Recent advances in plant NLR structure, function, localization, and signaling

Frontiers in Immunology

Volumn 4, Issue , 2013, Pages

  Qi, Dong ^a   Innes, Roger W ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Disease resistance; Hypersensitive response; Leucine rich repeats; Pathogen effectors; Plant innate immunity; pseudomonas syringae

Indexed keywords

INTERLEUKIN RECEPTOR; NUCLEOTIDE BINDING DOMAIN LEUCINE RICH REPEAT PROTEIN; NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ALLERGIC REACTION; AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; CELL COMPARTMENTALIZATION; CELL DEATH; CELL MIGRATION; CRYSTAL STRUCTURE; DISEASE RESISTANCE; DNA TRANSCRIPTION; GENE ACTIVATION; GENE MUTATION; INNATE IMMUNITY; MOLECULAR INTERACTION; NONHUMAN; OLIGOMERIZATION; PLANT DEFENSE; PLANT IMMUNITY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PSEUDOMONAS SYRINGAE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION;

EID: 84987779504     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00348     Document Type: Article

References (97)

1. JacobF,VernaldiS,MaekawaT. Evolution and conservation of plant NLR functions. Front Immunol (2013) 4:297. doi:10.3389/fimmu. 2013.00297
2. Jones JD, Dangl JL. The plant immune system. Nature (2006) 444:323-9. doi:10.1038/nature05286
3. van der Biezen EA, Jones JD. The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol (1998) 8:R226-7. doi:10.1016/ S0960-9822(98)70145-9
4. Inohara N, Chamaillard M, Mcdonald C, Nunez G. NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu Rev Biochem (2005) 74:355-83. doi:10.1146/annurev. biochem.74.082803.133347
5. Danot O, Marquenet E, Vidal-Ingigliardi D, Richet E. Wheel of life, wheel of death: a mechanistic insight into signaling by STAND proteins. Structure (2009) 17:172-82. doi:10.1016/j.str.2009. 01.001
6. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. Genome-wide analysis of NBSLRR-encoding genes in Arabidopsis. Plant Cell (2003) 15:809-34. doi:10. 1105/tpc.009308
7. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, et al. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science (1994) 265:1856-60. doi:10. 1126/science.8091210
8. Mindrinos M, Katagiri F, Yu GL, Ausubel FM. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell (1994) 78: 1089-99. doi:10.1016/0092-8674(94)90282-8
9. WhithamS,Dinesh-Kumar SP,Choi D, Hehl R, Corr C, Baker B. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell (1994) 78:1101-15. doi:10. 1016/0092-8674(94)90283-6
10. Shen QH, Saijo Y, Mauch S, Biskup C, Bieri S, Keller B, et al. Nuclear activity of MLA immune receptors links isolate-specific and basal disease-resistance responses.Science (2007) 315:1098-103. doi:10.1126/ science.1136372
11. Wirthmueller L, Zhang Y, Jones JD, Parker JE. Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr Biol (2007) 17:2023-9. doi:10.1016/ j.cub.2007.10.042
12. Caplan JL, Mamillapalli P, Burch-Smith TM, Czymmek K, Dinesh-Kumar SP. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector. Cell (2008) 132: 449-62. doi:10.1016/j.cell.2007.12. 031
13. Cheng YT, Germain H, Wiermer M, Bi D, Xu F, Garcia AV, et al. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell (2009) 21:2503-16. doi:10.1105/ tpc.108.064519
14. Chang C, Yu D, Jiao J, Jing S, Schulze-Lefert P, Shen QH. Barley MLA immune receptors directly interfere with antagonistically acting transcription factors to initiate disease resistance signaling. Plant Cell (2013) 25:1158-73. doi: 10.1105/tpc.113.109942
15. Garcia AV, Blanvillain-Baufume S, Huibers RP, Wiermer M, Li G, Gobbato E, et al. Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog (2010) 6:e1000970. doi:10. 1371/journal.ppat.1000970
16. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE. Arabidopsis EDS1 connects pathogen effector recognition to cell compartmentspecific immune responses. Science (2011) 334:1401-4. doi:10.1126/science.1211641
17. Sacco MA, Mansoor S, Moffett P. A RanGAP protein physically interacts with the NB-LRR protein Rx, and is required for Rx-mediated viral resistance. Plant J (2007) 52:82-93. doi:10.1111/j.1365-313X. 2007.03213.x
18. Tameling WI, Baulcombe DC. Physical association of the NBLRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell (2007) 19:1682-94. doi:10.1105/ tpc.107.050880
19. Slootweg E, Roosien J, Spiridon LN, Petrescu AJ, Tameling W, Joosten M, et al. Nucleocytoplasmic distribution is required for activation of resistance by the potato NB-LRR receptor Rx1 and is balanced by its functional domains. Plant Cell (2010) 22:4195-215. doi:10.1105/ tpc.110.077537
20. Tameling WI, Nooijen C, Ludwig N, Boter M, Slootweg E, GoverseA,et al. RanGAP2 mediates nucleocytoplasmic partitioning of the NB-LRR immune receptor Rx in the Solanaceae, thereby dictating Rx function. Plant Cell (2010) 22:4176-94. doi:10.1105/ tpc.110.077461
21. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW. Cleavage of Arabidopsis PBS1 by a bacterial type I I I effector. Science (2003) 301:1230-3. doi:10. 1126/science.1085671
22. Dowen RH, Engel JL, Shao F, Ecker JR, Dixon JE. A family of bacterial cysteine protease type I I I effectors utilizes acylation-dependent and -independent strategies to localize to plasma membranes. J Biol Chem (2009) 284:15867-79. doi:10.1074/ jbc.M900519200
23. Qi D, Deyoung BJ, Innes RW. Structure-function analysis of the coiled-coil and leucine-rich repeat domains of the RPS5 disease resistance protein. Plant Physiol (2012) 158:1819-32. doi:10.1104/pp.112. 194035
24. Chung EH, Da Cunha L, Wu AJ, Gao Z, Cherkis K, Afzal AJ, et al. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe (2011) 9:125-36. doi:10.1016/j.chom.2011.01.009
25. Gao Z, Chung EH, Eitas TK, Dangl JL. Plant intracellular innate immune receptor Resistance to Pseudomonas syringae pv. maculicola 1 (RPM1) is activated at, and functions on, the plasma membrane. Proc Natl Acad Sci U S A (2011) 108:7619-24. doi:10.1073/ pnas.1104410108
26. Liu J, Elmore JM, Lin ZJ, Coaker G. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe (2011) 9:137-46. doi:10.1016/j.chom.2011.01.010
27. Takemoto D, Rafiqi M, Hurley U, Lawrence GJ, Bernoux M, Hardham AR, et al. N-terminal motifs in some plant disease resistance proteins function in membrane attachment and contribute to disease resistance. Mol Plant Microbe Interact (2012) 25:379-92. doi:10.1094/ MPMI-11-10-0272
28. Engelhardt S, Boevink PC, Armstrong MR, Ramos MB, Hein I, Birch PR. Relocalization of late blight resistance protein R3a to endosomal compartments is associated with effector recognition and required for the immune response. Plant Cell (2012) 24:5142-58. doi: 10.1105/tpc.112.104992
29. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, et al. 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 (2006) 103:8888-93. doi:10.1073/ pnas.0602577103
30. Ravensdale M, Bernoux M, Ve T, Kobe B, Thrall PH, Ellis JG, et al. Intramolecular interaction influences binding of the Flax L5 and L6 resistance proteins to their AvrL567 ligands. PLoS Pathog (2012) 8:e1003004. doi:10.1371/ journal.ppat.1003004
31. Krasileva KV, Dahlbeck D, Staskawicz BJ. Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell (2010) 22:2444-58. doi:10. 1105/tpc.110.075358
32. Kanzaki H, Yoshida K, Saitoh H, Fujisaki K, Hirabuchi A, Alaux L, et al. Arms race co-evolution of Magnaporthe oryzae AVR-Pik and rice Pik genes driven by their physical interactions. Plant J (2012) 72:894-907. doi:10.1111/j.1365-313X.2012. 05110.x
33. 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) 21:4511-9. doi:10.1093/emboj/cdf453
34. Leister RT, Dahlbeck D, Day B, Li Y, Chesnokova O, Staskawicz BJ. Molecular genetic evidence for the role of SGT1 in the intramolecular complementation of Bs2 protein activity in Nicotiana benthamiana. Plant Cell (2005) 17:1268-78. doi:10.1105/tpc.104.029637
35. Ade J, Deyoung BJ, Golstein C, Innes RW. Indirect activation of a plant nucleotide binding siteleucine-rich repeat protein by a bacterial protease. Proc Natl Acad Sci U SA(2007) 104:2531-6.doi:10.1073/ pnas.0608779104
36. Rairdan GJ, Moffett P. Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell (2006) 18:2082-93. doi:10.1105/ tpc.106.042747
37. Slootweg EJ, Spiridon LN, Roosien J, Butterbach P, Pomp R, Westerhof L, et al. Structural determinants at the interface of the ARC2 and LRR domains control the activation of the NB-LRR plant immune receptors Rx1 and Gpa2. Plant Physiol (2013) 162:1510-28. doi:10.1104/ pp.113.218842
38. Hu Z, Yan C, Liu P, Huang Z, Ma R, Zhang C, et al. Crystal structure of NLRC4 reveals its autoinhibition mechanism. Science (2013) 341:172-5. doi:10.1126/ science.1236381
39. Takken FL, Albrecht M, Tameling WI. Resistance proteins: molecular switches of plant defence. Curr Opin Plant Biol (2006) 9:383-90. doi:10. 1016/j.pbi.2006.05.009
40. Miao EA, Mao DP, Yudkovsky N, Bonneau R, Lorang CG, Warren SE, et al. Innate immune detection of the type I I I secretion apparatus through the NLRC4 inflammasome. Proc Natl Acad Sci USA (2010) 107:3076-80. doi:10.1073/ pnas.0913087107
41. Bernoux M, Ve T, Williams S, Warren C, Hatters D, Valkov E, et al. Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for selfassociation, signaling, and autoregulation. Cell Host Microbe (2011) 9:200-11. doi:10.1016/j.chom.2011. 02.009
42. Maekawa T, Cheng W, Spiridon LN, Toller A, Lukasik E, Saijo Y, et al. Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe (2011) 9:187-99. doi:10. 1016/j.chom.2011.02.008
43. Rairdan GJ, Collier SM, Sacco MA, Baldwin TT, Boettrich T, Moffett P. The coiled-coil and nucleotide binding domains of the Potato Rx disease resistance protein function in pathogen recognition and signaling. Plant Cell (2008) 20:739-51. doi:10.1105/tpc.107.056036
44. Lukasik E, Takken FL. Standing strong, resistance proteins instigators of plant defence. Curr Opin Plant Biol (2009) 12:427-36. doi:10. 1016/j.pbi.2009.03.001
45. 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. doi: 10.2307/3870876
46. Dangl JL, Jones JD. Plant pathogens and integrated defence responses to infection. Nature (2001) 411:826-33. doi:10.1038/35081161
47. van der HoornRA,KamounS.From Guard to Decoy: a new model for perception of plant pathogen effectors. Plant Cell (2008) 20:2009-17. doi:10.1105/tpc.108.060194
48. DeYoung BJ, Qi D, Kim SH, Burke TP, Innes RW. Activation of a plant nucleotide binding-leucine rich repeat disease resistance protein by a modified self protein. Cell Microbiol (2012) 14:1071-84. doi: 10.1111/j.1462-5822.2012.01779.x
49. Axtell MJ, Staskawicz BJ. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell (2003) 112: 369-77. doi:10.1016/S0092-8674(03)00036-9
50. Riedl SJ, Li W, Chao Y, Schwarzenbacher R, Shi Y. Structure of the apoptotic protease-activating factor 1 bound to ADP. Nature (2005) 434:926-33. doi:10.1038/ nature03465
51. Yan N, Chai JJ, Lee ES, Gu LC, Liu Q, He JQ, et al. Structure of the CED-4-CED-9 complex provides insights into programmed cell death in Caenorhabditis elegans. Nature (2005) 437:831-7. doi:10. 1038/nature04002
52. Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL, Haring MA, et al. The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell (2002) 14:2929-39. doi:10.1105/ tpc.005793
53. Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha-and betasubunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J (1982) 1:945-51.
54. Tameling WIL, Vossen JH, Albrecht M, Lengauer T, Berden JA, Haring MA, et al. Mutations in the NBARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol (2006) 140:1233-45. doi:10.1104/pp.105.073510
55. Williams SJ, Sornaraj P, Decourcy-Ireland E, Menz RI, Kobe B, Ellis JG, et al. An autoactive mutant of the M flax rust resistance protein has a preference for binding ATP, whereas wild-type M protein binds ADP. Mol Plant Microbe Interact (2011)24:897-906. doi:10.1094/ MPMI-03-11-0052
56. Shiozaki EN, Chai JJ, Shi Y. Oligomerization and activation of caspase-9, induced by Apaf-1 CARD. Proc Natl Acad Sci USA (2002) 99:4197-202. doi:10.1073/pnas.072544399
57. Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE, Staskawicz BJ, et al. The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. Plant Cell (2006) 18:2792-806. doi:10.1105/ tpc.106.044016
58. Gutierrez JR, Balmuth AL, Ntoukakis V, Mucyn TS, Gimenez-Ibanez S, Jones AM, et al. Prf immune complexes of tomato are oligomeric and contain multiple Pto-like kinases that diversify effector recognition. Plant J (2010) 61:507-18. doi:10.1111/j.1365-313X.2009.04078.x
59. Mestre P, Baulcombe DC. Elicitormediated oligomerization of the tobacco N disease resistance protein. Plant Cell (2006) 18:491-501. doi:10.1105/tpc.105.037234
60. Kofoed EM, Vance RE. Innate immune recognition of bacterial ligands by NAIPs determines inflammasome specificity. Nature (2011) 477:592-5. doi:10.1038/nature10394
61. Zhao Y, Yang J, Shi J, Gong YN, Lu Q, Xu H, et al. The NLRC4 inflammasome receptors for bacterial flagellin and type I I I secretion apparatus. Nature (2011) 477:596-600. doi:10.1038/nature10510
62. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI, et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol (2006) 7:569-75. doi: 10.1038/ni1344
63. Birker D, Heidrich K, Takahara H, Narusaka M,Deslandes L,Narusaka Y, et al. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J (2009) 60:602-13. doi:10.1111/j. 1365-313X.2009.03984.x
64. Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, et al. RRS1 and RPS4 provide a dual resistance-gene system against fungal and bacterial pathogens. Plant J (2009) 60:218-26. doi:10.1111/j. 1365-313X.2009.03949.x
65. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, et al. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type I I I effector targeted to the plant nucleus. Proc Natl Acad Sci U S A (2003) 100:8024-9. doi:10.1073/ pnas.1230660100
66. Bonardi V, Tang S, Stallmann A, Roberts M, Cherkis K, Dangl JL. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci U S A (2011) 108:16463-8. doi: 10.1073/pnas.1113726108
67. Roberts M, Tang S, Stallmann A, Dangl JL, Bonardi V. Genetic requirements for signaling from an autoactive plant NB-LRR intracellular innate immune receptor. PLoS Genet (2013) 9:e1003465. doi:10. 1371/journal.pgen.1003465
68. 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) 15:968-73. doi:10.1016/j.cub.2005.04.053
69. Collier SM, Hamel LP, Moffett P. Cell death mediated by the Nterminal domains of a unique and highly conserved class of NB-LRR protein. Mol Plant Microbe Interact (2011) 24:918-31. doi:10.1094/ MPMI-03-11-0050
70. Parker JE, Holub EB, Frost LN, Falk A, Gunn ND, Daniels MJ. Characterization of eds1,amutation inArabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. Plant Cell (1996) 8:2033-46. doi:10.2307/ 3870410
71. Aarts N,Metz M,Holub E,Staskawicz BJ, Daniels MJ, Parker JE. Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis. Proc Natl Acad Sci U S A (1998) 95:10306-11. doi:10.1073/pnas.95. 17.10306
72. Bhattacharjee S, Halane MK, Kim SH, Gassmann W. Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science (2011) 334:1405-8. doi:10.1126/science.1211592
73. Kwon SI, Koczan JM, Gassmann W. Two Arabidopsis srfr (suppressor of rps4-RLD) mutants exhibit avrRps4-specific disease resistance independent of RPS4. Plant J (2004) 40:366-75. doi:10.1111/j. 1365-313X.2004.02213.x
74. Kwon SI, Kim SH, Bhattacharjee S, Noh JJ, Gassmann W. SRFR1,a suppressor of effector-triggered immunity, encodes a conserved tetratricopeptide repeat protein with similarity to transcriptional repressors. Plant J (2009) 57:109-19. doi:10. 1111/j.1365-313X.2008.03669.x
75. Sohn KH, Hughes RK, Piquerez SJ, Jones JD, Banfield MJ. Distinct regions of the Pseudomonas syringae coiled-coil effector Avr-Rps4 are required for activation of immunity. Proc Natl Acad Sci U S A (2012) 109:16371-6. doi:10.1073/ pnas.1212332109
76. Kim SH, Gao F, Bhattacharjee S, Adiasor JA, Nam JC, Gassmann W. The Arabidopsis resistance-like gene SNC1 is activated by mutations in SRFR1 and contributes to resistance to the bacterial effector AvrRps4. PLoS Pathog (2010) 6:e1001172. doi:10.1371/journal. ppat.1001172
77. Li Y, Li S, Bi D, Cheng YT, Li X, Zhang Y. SRFR1 negatively regulates plant NB-LRR resistance protein accumulation to prevent autoimmunity. PLoS Pathog (2010) 6:e1001111. doi:10.1371/ journal.ppat.1001111
78. Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M, Li X, et al. Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proc Natl Acad Sci U S A (2010) 107:13960-5. doi:10.1073/ pnas.1002828107
79. Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLoS Pathog (2013) 9:e1003235. doi:10.1371/ journal.ppat.1003235
80. Inoue H, Hayashi N, Matsushita A, Xinqiong L, Nakayama A, Sugano S, et al. Blast resistance of CC-NBLRR protein Pb1 is mediated by WRKY45 through protein-protein interaction. Proc Natl Acad Sci U S A (2013) 110:9577-82. doi:10.1073/ pnas.1222155110
81. Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerstrom M. Phospholipase-dependent signalling during the AvrRpm1-and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J (2006) 47:947-59. doi:10. 1111/j.1365-313X.2006.02844.x
82. Boudsocq M, Willmann MR, Mccormack M, Lee H, Shan L, He P, et al. Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature (2010) 464:418-22. doi:10.1038/nature08794
83. Gao X, Chen X, Lin W, Chen S, Lu D, Niu Y, et al. Bifurcation of Arabidopsis NLR immune signaling via Ca(2)(+)-dependent protein kinases. PLoS Pathog (2013) 9:e1003127. doi:10.1371/journal.ppat.1003127
84. Nomura H, Komori T, Uemura S, Kanda Y, Shimotani K, Nakai K, et al. Chloroplast-mediated activation of plant immune signalling in Arabidopsis. NatCommun (2012) 3:926. doi:10.1038/ncomms1926
85. Narusaka M, Kubo Y, Hatakeyama K, Imamura J, Ezura H, Nanasato Y, et al. Interfamily transfer of dual NB-LRR genes confers resistance to multiple pathogens. PLoS ONE (2013) 8:e55954. doi:10.1371/ journal.pone.0055954
86. Dodds PN, Lawrence GJ, Catanzariti AM, Ayliffe MA, Ellis JG. The Melampsora lini AvrL567 avirulence genes are expressed in haustoria and their products are recognized inside plant cells. Plant Cell (2004) 16:755-68. doi:10.1105/tpc.020040
87. Day B, Dahlbeck D, Huang J, Chisholm ST, Li D, Staskawicz BJ. Molecular basis for the RIN4 negative regulation of RPS2 disease resistance. Plant Cell (2005) 17:1292-305. doi:10.1105/tpc.104. 030163
88. Bai S, Liu J, Chang C, Zhang L, Maekawa T, Wang Q, et al. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS Pathog (2012) 8:e1002752. doi:10.1371/journal.ppat.1002752
89. Maekawa T, Kracher B, Vernaldi S, Ver Loren Van Themaat E, Schulze-Lefert P. Conservation of NLRtriggered immunity across plant lineages. Proc Natl Acad Sci U S A (2012) 109:20119-23. doi:10.1073/ pnas.1218059109
90. Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F, Dangl JL, et al. Arabidopsis type I metacaspases control cell death. Science (2010) 330:1393-7. doi:10. 1126/science.1194980
91. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K, Ogasawara K, et al. A novel membrane fusionmediated plant immunity against bacterial pathogens. Genes Dev (2009) 23:2496-506. doi:10.1101/ gad.1825209
92. Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI, Kim SH, et al. Phytaspase, a relocalisable cell death promoting plant protease with caspasespecificity.EMBO J (2010) 29:1149-61. doi:10.1038/ emboj.2010.1
93. Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proc Natl Acad Sci U S A (2011) 108: 10774-9. doi:10.1073/pnas. 1103338108
94. Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY. A bacterial virulence protein suppresses host innate immunity tocause plant disease. Science (2006) 313:220-3. doi:10.1126/science.1129523
95. Elmore JM, Liu J, Smith B, Phinney B, Coaker G. Quantitative proteomics reveals dynamic changes in the plasma membrane during Arabidopsis immune signaling.Mol Cell Proteomics (2012) 11:M111014555. doi:10.1074/mcp.M111.014555
96. Zhang X,Zhao H, Gao S,Wang WC, Katiyar-Agarwal S,Huang HD, et al. Arabidopsis Argonaute 2 regulates innate immunity via miRNA 393(*)-mediated silencing of a Golgilocalized SNARE gene, MEMB12. Mol Cell (2011) 42:356-66. doi:10. 1016/j.molcel.2011.04.010
97. Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G. RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biol (2009) 7:e1000139. doi:10.1371/journal.pbio.1000139