Plant NBS-LRR proteins: Adaptable guards

Genome Biology

Volumn 7, Issue 4, 2006, Pages

  McHale, Leah ^a   Tan, Xiaoping ^a   Koehl, Patrice ^a   Michelmore, Richard W ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; ARABIDOPSIS PROTEIN; COAT PROTEIN; DECORIN; DOUBLE STRANDED RNA; HEAT SHOCK PROTEIN 90; INTERLEUKIN 1 RECEPTOR; NUCLEOTIDE BINDING SITE LEUCINE RICH REPEAT PROTEIN; PLANT RNA; REGULATOR PROTEIN; SIGNAL TRANSDUCTION ADENOSINE TRIPHOSPHATASE WITH NUMEROUS DOMAINS; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; LEUCINE; VEGETABLE PROTEIN;

ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CLADISTICS; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DISEASE RESISTANCE; GENE CLUSTER; GENE CONVERSION; GENE DELETION; GENE INSERTION; GENE MUTATION; GENETIC ORGANIZATION; GENETIC RECOMBINATION; GENETIC VARIABILITY; MACROMOLECULE; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; OLIGOMERIZATION; PLANT PATHOGEN INTERACTION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS; SEQUENCE DATABASE; SIGNAL TRANSDUCTION; AMINO ACID SEQUENCE; CHEMISTRY; GENETICS; GENOME; INNATE IMMUNITY; MOLECULAR GENETICS; PHYSIOLOGY; PLANT DISEASE; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; EVOLUTION, MOLECULAR; GENOME, PLANT; IMMUNITY, NATURAL; LEUCINE; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT PROTEINS; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID;

EID: 33745040554     PISSN: 1474760X     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2006-7-4-212     Document Type: Review

References (96)

1. Jones DA, Jones JDG: The role of leucine-rich repeat proteins in plant defenses. Adv Bot Res 1997, 24:90-167.
2. Ellis J, Dodds P, Pryor T: Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 2000 3:278-284.
3. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW: Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 2003, 15:809-834.
4. Belkhadir Y, Subramaniam R, Dangl JL: Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr Opin Plant Biol 2004, 7:391-399.
5. Jones DA, Takemoto D: Plant innate immunity - direct and indirect recognition of general and specific pathogen-associated molecules. Curr Opin Immunol 2004, 16:48-62.
6. Inohara N, Chamaillard M, McDonald C, Nunez, G: NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu Rev Biochem 2005, 74:355-383.
7. Ausubel FM: Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 2005, 6:973-979.
8. Ting JP, Davis BK: CATERPILLER: a novel gene family important in immunity, cell death, and diseases. Annu Rev Immunol 2005, 23:387-414.
9. Functional and Comparative Genomics of Disease Resistance Gene Homologs [http://niblrrs.ucdavis.edu]
10. Monosi B, Wisser RJ, Pennill L, Hulbert SH: Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 2004, 109:1434-1447.
11. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D: Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 2004, 271:402-415.
12. Akita M, Valkonen JP: A novel gene family in moss (Physcomitrella patens) shows sequence homology and a phylogenetic relationship with the TIR-NBS class of plant disease resistance genes. J Mol Evol 2002, 55:595-605.
13. Cannon SB, Zhu H, Baumgarten AM, Spangler R, May G, Cook DR, Young ND: Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. J Mol Evol 2002, 54:548-562.
14. Plocik A, Layden J, Kesseli R: Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory. Mol Phylogenet Evol 2004, 31:153-163.
15. Yaish MW, Saenz de Miera LE, Perez de la Vega M: Isolation of a family of resistance gene analogue sequences of the nucleotide binding site (NBS) type from Lens species. Genome 2004, 47:650-659.
16. Richly E, Kurth J, Leister D: Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 2002, 19:76-84.
17. Leister D: Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends Genet 2004, 20:116-122.
18. Chin DB, Arroyo-Garcia R, Ochoa OE, Kesseli RV, Lavelle DO, Michelmore RW: Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics 2001, 157:831-849.
19. Kuang H, Woo SS, Meyers BC, Nevo E, Michelmore RW: Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 2004, 16:2870-2894.
20. Baumgarten A, Cannon S, Spangler R, May G: Genome-level evolution of resistance genes in Arabidopsis thaliana. Genetics 2003, 165:309-319.
21. Mondragon-Palomino M, Gaut BS: Gene conversion and the evolution of three leucine-rich repeat gene families in Arabidopsis thaliana. Mol Biol Evol 2005, 22:2444-2456.
22. Michelmore RW, Meyers BC: Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 1998, 8:1113-1130.
23. Mondragon-Palomino M, Meyers BC, Michelmore RW, Gaut BS: Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana. Genome Res 2002, 12:1305-1315.
24. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND: Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 1999, 20:317-332.
25. Pan Q, Wendel J, Fluhr R: Divergent evolution of plant NBSLRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 2000, 50:203-213.
26. Bai J, Pennill LA, Ning J, Lee SW, Ramalingam J, Webb CA, Zhao B, Sun Q, Nelson JC, Leach JE, Hulbert SH: Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 2002, 12:1871-1884.
27. Meyers BC, Morgante M, Michelmore RW: TIR-X and TIR-NBS proteins: two new families related to disease resistance TIRNBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 2002, 32:77-92.
28. Luck JE, Lawrence GJ, Dodds PN, Shepherd KW, Ellis JG: Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell 2000, 12:1367-1377.
29. Leipe DD, Koonin EV, 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 2004, 343:1-28.
30. Albrecht M, Takken FL: Update on the domain architectures of NLRs and R proteins. Biochem Biophys Res Commun 2006, 339:459-462.
31. Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL, Haring MA, Cornelissen BJ: The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 2002, 14:2929-2939.
32. Mestre P, Baulcombe DC: Elicitor-mediated oligomerization of the tobacco N disease resistance protein. Plant Cell 2006, 18:491-501.
33. Riedl SJ, Li W, Chao Y, Schwarzenbacher R, Shi Y: Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature 2005, 434:926-933.
34. Enkhbayar, P, Kamiya, M, Osaki, M, Matsumoto, T, Matsumisha, M: Structural principles of Leucine Rich Repeat proteins. Proteins 2003, 54: 393-403.
35. Scott PG, McEwan PA, Dodd CM, Bergmann PM, Bishop PN, Bella J: Crystal structure of the dimeric protein core of decorin, the archetypal small leucine rich repeat proteoglycan. Proc Natl Acad Sci USA 2004, 101:15633-15638.
36. Bell JK, Mullen GE, Leifer CA, Mazzoni A, Davies DR, Segal DM: Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol 2003, 24:528-533.
37. Choe J, Kelker MS, Wilson IA: Crystal structure of human toll-like receptor 3 (TLR3) ectodomain. Science 2005, 309:581-585.
38. Kim JI, Lee CJ, Jin MS, Lee CH, Paik SG, Lee H, Lee JO: Crystal structure of CD14 and its implications for lipopolysaccharide signaling. J Biol Chem 2005, 280:11347-11351.
39. Wulff BB, Thomas CM, Smoker M, Grant M, Jones JD: Domain swapping and gene shuffling identify sequences required for induction of an Avr-dependent hypersensitive response by the tomato Cf-4 and Cf-9 proteins. Plant Cell 2001, 13:255-272.
40. Dodds PN, Lawrence GJ, Ellis JG: Six amino acid changes confined to the leucine-rich repeat beta-strand/beta-turn motif determine the difference between the P and P2 rust resistance specificities in flax. Plant Cell 2001, 13:163-178.
41. Ellis JG, Lawrence GJ, Luck JE, Dodds PN: Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 1999, 11:495-506.
42. Hwang CF, Williamson VM: Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. Plant J 2003, 34:585-593.
43. Moffett P, Farnham G, Peart J, Baulcombe DC: Interaction between domains of a plant NBS-LRR protein in disease resistance-related cell death. EMBO J 2002, 21:4511-4519.
44. Warren RF, Henk A, Mowery P, Holub E, Innes RW: A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes. Plant Cell 1998, 10:1439-1452.
45. Bendahmane A, Farnham G, Moffett P, Baulcombe DC: Constitutive gain-of-function mutants in a nucleotide binding site-leucine rich repeat protein encoded at the Rx locus of potato. Plant J 2002, 32:195-204.
46. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y: Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci USA 2002, 99:2404-2409.
47. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B: Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 2000, 19:4004-4014.
48. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich I, Genin S, 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 USA 2003, 100:8024-8029.
49. Van der Biezen EA, Jones, JD: Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 1998, 23:454-456.
50. Dangl JL, Jones JD: Plant pathogens and integrated defense responses to infection. Nature 2001, 411:826-833.
51. Mackey D, Holt BF 3rd, Wiig A, Dangl, JL: RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 2002, 108:743-754.
52. Axtell MJ, Chisholm ST, Dahlbeck D, Staskawicz BJ: Genetic and molecular evidence that the Pseudomonas syringae type III effector protein AvrRpt2 is a cysteine protease. Mol Microbiol 2003, 49:1537-1546.
53. Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL: The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Natl Acad Sci USA 2005, 102:6496-6501.
54. Axtell MJ, Staskawicz BJ: Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 2003, 112:369-377.
55. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL: Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 2003, 112:379-389.
56. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW: Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 2003, 301:1230-1233.
57. Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, Mulder L, Jones JD: A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science 2002, 296:744-747.
58. Rooney HC, Van't Klooster JW, van der Hoorn RA, Joosten MH, Jones JD, de Wit PJ: Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 2005, 308:1783-1786.
59. Shirasu K, Schulze-Lefert P: Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci 2003, 8:252-258.
60. Xu Y, Tao X, Shen B, Horng T, Medzhitov R, Manley JL, Tong L: Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 2000, 408:111-115.
61. Inohara N, Nunez G: NODs: intracellular proteins involved in inflammation and apoptosis. Nat Rev Immunol 2003, 5:371-382.
62. Hu X, Yagi Y, Tanji T, Zhou S, Ip YT: Multimerization and interaction of Toll and Spatzle in Drosophila. Proc Natl Acad Sci USA 2004, 101:9369-9374.
63. Sun H, Towb P, Chiem DN, Foster BA, Wasserman SA: Regulated assembly of the Toll signaling complex drives Drosophila dorsoventral patterning. EMBO J 2004, 23:100-110.
64. McGettrick AF, O'Neill LA: The expanding family of MyD88-like adaptors in Toll-like receptor signal transduction. Mol Immunol 2004, 41:577-582.
65. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JD: The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense response and bacterial pathogenesis. Plant Physiol 2004, 135:1113-1128.
66. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T: Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 2004, 428:764-767.
67. Iwami KI, Matsuguchi T, Masuda A, Kikuchi T, Musikacharoen T, Yoshikai Y: Cutting edge: naturally occurring soluble form of mouse Toll-like receptor 4 inhibits lipopolysaccharide signaling. J Immunol 2000, 165:6682-6686.
68. Jordan T, Schornack S, Lahaye T: Alternative splicing of transcripts encoding Toll-like plant resistance proteins - what's the functional relevance to innate immunity? Trends Plant Sci 2002, 7:392-398.
69. Ayliffe MA, Frost DV, Finnegan EJ, Lawrence GJ, Anderson PA, Ellis JG: Analysis of alternative transcripts of the flax L6 rust resistance gene. Plant J 1999, 17:287-292.
70. Parker JE, Coleman MJ, Szabo V, Frost LN, Schmidt R, van der Biezen EA, Moores T, Dean C, Daniels MJ, Jones JD: The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. Plant Cell 1997, 9:879-894.
71. Marathe R, Anandalakshmi R, Liu Y, Dinesh-Kumar SP: The tobacco mosaic virus resistance gene, N. Mol Plant Pathol 2002, 3:167-172.
72. Vidal S, Cabrera H, Andersson RA, Fredriksson A, Valkonen JP: Potato gene Y-1 is an N gene homolog that confers cell death upon infection with potato virus Y. Mol Plant Microbe Interact 2002, 15:717-727.
73. Zhang XC, Gassmann W: RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames. Plant Cell 2003, 15:2333-2342.
74. Borhan MH, Holub EB, Beynon JL, Rozwadowski K, Rimmer SR: The Arabidopsis TIR-NB-LRR gene RAC1 confers resistance to Albugo candida (white rust) and is dependent on EDS1 but not PAD4. Mol Plant Microbe Interact 2004, 17:711-719.
75. Schornack S, Ballvora A, Gurlebeck D, Peart J, Baulcombe D, Ganal M, Baker B, Bonas U, Lahaye T: The tomato resistance protein Bs4 is a predicted non-nuclear TIR-NB-LRR protein that mediates defense responses to severely truncated derivatives of AvrBs4 and overexpressed AvrBs3. Plant J 2004, 37:46-60.
76. Ferrier-Cana E, Macadre C, Sevignac M, David P, Langin T, Geffroy V: Distinct post-transcriptional modifications result into seven alternative transcripts of the CC-NBS-LRR gene JA1tr of Phaseolus vulgaris. Theor Appl Genet 2005, 110:895-905.
77. Hubert DA, Tornero P, Belkhadir Y, Krishna P, Takahashi A, Shirasu K, Dangl JL: Cytosolic HSP90 associates with and modulates the Arabidopsis RPM1 disease resistance protein. EMBO J 2003, 22:5679-5689.
78. Lu R, Malcuit T, Moffett P, Ruiz MT, Peart J, Wu AJ, Rathjen JP, Bendahmane A, Day L, Baulcombe DC: High throughput virus-induced gene silencing implicates heat shock protein 90 in plant disease resistance. EMBO J 2003, 22:5690-5699.
79. Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP: Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J Biol Chem 2004, 279:2101-2108.
80. Van der Hoorn RAL, Jones JDG: The plant proteolytic machinery and its role in defence. Curr Opin Plant Biol 2004, 7:400-407.
81. Liu Y, Schiff M, Serino G, Deng XW, Dinesh-Kumar SP: Role of SCF ubiquitin-ligase and the COP9 signalosome in the N gene-mediated resistance response to tobacco mosaic virus. Plant Cell 2002, 14:1483-1496.
82. Boyes DC, Nam J, Dangl JL: The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc Natl Acad Sci USA 1998, 95:15849-15854.
83. Kawasaki T, Nam J, Boyes DC, Holt BF, Hubert DA, Wiig A, Dangl JL: A duplicated pair of Arabidopsis RING-finger E3 ligase contribute to the RPM1- and RPS2-mediated hypersensitive response. Plant J 44:258-270.
84. Hammond-Kosack KE, Parker JE: Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding. Curr Opin Biotechnol 2003, 14:177-193.
85. Nimchuk Z, Eulgem T, Holt BF 3rd, Dangl JL: Recognition and response in the plant immune system. Annu Rev Genet 2003, 37:579-609.
86. Pedley KF, Martin GB: Role of mitogen-activated protein kinases in plant immunity. Curr Opin Plant Biol 2005, 8:541-547.
87. Glazebrook J: Genes controlling expression of defense responses in Arabidopsis-2001 status. Curr Opin Plant Biol 2001, 4:301-308.
88. Kunkel BN, Brooks DM: Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 2002, 5:325-331.
89. Delledonne M, Polverari A, Murgia I: The functions of nitric oxide-mediated signaling and changes in gene expression during the hypersensitive response. Antioxid Redox Signal 2003, 5:33-41.
90. De Vos M, Van Oosten VR, Van Poecke RM, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Metraux JP, Van Loon LC, Dicke M, Pieterse CM: Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 2005, 18:923-937.
91. Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C: The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 2005, 140:249-62.
92. Peart JR, Mestre P, Lu R, Malcuit I, Baulcombe DC: NRG1, a CCNB-LRR protein, together with N, a TIR-NB-LRR protein, mediates resistance against tobacco mosaic virus. Curr Biol 2005, 15:968-973.
93. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ: Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc Natl Acad Sci USA 1999, 96:14153-14158.
94. Phyre: Protein Homology/analogY Recognition Engine [http://www.sbg.bio.ic.ac.uk/~phyre]
95. Koehl, P, Delarue, M: A self-consistent mean field approach to simultaneous gap closure and side-chain positioning in homology modeling. Nat Struct Biol 1995, 2:163-170.
96. PyMOL [http://pymol.sourceforge.net]