Brothers in arms? Common and contrasting themes in pathogen perception by plant NB-LRR and animal NACHT-LRR proteins

Microbes and Infection

Volumn 9, Issue 5, 2007, Pages 677-686

  Rairdan, Greg ^a   Moffett, Peter ^a,b  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

NACHT LRR; NBS LRR; NOD LRR; R gene; STAND ATPase

Indexed keywords

LEUCINE; NACHT LRR PROTEIN; NB LRR PROTEIN; NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL DISEASE; ANIMAL GENETICS; CONVERGENT EVOLUTION; DISEASE RESISTANCE; GENOME; MICROORGANISM DETECTION; NONHUMAN; PATHOGENESIS; PLANT DISEASE; PLANT GENETICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; SHORT SURVEY;

ANIMALS; IMMUNITY, NATURAL; PLANT PROTEINS; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 34247115054     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2007.01.019     Document Type: Short Survey

References (94)

1. Litman G.W., Cannon J.P., and Rast J.P. New insights into alternative mechanisms of immune receptor diversification. Adv. Immunol. 87 (2005) 209-236
2. Zipfel C., and Felix G. Plants and animals: a different taste for microbes?. Curr. Opin. Plant Biol. 8 (2005) 353-360
3. van der Biezen E.A., and Jones J.D. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr. Biol. 8 (1998) R226-R227
4. Meyers B.C., Kozik A., Griego A., Kuang H., and Michelmore R.W. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15 (2003) 809-834
5. Bai J., Pennill L.A., Ning J., Lee S.W., Ramalingam J., Webb C.A., Zhao B., Sun Q., Nelson J.C., Leach J.E., and Hulbert S.H. Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res. 12 (2002) 1871-1884
6. Mucyn T.S., Clemente A., Andriotis V.M., Balmuth A.L., Oldroyd G.E., Staskawicz B.J., and Rathjen J.P. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell (2006)
7. Tuskan G.A., Difazio S., Jansson S., Bohlmann J., Grigoriev I., Hellsten U., Putnam N., Ralph S., Rombauts S., Salamov A., Schein J., Sterck L., Aerts A., Bhalerao R.R., Bhalerao R.P., Blaudez D., Boerjan W., Brun A., Brunner A., Busov V., Campbell M., Carlson J., Chalot M., Chapman J., Chen G.L., Cooper D., Coutinho P.M., Couturier J., Covert S., Cronk Q., Cunningham R., Davis J., Degroeve S., Dejardin A., Depamphilis C., Detter J., Dirks B., Dubchak I., Duplessis S., Ehlting J., Ellis B., Gendler K., Goodstein D., Gribskov M., Grimwood J., Groover A., Gunter L., Hamberger B., Heinze B., Helariutta Y., Henrissat B., Holligan D., Holt R., Huang W., Islam-Faridi N., Jones S., Jones-Rhoades M., Jorgensen R., Joshi C., Kangasjarvi J., Karlsson J., Kelleher C., Kirkpatrick R., Kirst M., Kohler A., Kalluri U., Larimer F., Leebens-Mack J., Leple J.C., Locascio P., Lou Y., Lucas S., Martin F., Montanini B., Napoli C., Nelson D.R., Nelson C., Nieminen K., Nilsson O., Pereda V., Peter G., Philippe R., Pilate G., Poliakov A., Razumovskaya J., Richardson P., Rinaldi C., Ritland K., Rouze P., Ryaboy D., Schmutz J., Schrader J., Segerman B., Shin H., Siddiqui A., Sterky F., Terry A., Tsai C.J., Uberbacher E., Unneberg P., Vahala J., Wall K., Wessler S., Yang G., Yin T., Douglas C., Marra M., Sandberg G., Van de Peer Y., and Rokhsar D. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313 (2006) 1596-1604
8. Martin G.B., Bogdanove A.J., and Sessa G. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54 (2003) 23-61
9. Inohara N., Chamaillard M., McDonald C., and Nunez G. NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74 (2005) 355-383
10. Ting J.P., and Davis B.K. CATERPILLER: a novel gene family important in immunity, cell death, and diseases. Annu. Rev. Immunol. 23 (2005) 387-414
11. Harton J.A., Linhoff M.W., Zhang J., and Ting J.P. Cutting edge: CATERPILLER: a large family of mammalian genes containing CARD, pyrin, nucleotide-binding, and leucine-rich repeat domains. J. Immunol. 169 (2002) 4088-4093
12. Kufer T.A., Fritz J.H., and Philpott D.J. NACHT-LRR proteins (NLRs) in bacterial infection and immunity. Trends Microbiol. 13 (2005) 381-388
13. Kohl A., and Grutter M.G. Fire and death: the pyrin domain joins the death-domain superfamily. C. R. Biol. 327 (2004) 1077-1086
14. Fortier A., Diez E., and Gros P. Naip5/Birc1e and susceptibility to Legionella pneumophila. Trends Microbiol. 13 (2005) 328-335
15. Steimle V., Otten L.A., Zufferey M., and Mach B. Complementation cloning of an MHC class II transactivator mutated in hereditary MHC class II deficiency (or bare lymphocyte syndrome). Cell 75 (1993) 135-146
16. Martinon F., Agostini L., Meylan E., and Tschopp J. Identification of bacterial muramyl dipeptide as activator of the NALP3/Cryopyrin inflammasome. Curr. Biol. 14 (2004) 1929-1934
17. Amer A., Franchi L., Kanneganti T.D., Body-Malapel M., Ozoren N., Brady G., Meshinchi S., Jagirdar R., Gewirtz A., Akira S., and Nunez G. Regulation of Legionella phagosome maturation and infection through flagellin and host IPAF. J. Biol. Chem. (2006)
18. Franchi L., Amer A., Body-Malapel M., Kanneganti T.D., Ozoren N., Jagirdar R., Inohara N., Vandenabeele P., Bertin J., Coyle A., Grant E.P., and Nunez G. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat. Immunol. 7 (2006) 576-582
19. Zamboni D.S., Kobayashi K.S., Kohlsdorf T., Ogura Y., Long E.M., Vance R.E., Kuida K., Mariathasan S., Dixit V.M., Flavell R.A., Dietrich W.F., and Roy C.R. The Birc1e cytosolic pattern-recognition receptor contributes to the detection and control of Legionella pneumophila infection. Nat. Immunol. 7 (2006) 318-325
20. Viala J., Chaput C., Boneca I.G., Cardona A., Girardin S.E., Moran A.P., Athman R., Memet S., Huerre M.R., Coyle A.J., Distefano P.S., Sansonetti P.J., Labigne A., Bertin J., Philpott D.J., and Ferrero R.L. Nod1 responds to peptidoglycan delivered by the Helicobacter pylori cag pathogenicity island. Nat. Immunol. 5 (2004) 1166-1174
21. Leipe D.D., Koonin E.V., and Aravind L. STAND a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. J. Mol. Biol. 343 (2004) 1-28
22. Tameling W.I., Elzinga S.D., Darmin P.S., Vossen J.H., Takken F.L., Haring M.A., and Cornelissen B.J. The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14 (2002) 2929-2939
23. Tameling W.I., Vossen J.H., Albrecht M., Lengauer T., Berden J.A., Haring M.A., Cornelissen B.J., and Takken F.L. Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol. 140 (2006) 1233-1245
24. Albrecht M., and Takken F.L. Update on the domain architectures of NLRs and R proteins. Biochem. Biophys. Res. Commun. 339 (2006) 459-462
25. Mestre P., and Baulcombe D.C. Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 18 (2006) 491-501
26. Brown J., Rogers E., and Boss J. The MHC class II transactivator (CIITA) requires conserved leucine charged domains for interactions with the conserved W box promoter element. Nucleic Acids Res. 26 (1998) 4128-4136
27. Meyers B.C., Dickerman A.W., Michelmore R.W., Sivaramakrishnan S., Sobral B.W., and Young N.D. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 20 (1999) 317-332
28. Koonin E.V., and Aravind L. The NACHT family - a new group of predicted NTPases implicated in apoptosis and MHC transcription activation. Trends Biochem. Sci. 25 (2000) 223-224
29. Rairdan G.J., and Moffett P. Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18 (2006) 2082-2093
30. Riedl S.J., Li W., Chao Y., Schwarzenbacher R., and Shi Y. Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 434 (2005) 926-933
31. Bendahmane A., Farnham G., Moffett P., and Baulcombe D.C. Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J. 32 (2002) 195-204
32. Howles P., Lawrence G., Finnegan J., McFadden H., Ayliffe M., Dodds P., and Ellis J. Autoactive alleles of the flax L6 rust resistance gene induce non-race-specific rust resistance associated with the hypersensitive response. Mol. Plant Microbe Interact. 18 (2005) 570-582
33. Miao E.A., Alpuche-Aranda C.M., Dors M., Clark A.E., Bader M.W., Miller S.I., and Aderem A. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat. Immunol. 7 (2006) 569-575
34. Mariathasan S., Weiss D.S., Newton K., McBride J., O'Rourke K., Roose-Girma M., Lee W.P., Weinrauch Y., Monack D.M., and Dixit V.M. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440 (2006) 228-232
35. Martinon F., Petrilli V., Mayor A., Tardivel A., and Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440 (2006) 237-241
36. Kanneganti T.D., Ozoren N., Body-Malapel M., Amer A., Park J.H., Franchi L., Whitfield J., Barchet W., Colonna M., Vandenabeele P., Bertin J., Coyle A., Grant E.P., Akira S., and Nunez G. Bacterial RNA and small antiviral compounds activate caspase-1 through cryopyrin/Nalp3. Nature 440 (2006) 233-236
37. Kanneganti T.D., Body-Malapel M., Amer A., Park J.H., Whitfield J., Taraporewala Z.F., Miller D., Patton J.T., Inohara N., and Nunez G. Critical role for cryopyrin/Nalp3 in activation of caspase-1 in response to viral infection and double-stranded RNA. J. Biol. Chem. (2006)
38. Sutterwala F.S., Ogura Y., Szczepanik M., Lara-Tejero M., Lichtenberger G.S., Grant E.P., Bertin J., Coyle A.J., Galan J.E., Askenase P.W., and Flavell R.A. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24 (2006) 317-327
39. Boyden E.D., and Dietrich W.F. Nalp1b controls mouse macrophage susceptibility to anthrax lethal toxin. Nat. Genet. 38 (2006) 240-244
40. Alfano J.R., and Collmer A. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu. Rev. Phytopathol. 42 (2004) 385-414
41. Kang B.C., Yeam I., and Jahn M.M. Genetics of plant virus resistance. Annu. Rev. Phytopathol. 43 (2005) 581-621
42. Armstrong M.R., Whisson S.C., Pritchard L., Bos J.I., Venter E., Avrova A.O., Rehmany A.P., Bohme 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. An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 7766-7771
43. Ellis J., Dodds P., and Pryor T. Structure, function and evolution of plant disease resistance genes. Curr. Opin. Plant Biol. 3 (2000) 278-284
44. Shen Q.H., Zhou F., Bieri S., Haizel T., Shirasu K., and Schulze-Lefert P. Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus. Plant Cell 15 (2003) 732-744
45. Qu S., Liu G., Zhou B., Bellizzi M., Zeng L., Dai L., Han B., and Wang G.L. The broad-spectrum blast resistance gene Pi9 encodes a nucleotide-binding site-leucine-rich repeat protein and is a member of a multigene family in rice. Genetics 172 (2006) 1901-1914
46. Mondragon-Palomino M., Meyers B.C., Michelmore R.W., and Gaut B.S. Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res. 12 (2002) 1305-1315
47. Monosi B., Wisser R.J., Pennill L., and Hulbert S.H. Full-genome analysis of resistance gene homologues in rice. Theor. Appl. Genet. 109 (2004) 1434-1447
48. Takahashi H., Miller J., Nozaki Y., Takeda M., Shah J., Hase S., Ikegami M., Ehara Y., and Dinesh-Kumar S.P. RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant J. 32 (2002) 655-667
49. Dodds P.N., Lawrence G.J., Catanzariti A.M., Ayliffe M.A., and Ellis J.G. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell 16 (2004) 755-768
50. Grube R.C., Radwanski E.R., and Jahn M. Comparative genetics of disease resistance within the solanaceae. Genetics 155 (2000) 873-887
51. Nombela G., Williamson V.M., and Muniz M. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol. Plant Microbe Interact. 16 (2003) 645-649
52. Bisgrove S.R., Simonich M.T., Smith N.M., Sattler A., and Innes R.W. A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes. Plant Cell 6 (1994) 927-933
53. Magalhaes J.G., Philpott D.J., Nahori M.A., Jehanno M., Fritz J., Bourhis L.L., Viala J., Hugot J.P., Giovannini M., Bertin J., Lepoivre M., Mengin-Lecreulx D., Sansonetti P.J., and Girardin S.E. Murine Nod1 but not its human orthologue mediates innate immune detection of tracheal cytotoxin. EMBO Rep. (2005)
54. Jia Y., McAdams S.A., Bryan G.T., Hershey H.P., and Valent B. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19 (2000) 4004-4014
55. Deslandes L., Olivier J., Peeters N., Feng D.X., Khounlotham M., Boucher C., Somssich I., Genin S., and Marco Y. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 8024-8029
56. Dodds P.N., Lawrence G.J., Catanzariti A.M., Teh T., Wang C.I., Ayliffe M.A., Kobe B., and Ellis J.G. Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 8888-8893
57. Mackey D., Holt B.F., Wiig A., and Dangl J.L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108 (2002) 743-754
58. Axtell M.J., and Staskawicz B.J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112 (2003) 369-377
59. Mackey D., Belkhadir Y., Alonso J.M., Ecker J.R., and Dangl J.L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112 (2003) 379-389
60. Belkhadir Y., Nimchuk Z., Hubert D.A., Mackey D., and Dangl J.L. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence Functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16 (2004) 2822-2835
61. Shao F., Golstein C., Ade J., Stoutemyer M., Dixon J.E., and Innes R.W. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301 (2003) 1230-1233
62. Van der Biezen E.A., and Jones J.D. Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23 (1998) 454-456
63. Kim M.G., da Cunha L., McFall A.J., Belkhadir Y., DebRoy S., Dangl J.L., and Mackey D. Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121 (2005) 749-759
64. Gassmann W., Dahlbeck D., Chesnokova O., Minsavage G.V., Jones J.B., and Staskawicz B.J. Molecular evolution of virulence in natural field strains of Xanthomonas campestris pv. Vesicatoria. J. Bacteriol. 182 (2000) 7053-7059
65. Harrison B.D. Virus variation in relation to resistance-breaking in plants. Euphytica 124 (2002) 181-192
66. Chisholm S.T., Dahlbeck D., Krishnamurthy N., Day B., Sjolander K., and Staskawicz B.J. Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 2087-2092
67. Ade J., DeYoung B.J., Golstein C., and Innes R.W. Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease. Proc. Natl. Acad. Sci. U.S.A. 107 (2007) 2531-2536
68. Tanabe T., Chamaillard M., Ogura Y., Zhu L., Qiu S., Masumoto J., Ghosh P., Moran A., Predergast M.M., Tromp G., Williams C.J., Inohara N., and Nunez G. Regulatory regions and critical residues of NOD2 involved in muramyl dipeptide recognition. EMBO J. 23 (2004) 1587-1597
69. Girardin S.E., Jehanno M., Mengin-Lecreulx D., Sansonetti P.J., Alzari P.M., and Philpott D.J. Identification of the critical residues involved in peptidoglycan detection by Nod1. J. Biol. Chem. (2005)
70. Murray P.J. NOD proteins: an intracellular pathogen-recognition system or signal transduction modifiers?. Curr. Opin. Immunol. 17 (2005) 352-358
71. Chisholm S.T., Coaker G., Day B., and Staskawicz B.J. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124 (2006) 803-814
72. Hibino T., Loza-Coll M., Messier C., Majeske A.J., Cohen A.H., Terwilliger D.P., Buckley K.M., Brockton V., Nair S.V., Berney K., Fugmann S.D., Anderson M.K., Pancer Z., Cameron R.A., Smith L.C., and Rast J.P. The immune gene repertoire encoded in the purple sea urchin genome. Dev. Biol. 300 (2006) 349-365
73. Kim H.E., Du F., Fang M., and Wang X. Formation of apoptosome is initiated by cytochrome c-induced dATP hydrolysis and subsequent nucleotide exchange on Apaf-1. Proc. Natl. Acad. Sci. U.S.A. (2005)
74. Poyet J.L., Srinivasula S.M., Tnani M., Razmara M., Fernandes-Alnemri T., and Alnemri E.S. Identification of Ipaf, a human caspase-1-activating protein related to Apaf-1. J. Biol. Chem. 276 (2001) 28309-28313
75. Inohara N., Koseki T., Lin J., del Peso L., Lucas P.C., Chen F.F., Ogura Y., and Nunez G. An induced proximity model for NF-kappa B activation in the Nod1/RICK and RIP signaling pathways. J. Biol. Chem. 275 (2000) 27823-27831
76. Wang Y., Hasegawa M., Imamura R., Kinoshita T., Kondo C., Konaka K., and Suda T. PYNOD, a novel Apaf-1/CED4-like protein is an inhibitor of ASC and caspase-1. Int. Immunol. 16 (2004) 777-786
77. Chu Z.L., Pio F., Xie Z., Welsh K., Krajewska M., Krajewski S., Godzik A., and Reed J.C. A novel enhancer of the Apaf1 apoptosome involved in cytochrome c-dependent caspase activation and apoptosis. J. Biol. Chem. 276 (2001) 9239-9245
78. Yan N., Chai J., Lee E.S., Gu L., Liu Q., He J., Wu J.W., Kokel D., Li H., Hao Q., Xue D., and Shi Y. Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans. Nature 437 (2005) 831-837
79. Sisk T.J., Roys S., and Chang C.H. Self-association of CIITA and its transactivation potential. Mol. Cell. Biol. 21 (2001) 4919-4928
80. Moffett P., Farnham G., Peart J., and Baulcombe D.C. Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J. 21 (2002) 4511-4519
81. Leister R.T., Dahlbeck D., Day B., Li Y., Chesnokova O., and Staskawicz B.J. Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell 17 (2005) 1268-1278
82. Kretsovali A., Spilianakis C., Dimakopoulos A., Makatounakis T., and Papamatheakis J. Self-association of class II transactivator correlates with its intracellular localization and transactivation. J. Biol. Chem. 276 (2001) 32191-32197
83. Chamaillard M., Philpott D., Girardin S.E., Zouali H., Lesage S., Chareyre F., Bui T.H., Giovannini M., Zaehringer U., Penard-Lacronique V., Sansonetti P.J., Hugot J.P., and Thomas G. Gene-environment interaction modulated by allelic heterogeneity in inflammatory diseases. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 3455-3460
84. Dowds T.A., Masumoto J., Zhu L., Inohara N., and Nunez G. Cryopyrin-induced interleukin 1beta secretion in monocytic cells: enhanced activity of disease-associated mutants and requirement for ASC. J. Biol. Chem. 279 (2004) 21924-21928
85. Shirano Y., Kachroo P., Shah J., and Klessig D.F. A gain-of-function mutation in an Arabidopsis Toll interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. Plant Cell 14 (2002) 3149-3162
86. Zhang Y., Goritschnig S., Dong X., and Li X. A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15 (2003) 2636-2646
87. Hwang C.F., Bhakta A.V., Truesdell G.M., Pudlo W.M., and Williamson V.M. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12 (2000) 1319-1329
88. Sun Q., Collins N.C., Ayliffe M., Smith S.M., Drake J., Pryor T., and Hulbert S.H. Recombination between paralogues at the Rp1 rust resistance locus in maize. Genetics 158 (2001) 423-438
89. Inohara N., Koseki T., del Peso L., Hu Y., Yee C., Chen S., Carrio R., Merino J., Liu D., Ni J., and Nunez G. Nod1, an Apaf-1-like activator of caspase-9 and nuclear factor-kappaB. J. Biol. Chem. 274 (1999) 14560-14567
90. Ogura Y., Inohara N., Benito A., Chen F.F., Yamaoka S., and Nunez G. Nod2, a Nod1/Apaf-1 family member that is restricted to monocytes and activates NF-kappaB. J. Biol. Chem. 276 (2001) 4812-4818
91. Zhang Y., Dorey S., Swiderski M., and Jones J.D. Expression of RPS4 in tobacco induces an AvrRps4-independent HR that requires EDS1, SGT1 and HSP90. Plant J. 40 (2004) 213-224
92. Michael Weaver L., Swiderski M.R., Li Y., and Jones J.D. The Arabidopsis thaliana TIR-NB-LRR R-protein, RPP1A; protein localization and constitutive activation of defence by truncated alleles in tobacco and Arabidopsis. Plant J. 47 (2006) 829-840
93. Chamaillard M., Hashimoto M., Horie Y., Masumoto J., Qiu S., Saab L., Ogura Y., Kawasaki A., Fukase K., Kusumoto S., Valvano M.A., Foster S.J., Mak T.W., Nunez G., and Inohara N. An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat. Immunol. 4 (2003) 702-707
94. Peart J.R., Mestre P., Lu R., Malcuit I., and Baulcombe D.C. NRG1, a CC-NB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr. Biol. 15 (2005) 968-973