring, C.F., Smith, B.M., Sobral, B.W., Terry, A., Torto-Alalibo, T.A., Win, J., Xu, Z., Zhang, H., Grigoriev, I.V., Rokhsar, D.S. and Boore, J.L. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis, Science, 313, 1261-1266.
119. Umemoto, N., Kakitani, M., Iwamatsu, A., Yoshikawa, M., Yamaoka, M. and lshida, I. (1997) The structure and function of a soybean beta glucan-elicitor binding protein. Proc. Natl. Acad. Sci. USA, 94, 10291034.
120. Vauthrin, S., Mikes, V., Milat, M.L., Ponchet, M., Maume, B., Osman, H. and Blein, J.P. (1999) Elicitins trap and transfer sterols from micelles, liposomes and plant plasma membranes. Biochim. Biophys. Acta, 1419, 335-342.
121. Vleeshouwers, V.G., Rietman, H., Krenek, P., Champouret, N., Young, C., Oh, S.K., Wang, M., Bouwmeester, K., Vosman, B., Visser, R.G., Jacobsen, E., Govers, F., Kamoun, S. and Van der Vossen, E.A. (2008) Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes, PLoS ONE 3, e2875.
122. van der Vossen, E., Gros, J., Sikkema, A., Muskens, M., Wouters, D., Wolters, P., Pereira, A. and Allefs, S. (2005) The Rpi-blb2 gene from Solanum bulbocastanum is an Mi-1 gene homolog conferring broadspectrum late blight resistance in potato. Plant J. 44, 208-222.
123. van der Vossen, E., Sikkema, A., Hekkert, B.L., Gros, J., Stevens, P., Muskens, M., Wouters, D., Pereira, A., Stiekema, W. and Allefs, S. (2003) An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 36, 867-382.
124. Wang, M., Allefs, S., van den Berg, R.G., Vleeshouwers, V.G., van der Vossen, E.A.G. and Vosman, B. (2008) Allele mining in Solanum: conserved homologues of Rpi-blb1 are identified in Solanum stoloniferum. Theor. Appl. Genet. 116, 933-943.
125. van West, P., de Jong, A.J., Judelson, H.S., Emons, A.M. and Govers, F. (1998) The ipiO gene of Phytophthora infestans is highly expressed in invading hyphae during infection. Fungal Genet. Biol. 23, 126138.
126. Whisson, S.C., Boevink, P.C., Moleleki, L., Avrova, A.O., Morales, J.G., Gilroy, E.M., Armstrong, M.R., Grouffaud, S., van West, P., Chapman, S., Hein, I., Toth, I.K., Pritchard, L. and Birch, P.R.J. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature, 450, 115-119.
127. Win, J., Kanneganti, T.D., Torto-Alalibo, T. and Kamoun, S. (2006) Computational and comparative analyses of 150 full-length cDNA sequences from the oomycete plant pathogen Phytophthora infestans. Fungal Genet. Biol. 43, 20-23.
128. Win, J., Morgan, W., Bos, J., Krasileva, K.V., Cano, L.M., ChaparroGarcia, A., Ammar, R., Staskawicz, B.J. and Kamoun, S. (2007) Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell, 19, 23492369.
129. Yi, H. and Richards, E.J. (2007) A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing, Plant Cell, 19, 2929-2939.
130. Yoshioka, H., Numata, N., Nakajima, K., Katou, S., Kawakita, K., Rowland, O., Jones, J.D. and Doke, N. (2003) Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H202 accumulation and resistance to Phytophthora infestans. Plant Cell, 15, 706718.
131. Zipfel, C. (2008) Pattern-recognition receptors in plant innate immunity, Curr. Opin. Immun. 20, 10-16.