Plant NB-LRR Immune Receptors: From Recognition to Transcriptional Reprogramming

Cell Host and Microbe

Volumn 3, Issue 3, 2008, Pages 126-135

  Caplan, Jeffrey ^a   Padmanabhan, Meenu ^a   Dinesh Kumar, Savithramma P ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; NUCLEOPORIN; NUCLEOTIDE BINDING DOMAIN AND LEUCINE RICH REPEAT RECEPTOR; PROTEIN MOS3; PROTEIN MOS7; PROTEIN RPM1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR WRKY1; TRANSCRIPTION FACTOR WRKY2; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS; CELLULAR DISTRIBUTION; GENETIC TRANSCRIPTION; HOST RESISTANCE; IMMUNE RESPONSE; MAGNAPORTHE GRISEA; MICROORGANISM DETECTION; MOLECULAR RECOGNITION; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PLANT PATHOGEN INTERACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PSEUDOMONAS SYRINGAE; REVIEW; TOBACCO MOSAIC VIRUS; TRANSCRIPTION INITIATION; XANTHOMONAS CAMPESTRIS;

ANIMALIA;

EID: 40149104095     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2008.02.010     Document Type: Review

References (91)

1. J. Ade B.J. DeYoung C. Golstein R.W. Innes Indirect activation of a plant nucleotide binding site-leucine-rich repeat protein by a bacterial protease Proc. Natl. Acad. Sci. USA 104 2007 2531 2536
2. L. Aravind The BED finger, a novel DNA-binding domain in chromatin-boundary-element-binding proteins and transposases Trends Biochem. Sci. 25 2000 421 423
3. T. Ashfield L.E. Ong K. Nobuta C.M. Schneider R.W. Innes Convergent evolution of disease resistance gene specificity in two flowering plant families Plant Cell 16 2004 309 318
4. F.M. Ausubel Are innate immune signaling pathways in plants and animals conserved? Nat. Immunol. 6 2005 973 979
5. M.J. Axtell B.J. Staskawicz Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4 Cell 112 2003 369 377
6. A. Bauer S. Chauvet O. Huber F. Usseglio U. Rothbacher D. Aragnol R. Kemler J. Pradel Pontin52 and reptin52 function as antagonistic regulators of beta-catenin signalling activity EMBO J. 19 2000 6121 6130
7. M. Beck V. Lucic F. Forster W. Baumeister O. Medalia Snapshots of nuclear pore complexes in action captured by cryo-electron tomography Nature 449 2007 611 615
8. K. Bomblies J. Lempe P. Epple N. Warthmann C. Lanz J.L. Dangl D. Weigel Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants PLoS Biol. 5 2007 e236
9. D.C. Boyes J. Nam J.L. Dangl The Arabidopsis thaliana RPM1 disease reistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response Proc. Natl. Acad. Sci. USA 95 1998 15849 15854
10. M. Brameier A. Krings R.M. MacCallum NucPred–predicting nuclear localization of proteins Bioinformatics 23 2007 1159 1160
11. G.T. Bryan K.S. Wu L. Farrall Y. Jia H.P. Hershey S.A. McAdams K.N. Faulk G.K. Donaldson R. Tarchini B. Valent tA single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta Plant Cell 12 2000 2033 2046
12. T.M. Burch-Smith M. Schiff J.L. Caplan J. Tsao K. Czymmek S.P. Dinesh-Kumar A Novel Role for the TIR Domain in Association with Pathogen-Derived Elicitors PLoS Biol. 5 2007 e68
13. J.L. Caplan P. Mamillapalli T.M. Burch-Smith K. Czymmek S.P. Dinesh-Kumar Chloroplastic Protein NRIP1 Mediates Innate Immune Receptor Recognition of a Viral Effector Cell 132 2008 449 462
14. J.L. Dangl J.D.G. Jones Plant pathogens and integrated defence responses to infection Nature 411 2001 826 833
15. B. Day D. Dahlbeck J. Huang S.T. Chisholm D. Li B.J. Staskawicz Molecular basis for the RIN4 negative regulation of RPS2 disease resistance Plant Cell 17 2005 1292 1305
16. L. Deslandes J. Olivier N. Peeters D.X. Feng M. Khounlotham C. Boucher I. Somssich S. Genin Y. Marco 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 100 2003 8024 8029
17. D. Desveaux A.U. Singer A.J. Wu B.C. McNulty L. Musselwhite Z. Nimchuk J. Sondek J.L. Dangl Type III effector activation via nucleotide binding, phosphorylation, and host target interaction PLoS Pathog. 3 2007 e48
18. B.J. DeYoung R.W. Innes Plant NBS-LRR proteins in pathogen sensing and host defense Nat. Immunol. 7 2006 1243 1249
19. S.P. Dinesh-Kumar W.-H. Tham B. Baker The structure-function analysis of the tobacco mosaic resistance gene Proc. Natl. Acad. Sci. USA 97 2000 14789 14794
20. P.N. Dodds G.J. Lawrence J.G. Ellis 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 13 2001 163 178
21. P.N. Dodds G.J. Lawrence A.M. Catanzariti M.A. Ayliffe J.G. Ellis The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells Plant Cell 16 2004 755 768
22. P.N. Dodds G.J. Lawrence A.M. Catanzariti T. Teh C.I. Wang M.A. Ayliffe B. Kobe J.G. Ellis Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes Proc. Natl. Acad. Sci. USA 103 2006 8888 8893
23. K.A. Dugan M.A. Wood M.D. Cole TIP49, but not TRRAP, modulates c-Myc and E2F1 dependent apoptosis Oncogene 21 2002 5835 5843
24. J.G. Ellis G.J. Lawrence J.E. Luck P.N. Dodds Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity Plant Cell 11 1999 495 506
25. J.G. Ellis P.N. Dodds G.J. Lawrence Flax rust resistance gene specificity is based on direct resistance-avirulence protein interactions Annu. Rev. Phytopathol. 45 2007 289 306
26. O. Emanuelsson H. Nielsen G. von Heijne ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites Protein Sci. 8 1999 978 984
27. J. Enninga D.E. Levy G. Blobel B.M. Fontoura Role of nucleoporin induction in releasing an mRNA nuclear export block Science 295 2002 1523 1525
28. T. Eulgem I.E. Somssich Networks of WRKY transcription factors in defense signaling Curr. Opin. Plant Biol. 10 2007 366 371
29. A. Faigon-Soverna F.G. Harmon L. Storani E. Karayekov R.J. Staneloni W. Gassmann P. Mas J.J. Casal S.A. Kay M.J. Yanovsky A constitutive shade-avoidance mutant implicates TIR-NBS-LRR proteins in Arabidopsis photomorphogenic development Plant Cell 18 2006 2919 2928
30. A.M. Faria A. Levay Y. Wang A.O. Kamphorst M.L. Rosa D.R. Nussenzveig W. Balkan Y.M. Chook D.E. Levy B.M. Fontoura The nucleoporin Nup96 is required for proper expression of interferon-regulated proteins and functions Immunity 24 2006 295 304
31. S.H. Gabriels J.H. Vossen S.K. Ekengren G. van Ooijen A.M. Abd-El-Haliem G.C. van den Berg D.Y. Rainey G.B. Martin F.L. Takken P.J. de Wit M.H. Joosten An NB-LRR protein required for HR signalling mediated by both extra- and intracellular resistance proteins Plant J. 50 2007 14 28
32. S.R. Grant E.J. Fisher J.H. Chang B.M. Mole J.L. Dangl Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria Annu. Rev. Microbiol. 60 2006 425 449
33. K. Gu B. Yang D. Tian L. Wu D. Wang C. Sreekala F. Yang Z. Chu G.L. Wang F.F. White Z. Yin R gene expression induced by a type-III effector triggers disease resistance in rice Nature 435 2005 1122 1125
34. D. Gurlebeck F. Thieme U. Bonas Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant J. Plant Physiol. 163 2006 233 255
35. D.S. Guttman B.A. Vinatzer S.F. Sarkar M.V. Ranall G. Kettler J.T. Greenberg A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae Science 295 2002 1722 1726
36. M.C. Heath Hypersensitive response-related death Plant Mol. Biol. 44 2000 321 334
37. B.F. Holt III D.C. Boyes M. Ellerstrom N. Siefers A. Wiig S. Kauffman M.R. Grant J.L. Dangl An evolutionarily conserved mediator of plant disease resistance gene function is required for normal Arabidopsis development Dev. Cell 2 2002 807 817
38. S. Hubner H.M. Smith W. Hu C.K. Chan H.P. Rihs B.M. Paschal N.V. Raikhel D.A. Jans Plant importin alpha binds nuclear localization sequences with high affinity and can mediate nuclear import independent of importin beta J. Biol. Chem. 274 1999 22610 22617
39. J. Jelenska N. Yao B.A. Vinatzer C.M. Wright J.L. Brodsky J.T. Greenberg A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses Curr. Biol. 17 2007 499 508
40. Y. Jia S.A. McAdams G.T. Bryan H.P. Hershey B. Valent Direct interaction of resistance gene and avirulence gene products confers rice blast resistance EMBO J. 19 2000 4004 4014
41. T.D. Kanneganti M. Lamkanfi G. Nunez Intracellular NOD-like receptors in host defense and disease Immunity 27 2007 549 559
42. T. Kawai S. Akira TLR signaling Cell Death Differ. 13 2006 816 825
43. S. Kay S. Hahn E. Marois G. Hause U. Bonas A bacterial effector acts as a plant transcription factor and induces a cell size regulator Science 318 2007 648 651
44. H.S. Kim D. Desveaux A.U. Singer P. Patel J. Sondek J.L. Dangl The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation Proc. Natl. Acad. Sci. USA 102 2005 6496 6501
45. M.G. Kim L. da Cunha A.J. McFall Y. Belkhadir S. DebRoy J.L. Dangl D. Mackey Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis Cell 121 2005 749 759
46. G.J. Lawrence P. Dodds J.G. Ellis Rust of flax and linseed caused by Melampsora lini Mol. Plant Pathol. 8 2007 349 354
47. K. Lehto M. Tikkanen J.B. Hiriart V. Paakkarinen E.M. Aro Depletion of the photosystem II core complex in mature tobacco leaves infected by the flavum strain of tobacco mosaic virus Mol. Plant Microbe Interact. 16 2003 1135 1144
48. X. Li J.D. Clarke Y. Zhang X. Dong Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance Mol. Plant Microbe Interact. 14 2001 1131 1139
49. J.M. Lorang T.A. Sweat T.J. Wolpert Plant disease susceptibility conferred by a “resistance” gene Proc. Natl. Acad. Sci. USA 104 2007 14861 14866
50. D. Mackey B.F. Holt A. Wiig J.L. Dangl RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis Cell 108 2002 743 754
51. D. Mackey Y. Belkhadir J.M. Alonso J.R. Ecker J.L. Dangl Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance Cell 112 2003 379 389
52. G.B. Martin S.H. Brommonschenkel J. Chunwongse A. Frary M.W. Ganal R. Spivey T. Wu E.D. Earle S.D. Tanksley Map-based cloning of a protein kinase gene conferring disease resistance in tomato Science 262 1993 1432 1436
53. A.J. Maule M. Escaler M.A. Aranda Programmed responses to virus replication in plants Mol. Plant Pathol. 1 2000 9 15
54. F. Meehan H.C. Murphy A New Helminthosporium Blight of Oats Science 104 1946 413 414
55. P. Mestre D.C. Baulcombe Elicitor-mediated oligomerization of the tobacco N disease resistance protein Plant Cell 18 2006 491 501
56. B.C. Meyers M. Morgante R.W. Michelmore TIR-X and TIR-NBS proteins: Two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes Plant J. 32 2002 77 92
57. B.C. Meyers A. Kozik A. Griego H. Kuang R.W. Michelmore Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis Plant Cell 15 2003 809 834
58. B. Monosi R.J. Wisser L. Pennill S.H. Hulbert Full-genome analysis of resistance gene homologues in rice Theor. Appl. Genet. 109 2004 1434 1447
59. T.S. Mucyn A. Clemente V.M. Andriotis A.L. Balmuth G.E. Oldroyd B.J. Staskawicz J.P. Rathjen The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity Plant Cell 18 2006 2792 2806
60. R. Nair B. Rost Mimicking cellular sorting improves prediction of subcellular localization J. Mol. Biol. 348 2005 85 100
61. Z. Nimchuk E. Marois S. Kjemtrup R.T. Leister F. Katagiri J.L. Dangl Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae Cell 101 2000 353 363
62. G. Nissan S. Manulis-Sasson D. Weinthal H. Mor G. Sessa I. Barash The type III effectors HsvG and HsvB of gall-forming Pantoea agglomerans determine host specificity and function as transcriptional activators Mol. Microbiol. 61 2006 1118 1131
63. Y. Noutoshi T. Ito M. Seki H. Nakashita S. Yoshida Y. Marco K. Shirasu K. Shinozaki A single amino acid insertion in the WRKY domain of the Arabidopsis TIR-NBS-LRR-WRKY-type disease resistance protein SLH1 (sensitive to low humidity 1) causes activation of defense responses and hypersensitive cell death Plant J. 43 2005 873 888
64. L.A. O'Neill A.G. Bowie The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling Nat. Rev. Immunol. 7 2007 353 364
65. L.E. Ong R.W. Innes AvrB mutants lose both virulence and avirulence activities on soybean and Arabidopsis Mol. Microbiol. 60 2006 951 962
66. K. Palma Y. Zhang X. Li An importin alpha homolog, MOS6, plays an important role in plant innate immunity Curr. Biol. 15 2005 1129 1135
67. P. Palukaitis M.J. Rossinck R.G. Dietzgen R.I.B. Francki Cucumber Mosaic Virus Adv. Virus Res. 41 1992 281 348
68. S.S. Patel B.J. Belmont J.M. Sante M.F. Rexach Natively unfolded nucleoporins gate protein diffusion across the nuclear pore complex Cell 129 2007 83 96
69. J.R. Peart P. Mestre R. Lu I. Malcuit D.C. Baulcombe 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
70. P. Romer S. Hahn T. Jordan T. Strauss U. Bonas T. Lahaye Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene Science 318 2007 645 648
71. A. Rose I. Meier A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim Proc. Natl. Acad. Sci. USA 98 2001 15377 15382
72. M.A. Sacco S. Mansoor P. Moffett A RanGAP protein physically interacts with the NB-LRR protein Rx, and is required for Rx-mediated viral resistance Plant J. 52 2007 82 93
73. S. Schmidt M. Lombardi D.M. Gardiner M. Ayliffe P.A. Anderson The M flax rust resistance pre-mRNA is alternatively spliced and contains a complex upstream untranslated region Theor. Appl. Genet. 115 2007 373 382
74. F. Shao C. Golstein J. Ade M. Stoutemyer J.E. Dixon R.W. Innes Cleavage of Arabidopsis PBS1 by a bacterial type III effector Science 301 2003 1230 1233
75. Q.H. Shen Y. Saijo S. Mauch C. Biskup S. Bieri B. Keller H. Seki B. Ulker I.E. Somssich P. Schulze-Lefert Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses Science 315 2007 1098 1103
76. Y. Shirano P. Kachroo J. Shah D.F. Klessig 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
77. E. Sinapidou K. Williams L. Nott S. Bahkt M. Tor I. Crute P. Bittner-Eddy J. Beynon Two TIR:NB:LRR genes are required to specify resistance to Peronospora parasitica isolate Cala2 in Arabidopsis Plant J. 38 2004 898 909
78. D. Takemoto D.A. Jones Membrane release and destabilization of Arabidopsis RIN4 following cleavage by Pseudomonas syringae AvrRpt2 Mol. Plant Microbe Interact. 18 2005 1258 1268
79. W.I. Tameling D.C. Baulcombe Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X Plant Cell 19 2007 1682 1694
80. W.I. Tameling S.D. Elzinga P.S. Darmin J.H. Vossen F.L. Takken M.A. Haring B.J. Cornelissen The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity Plant Cell 14 2002 2929 2939
81. W.I. Tameling J.H. Vossen M. Albrecht T. Lengauer J.A. Berden M.A. Haring B.J. Cornelissen F.L. Takken Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation Plant Physiol. 140 2006 1233 1245
82. H. Ueda Y. Yamaguchi H. Sano Direct Interaction between the Tobacco Mosaic Virus Helicase Domain and the ATP-bound Resistance Protein, N Factor during the Hypersensitive Response in Tobacco Plants Plant Mol. Biol. 61 2006 31 45
83. G. Van den Ackerveken E. Marois U. Bonas Recognition of the bacterial avirulence protein AvrBs3 occurs inside the host plant cell Cell 87 1996 1307 1316
84. E.A. Van der Biezen J.D. Jones Plant disease-resistance proteins and the gene-for-gene concept Trends Biochem. Sci. 23 1998 454 456
85. C.I. Wang G. Guncar J.K. Forwood T. Teh A.M. Catanzariti G.J. Lawrence F.E. Loughlin J.P. Mackay H.J. Schirra P.A. Anderson Crystal structures of flax rust avirulence proteins AvrL567-A and -D reveal details of the structural basis for flax disease resistance specificity Plant Cell 19 2007 2898 2912
86. R.F. Warren P.M. Merritt E. Holub R.W. Innes Identification of three putative signal transduction genes involved in R gene-specified disease resistance in Arabidopsis Genetics 152 1999 401 412
87. M. Wiermer K. Palma Y. Zhang X. Li Should i stay or should i go? Nucleocytoplasmic trafficking in plant innate immunity Cell. Microbiol. 9 2007 1880 1890
88. L. Wirthmueller Y. Zhang J.D. Jones J.E. Parker Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense Curr. Biol. 17 2007 2023 2029
89. M.A. Wood S.B. McMahon M.D. Cole An ATPase/helicase complex is an essential cofactor for oncogenic transformation by c-Myc Mol. Cell 5 2000 321 330
90. W. Xing Y. Zou Q. Liu J. Liu X. Luo Q. Huang S. Chen L. Zhu R. Bi Q. Hao The structural basis for activation of plant immunity by bacterial effector protein AvrPto Nature 449 2007 243 247
91. X.C. Zhang W. Gassmann RPS4-mediated disease resistance requires the combined presence of RPS4 transcripts with full-length and truncated open reading frames Plant Cell 15 2003 2333 2342