MAMP (microbe-associated molecular pattern) triggered immunity in plants

Frontiers in Plant Science

Volumn 4, Issue MAY, 2013, Pages

  Newman, Mari Anne ^a   Sundelin, Thomas ^a   Nielsen, Jon T ^a   Erbs, Gitte ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Ax21; Chitin; EF Tu; Flg22; Innate immunity; LPS; MAMPs; PGN

Indexed keywords

EID: 84885852278     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00139     Document Type: Review

References (175)

1. Aslam, S. N., Erbs, G., Morrissey, K. L., Newman, M.-A., Chinchilla, D., Boller, T., et al. (2009). MAMPs signatures, synergy, size and charge: influences on perception or mobility and host defense responses. Mol. Plant Pathol. 10, 375-387.
2. Ausubel, F. (2005). Are innate immune signalling pathways in plants and animals conserved? Nat. Immunol. 6, 973-979.
3. Bailey, B. A., Dean, J. F. D., and Anderson, J. D. (1990). An ethylene biosynthesis inducing endoxylanase elicits electrolyte leakage and necrosis in Nicotiana tabacum cv xanthi Leaves. Plant Physiol. 94, 1849-1854.
4. Bar, M., and Avni, A. (2009). EHD2 inhibits ligand-induced endocytosis and signaling of the leucine-rich repeat receptor-like protein LeEix2. Plant J. 59, 600-611.
5. Bar, M., Sharfman, M., Ron, M., and Avni, A. (2010). BAK1 is required for the attenuation of ethylene-inducing xylanase (Eix)-induced defense responses by the decoy receptor LeEix1. Plant J. 63, 791-800.
6. Bauer, Z., Gomez-Gomez, L., Boller, T., and Felix, G. (2001). Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptorbinding sites. J. Biol. Chem. 276, 45669-45676.
7. Bedini, E., De Castro, C., Erbs, G., Mangoni, L., Dow, J. M., Newman, M.-A., et al. (2005). Structure-dependent modulation of a pathogen response in plants by synthetic O-antigen polysaccharides. J. Am. Chem. Soc. 127, 2414-2416.
8. Bedini, E., Parrilli, M., and Unverzagt, C. (2002). Oligomerization of a rhamnanic trisaccharide repeating unit of O-chain polysaccharides from phytopathogenic bacteria. Tetrahedron Lett. 43, 8879-8882.
9. Bent, A. F., and MacKey, D. (2007). Elicitors, effectors, and R genes: the new paradigm and a lifetime supply of questions. Annu. Rev. Phytopathol. 45, 399-436.
10. Bogdanove, A. J., Koebnik, R., Lu, H., Furutani, A., Angiuoli, S. V., Patil, P. B., et al. (2011). Two new complete genome sequences offer insight into host and tissue specificity of plant pathogenic Xanthomonas spp. J. Bacteriol. 193, 5450-5464.
11. Boller, T., and Felix, G. (2009). A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60, 379-406.
12. Braun, S. G., Meyer, A., Holst, O., Pühler, A., and Niehaus, K. (2005). Characterization of the Xanthomonas campestris pv. campestris lipopolysaccharide substructures essential for elicitation of an oxidative burst in tobacco cells. Mol. Plant Microbe Interact. 18, 674-681.
13. Brutus, A., Sicilia, F., Macone, A., Cervone, F., and De Lorenzo, G. (2010). A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Sci. U.S.A. 107, 9452-9457.
14. Burdman, S., Shen, Y., Lee, S. W., Xue, Q., and Ronald, P. C. (2004). RaxH/RaxR: a two-component regulatory system in Xanthomonas oryzae pv. oryzae required for AvrXa21 activity. Mol. Plant-Microbe Interact. 17, 602-612.
15. Cai, R., Lewis, J., Yan, S., Liu, H., Clarke, C. R., Campanile, F., et al. (2011). The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog. 7:e1002130. doi: 10.1371/journal.ppat.1002130
16. Chamaillard, M., Hashimoto, M., Horie, Y., Masumoto, J., Qiu, S., Saab, L., et al. (2003). An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat. Immunol. 4, 702-707.
17. Chen, X., Chern, M., Canlas, P. E., Ruan, D., Jiang, C., and Ronald, P. C. (2010). An ATPase promotes autophosphorylation of the pattern recognition receptor XA21 and inhibits XA21-mediated immunity. Proc. Natl. Acad. Sci. U.S.A. 107, 8029-8034.
18. Cheong, J.-J., and Hahn, M. G. (1991). A specific, high-affinity binding site for the hepta-β-glucoside elicitor exists in soybean membranes. Plant Cell 3, 137-147.
19. Chinchilla, D., Bauer, Z., Regenass, M., Boller, T., and Felix, G. (2006). The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18, 465-476.
20. Chinchilla, D., Zipfel, C., Robatzek, S., Kemmerling, B., Nurnberger, T., Jones, D. G. J., et al. (2007). A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defense. Nature 448, 497-500.
21. Csorba, T., Pantaleo, V., and Burgyán, J. (2009). RNA silencing: an antiviral mechanism. Adv. Virus Res. 75, 35-71.
22. da Silva, F. G., Shen, Y., Dardick, C., Burdman, S., Yadav, R. C., de Leon, A. L., et al. (2004). Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Mol. Plant-Microbe Interact. 17, 593-601.
23. Danna, C. H., Millet, Y. A., Koller, T., Han, S. W., Bent, A. F., Ronald, P. C., et al. (2011). The Arabidopsis flagellin receptor FLS2 mediates the perception of Xanthomonas Ax21 secreted peptides. Proc. Natl. Acad. Sci. U.S.A. 108, 9286-9291.
24. Danna, C. H., Zhang, X. C., Khatri, A., Bent, A. F., Ronald, P. C., and Ausubel, F. M. (2012). FLS2-mediated responses to Ax21-derived peptides: response to the Mueller et al. commentary. Plant Cell 24, 3174-3176.
25. Dardick, C., and Ronald, P. (2006). Plant and animal pathogen recognition receptors signal through non-RD kinases. PLoS Pathog. 2:e2. doi: 10.1371/journal.ppat.0020002
26. Darvill, A. G., and Albersheim, P. (1984). Phytoalexins and their elicitors-a defense against microbial infection in plants. Annu. Rev. Plant Physiol. 35, 243-275.
27. de Jonge, R., Peter van Esse, H., Maruthachalam, K., Bolton, M. D., Santhanam, P., Saber, M. K., et al. (2012). Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. U.S.A. 109, 5110-5115.
28. Denoux, C., Galletti, R., Mammarella, N., Gopalan, S., Werck, D., De Lorenzo, G., et al. (2008). Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol. Plant 1, 423-445.
29. Desaki, Y., Miya, A., Venkatesh, B., Tsuyumu, S., Yamane, H., Kaku, H., et al. (2006). Bacterial lipopolysaccharides induce defense responses associated with programmed cell death in rice cells. Plant Cell Physiol. 47, 1530-1540.
30. Desaki, Y., Otomo, I., Kobayashi, D., Jikumaru, Y., Kamiya, Y., Venkatesh, B., et al. (2012). Positive crosstalk of MAMP signaling pathways in rice cells. PLoS ONE 7:e51953. doi: 10.1371/journal.pone.0051953
31. Dow, M., Newman, M.-A., and von Roepenack, E. (2000). The induction and modulation of plant defense responses by bacterial lipopolysaccharides. Annu. Rev. Phytopathol. 38, 241-261.
32. Dow, J. M., Osbourn, A. E., Wilson, T. J. G., and Daniels, M. J. (1995). A locus determining pathogenicity of Xanthomonas-campestris is involved in lipopolysaccharide biosynthesis. Mol. Plant Microbe Interact. 8, 768-777.
33. Dziarski, R., and Gupta, D. (2006). The peptidoglycan recognition proteins (PGRPs). Genome Biol. 7, 232-245.
34. Erbs, G., and Newman, M.-A. (2012). The role of lipopolysaccharide and peptidoglycan, two glycosylated bacterial microbe-associated molecular patterns (MAMPs), in plant innate immunity. Mol. Plant Pathol. 13, 95-104.
35. Erbs, G., Silipo, A., Aslam, S., De Castro, C., Liparoti, V., Flagiello, A., et al. (2008a). Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomanas elicit innate immunity: structure and activity. Chem. Biol. 15, 438-448.
36. Erbs, G., Jensen, T. T., Silipo, A., Grant, W., Dow, J. M., Molinaro, A., et al. (2008b). An antagonist of lipid A action in mammals has complex effects on lipid A induction of defense responses in the model plant Arabidopsis thaliana. Microbes Infect. 10, 571-574.
37. Felix, G., and Boller, T. (2003a). Molecular sensing of bacteria in plants. J. Biol. Chem. 278, 6201-6208.
38. Felix, G., and Boller, T. (2003b). 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.
39. Felix, G., Duran, J. D., Volko, S., and Boller, T. (1999). Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J. 18, 265-276.
40. Felix, G., Regenass, M., and Boller, T. (1993). Specific perception of subnanomolar concentrations of chitin fragments by tomato cells-induction of extracellular alkalinization, changes in protein phosphorylation, and establishment of a refractory state. Plant J. 4, 307-316.
41. Fischer, S. E., Miguel, M. J., and Mori, G. B. (2003). Effect of root exudates on the exopolysaccharide composition and the lipopolysaccharide profile of Azospirillum brasilense Cd under saline stress. FEMS Microbiol. Lett. 219, 53-62.
42. Flor, H. H. (1942). Inheritance of pathogenicity in Melampsora lini. Phytopathology 32, 653-669.
43. Fradin, E. F., Zhang, Z., Ayala, J. C. J., Castroverde, C. D. M., Nazar, R. N., Robb, J., et al. (2009). Genetic dissection of Verticillium wilt resistance mediated by tomato Ve1. Plant Physiol. 150, 320-332.
44. Furman-Matarasso, N., Cohen, E., Du, Q., Chejanovsky, N., Hanania, U., and Avni, A. (1999). A point mutation in the ethylene-inducing xylanase elicitor inhibits the β-1-4-endoxylanase activity but not the elicitation activity. Plant Physiol. 121, 345-351.
45. Gaulin, E., Dramé, N., Lafitte, C., Torto-Alalibo, T., Martinez, Y., Ameline-Torregrosa, C., et al. (2006). Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18, 1766-1777.
46. Gerber, I. B., Laukens, K., De Vijlder, T., Witters, E., and Dubery, I. A. (2008). Proteomic profiling of cellular targets of lipopolysaccharide-induced signaling in Nicotiana tabacum BY-2 cells. Biochim. Biophys. Acta 1784, 1750-1762.
47. Gerber, I. B., Laukens, K., Witters, E., and Dubery, I. A. (2006). Lipopolysaccharide-responsive phosphoproteins in Nicotiana tabacum cells. Plant Physiol. Biochem. 44, 369-379.
48. Gimenez-Ibanez, S., Ntoukakis, V., and Rathjen, J. P. (2009). The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Signal. Behav. 4, 539-541.
49. Girardin, S. E., Travassos, L. H., Herve, M., Blanot, D., Boneca, I. G., Philpott, D. J., et al. (2003). Peptidoglycan molecular requirements allowing detection by Nod1 and Nod2. J. Biol. Chem. 278, 41702-41708.
50. Gómez-Gómez, L., Bauer, Z., and Boller, T. (2001). Both the extracellular leucine-rich repeat domain and the kinase activity of FLS2 are required for flagellin binding and signalling in Arabidopsis. Plant Cell 13, 1155-1163.
51. Gomez-Gomez, L., and Boller, T. (2000). FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol. Cell 5, 1003-1011.
52. Greenberg, J. T. (1997). Programmed cell death in plant-pathogen interactions. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 525-545.
53. Gross, A., Kapp, D., Nielsen, T., and Niehaus, K. (2005). Endocytosis of Xathomonas campestris pathovar campestris lipopolysaccharides in non-host plant cells of N. benthamiana. New Phytol. 165, 215-226.
54. Gust, A., Biswas, R., Lenz, H. D., Rauhut, T., Ranf, S., Kemmerling, B., et al. (2007). Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J. Biol. Chem. 282, 32338-32348.
55. Gust, A. A., Willmann, R., Desaki, Y., Grabherr, H. M., and Nürnberger, T. (2012). Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci. 17, 495-502.
56. Gutsmann, T., Schromm, A. B., and Brandenburg, K. (2007). The physiochemistry of endotoxins in relation to bioactivity. J. Med. Microbiol. 297, 341-352.
57. Hammond-Kosack, K. E., and Jones, J. D. (1996). Resistance gene-dependent plant defense responses. Plant Cell 8, 1773-1791.
58. Han, S. W., Sriariyanum, M., Lee, S. W., Sharma, M., Bahar, O., Bower, Z., et al. (2011). Small protein-mediated quorum sensing in a gram negative bacterium. PLoS ONE 6:e29192. doi: 10.1371/journal.pone.0029192
59. Häweker, H., Rips, S., Koiwa, H., Salomon, S., Saijo, Y., Chinchilla, D., et al. (2010). Pattern recognition receptors require N-glycosylation to mediate plant immunity. J. Biol. Chem. 285, 4629-4636.
60. Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D. R., et al. (2001). The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103.
61. He, P., Shan, L., Lin, N.-C., Martin, G. B., Kemmerling, B., Nürnberger, T., et al. (2006). Specific bacterial suppressors of MAMP signalling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125, 563-575.
62. Holton, N., Caño-Delgado, A., Harrison, K., Montoya, T., Chory, J., and Bishop, G. J. (2007). Tomato BRASSINOSTEROID INTENSITIVE1 is required for systemin-induced root elongation in Solanum pimpinellifoliumbut is not essential for wound signaling. Plant Cell 19, 1709-1717.
63. Huffaker, A., Pearce, G., and Ryan, C. A. (2006). An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc. Natl. Acad. Sci. U.S.A. 103, 10098-10103.
64. Ialenti, A., Di Meglio, P., Grassia, G., Maffia, P., Di Rosa, M., Lanzetta, R., et al. (2006). A novel lipid A from Halomonas magadiensis inhibits enteric LPS-induced human monocyte activation. Eur. J. Immunol. 36, 354-360.
65. Inohara, N., Chamaillard, M., McDonald, C., and Nunez, G. (2005). NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu. Rev. Biochem. 74, 355-383.
66. Jamir, Y., Guo, M., Oh, H.-S., Petnicki-Ocwieja, T., Chen, S., Tang, X., et al. (2004). Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J. 37, 554-565.
67. Jeppesen, M. G., Navratil, T., Spremulli, L. L., and Nyborg, J. (2005). Crystal structure of the bovine mitochondrial elongation factor Tu. Ts complex. J. Biol. Chem. 280, 5071-5081.
68. Jiang, S., Naito, M., Kaizu, C., Kuwata, K., Hasegawa, G., Mukaida, N., et al. (2000). Lipopolysaccharide-induced cytokine and receptor expression and neutrophil infiltration in the liver of osteopetrosis (op/op) mutant mice. Liver 20, 465-474.
69. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329.
70. Kaku, H., Nishizawa, Y., Ishll-Minami, N., Akimoto-Tomlyama, C., Dohmae, N., Taklo, K., et al. (2006). Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. U.S.A. 103, 11086-11091.
71. Kannenberg, E. L., and Carlson, R. W. (2001). Lipid A and O-chain modifications cause rhizobium lipopolysaccharides to become hydrophobic during bacteroid development. Mol. Microbiol. 39, 379-391.
72. Kauss, H., Fauth, M., Merten, A., and Jeblick, W. (1999). Cucumber hypocotyls respond to cutin monomers via both an inducible and a constitutive H2O2-generating system. Plant Physiol. 120, 1175-1182.
73. Kawchuk, L., Hachey, J., Lynch, D. R., Klcsar, F., van Rooijen, G., Waterer, D. R., et al. (2001). Tomato Ve disease resistance genes encode cell surface-like receptors. Proc. Natl Acad. Sci. U.S.A. 98, 6511-6515.
74. Khush, G. S., Bacalangco, E., and Ogawa, T. (1990). A new resistance gene to bacterial blight derived from O. longistaminata. Rice Genet. 7, 121-122.
75. Kunze, G., Zipfel, C., Robatzek, S., Niehaus, K., Boller, T., and Felix, G. (2004). The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16, 3496-3507.
76. Lamb, C., and Dixon, R. A. (1997). The oxidative burst in plant disease resistance. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 251-275.
77. Lanfermeijer, F. C., Staal, M., Malinowski, R., Stratmann, J. W., and Elzenga, T. M. (2008). Micro-electrode flux estimation confirms that the Solanum pimpinellifolium cu3 mutant still responds to systemin. Plant Physiol. 146, 129-139.
78. Lee, I., Seo, Y. S., Coltrane, D., Hwang, S., Oh, T., Marcotte, E. M., et al. (2011). Genetic dissection of the biotic stress response using a genome-scale gene network for rice. Proc. Natl. Acad. Sci. U.S.A. 108, 18548-18553.
79. Lee, S. W., Han, S. W., Sririyanum, M., Park, C. J., Seo, Y. S., and Ronald, P. C. (2009). A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science 326, 850-853.
80. Lee, S.-W., Han, S.-W., Bartley, L. E., and Ronald, P. C. (2006). Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proc. Natl. Acad. Sci. U.S.A. 103, 18395-18400.
81. Lee, S. W., Jeong, K. S., Han, S. W., Lee, S. E., Phee, B. K., Hahn, T. R., et al. (2008). The Xanthomonas oryzae pv. oryzae PhoPQ two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J. Bacteriol. 190, 2183-2196.
82. Leeman, M., Vanpelt, J. A., Denouden, F. M., Heinsbroek, M., Pahm, B., and Schippers, B. (1995). Induction of systemic resistance against fusarium-wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathol 85, 1021-1027.
83. Li, C., Guan, Z., Liu, D., and Raetz, C. R. H. (2011). Pathway for lipid A biosynthesis in Arabidopsis thalianaresembling that of Escherichia coli. Proc. Natl. Acad. Sci. U.S. A 108, 11397-11392.
84. Liu, B., Li, J.-F., Ao, Y., Qu, J., Li, Z., Su, J., et al. (2012). Lysin motif-containing proteins LYP4 and LYP6 play dual roles in peptidoglycan and chitin perception in rice innate immunity. Plant Cell 24, 3406-3419.
85. Livaja, M., Zeidler, D., von Rad, U., and Durner, J. (2008). Transcriptional responses of Arabidopsis thaliana to the bacteria-derived PAMPs harpin and lipopolysaccharide. Immunobiology 213, 161-171.
86. Lopez-Gomez, M., Sandal, N., Stougaard, J., and Boller, T. (2012). Interplay of flg22-induced defense responses and nodulation in Lotus japonicas. J. Exp. Bot. 63, 393-401.
87. Loppnow, H., Brade, H., Durrbaum, I., Dinarello, C. A., Kusumoto, S., Rietschel, E. T., et al. (1989). IL-1 induction-capacity of defined lipopolysaccharide partial structures. J. Immunol. 142, 3229-3238.
88. Lotze, M. T., Zeh, H. J., Rubartelli, A., Sparvero, L. J., Amoscato, A. A., Washburn, N. R., et al. (2007). The grateful dead: damage associated molecular pattern molecules and reduction/oxidation regulates immunity. Immunol. Rev. 220, 60-81.
89. Lu, D., Wu, S., Gao, X., Zhang, Y., Shan, L., and He, P. (2010). A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc. Natl. Acad. Sci. U.S.A. 107, 496-501.
90. Mackey, D., and McFall, A. J. (2006). MAMPs and MIMPs: proposed classifications for inducers of innate immunity. Mol. Microbiol. 61, 1365-1371.
91. Madala, N. E., Leone, M. R., Molinaro, A., and Dubery, I. A. (2011). Deciphering the structural and biological properties of the lipid A moiety of lipopolysaccharides from Burkholderia cepacia strain ASP B 2D, in Arabidopsis thaliana. Glycobiology 21, 184-194.
92. Maekawa, T., Kufer, T. A., and Schulze-Lefert, P. (2011). NLR functions in plant and animal immune systems: so far and yet so close. Nat. Immunol. 12, 817-826.
93. 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 lectin-like activities. Mol. Plant Microbe Interact. 10, 1045-1053.
94. McCann, H. C., Nahal, H., Thakur, S., and Guttman, D. S. (2012). Identification of innate immunity elicitors using molecular signatures of natural selection. Proc. Natl. Acad. Sci. U.S.A. 109, 4215-4220.
95. McCarthy, Y., Dow, J. M., and Ryan, R. P. (2011). The Ax21 protein is a cell-cell signal that regulates virulence in the nosocomial pathogen Stenotrophomonas maltophilia. J. Bacteriol. 193, 6375-6378.
96. McCoy, S. L., Kurtz, S. E., Hausman, F. A., Trune, D. R., Bennett, R. M., and Hefeneider, S. H. (2004). Activation of RAW264.7 macrophages by bacterial DNA and lipopolysaccharides increases cell surface DNA binding and internalization. J. Biol. Chem. 279, 17217-17223.
97. McDonald, C., Inohara, N., and Nuñez, G. (2005). Peptidoglycan signalling in innate immunity and inflammatory disease. J. Biol. Chem. 280, 20177-20180.
98. McGurl, B., Pearce, G., Orozco-Cardemas, M., and Ryan, C. A. (1992). Structure, expression, and antisese inhibition of the systemin precursor gene. Science 255, 1570-1573.
99. Meindl, T., Boller, T., and Felix, G. (2000). The bacterial elicitor flagellin activates its receptor in tomato cells according to the address-message concept. Plant Cell 12, 1783-1794.
100. Miyake, K. (2004). Innate recognition of lipopolysaccharide by Toll-like receptor 4-MD-2. Trends Microbiol. 12, 186-192.
101. Mishina, T. E., and Zeier, J. (2006). The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol. 141, 1666-1675.
102. Mishina, T. E., and Zeier, J. (2007). Pathogen-associated molecular pattern recognition rather than development of tissue necrosis contributes to bacterial induction of systemic acquired resistance in Arabidopsis. Plant J. 50, 500-513.
103. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., et al. (2007). CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 19613-19618.
104. Mueller, K., Chinchilla, D., Albert, M., Jehle, A. K., Kalbacher, H., Boller, T., et al. (2012). Contamination risks in work with synthetic peptides: flg22 as an example of a pirate in commercial peptide preparations. Plant Cell 24, 3193-3197.
105. Munford, R. S., and Varley, A. W. (2006). Shield as signal: lipopolysaccharide and the evolution of immunity to Gram-negative bacteria. PLoS Pathog. 2:e67. doi: 10.1371/journal.ppat.0020067
106. Narváez-Vásquez, J., and Ryan, C. A. (2004). The cellular localization of prosystemin: a functional role for phloem parenchyma in systemic wound signaling. Planta 218, 360-369.
107. Newman, M.-A., Daniels, M. J., and Dow, J. M. (1995). Lipopolysaccharide from Xanthomonas campestris induces defense-related gene expression in Brassica campestris. Mol. Plant Microbe Interact. 8, 778-780.
108. Newman, M.-A., Dow, J. M., Molinaro, A., and Parrilli, M. (2007). Priming, induction and modulation of plant defense responses by bacterial lipopolysaccharides. J. Endotoxin Res. 13, 68-79.
109. Newman, M. A., von Roepenack-Lahaye, E., Parr, A., Daniels, M. J., and Dow, J. M. (2002). Prior exposure to lipopolysaccharide potentiates expression of plant defenses in response to bacteria. Plant J. 29, 487-495.
110. Nguyen, H. P., Chakravarthy, S., Velásquez, A. C., McLane, H. L., Zeng, L., Nakayashiki, H., et al. (2010). Methods to Study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol. Plant Microbe Interact 23, 991-999.
111. Nomura, K., DebRoy, S., Lee, Y. H., Pumplin, N., Jones, J., and He, S. Y. (2006). A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313, 220-223.
112. Nothnagel, E. A., McNeil, M., Albersheim, P., and Dell, A. (1983). Host-pathogen interactions: XXII. A galacturonic acid oligosaccharide from plant cell walls elicits phytoalexins. Plant Physiol. 71, 916-926.
113. Nürnberger, T., and Kemmerling, B. (2006). Receptor protein kinases-pattern recognition receptors in plant immunity. Trends Plant Sci. 11, 519-522.
114. 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.
115. Park, C. J., Peng, Y., Chen, X., Dardick, C., Ruan, D., Bart, R., et al. (2008). Rice XB15, a protein phosphatase 2C negatively regulates cell death and XA21-mediated innate immunity. PLoS Biol. 6:e231. doi: 10.1371/journal.pbio.0060231
116. Park, C. J., and Ronald, P. C. (2012). Cleavage and nuclear localization of the rice XA21 immune receptor. Nat. Commun. 3, 920.
117. Pearce, G., Strydom, D., Johnson, S., and Ryan, C. A. (1991). A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253, 895-898.
118. Peng, Y., Bartley, L. E., Chen, X., Dardick, C., Chern, M., Ruan, R., et al. (2008). OsWRKY62 is a negative regulator of basal and Xa21-mediated defense against Xanthomonas oryzae pv. oryzae in rice. Mol. Plant 1, 446-458.
119. Prime-A-Plant Group: Conrath, U., Beckers, G. J. M., Flors, V., García-Agustín, P., Jakab, G., Mauch, F., et al. (2006). Priming: getting ready for battle. Mol. Plant-Microbe Interact. 19, 1062-107.
120. Raetz, C. R. H., Reynolds, C. M., Trent, M. S., and Bishop, R. E. (2007). Lipid A modification systems in Gram-negative bacteria. Annu. Rev. Biochem. 76, 295-329.
121. Raetz, C. R. H., and Whitfield, C. (2002). Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700.
122. Rallabhandi, P., Awomoyi, A., Thomas, K. E., Phalipon, A., Fujimoto, Y., Fukase, K., et al. (2008). Differential activation of human TLR4 by Escherichia coli and Shigella flexneri 2a lipopolysaccharide: combined effects of lipid A acylation state and TLR4 polymorphisms on signaling. J. Immunol. 180, 1139-1147.
123. Ramos, H. C., Rumbo, M., and Sirard, J.-C. (2004). Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12, 509-517.
124. Robatzek, S., Bittel, P., Chinchilla, D., Kochner, P., Felix, G., Shiu, S. H., et al. (2007). Molecular identification and characterization of the tomato flagellin LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol. Biol. 64, 539-547.
125. Robatzek, S., Chinchilla, D., and Boller, T. (2006). Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev. 20, 537-542.
126. Rockel, P., Strube, F., Rockel, A., Wildt, J., and Kaiser, W. M. (2002). Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53, 103-110.
127. Ron, M., and Avni, A. (2004). The receptor for the fungal elicitor ethylene-inducing xylanase is a member of a resistance-like gene family in tomato. Plant Cell 16, 1604-1615.
128. Ronald, P. C., Albano, B., Tabien, R., Abenes, L., Wu, K. S., McCouch, S., et al. (1992). Genetic and physical analysis of the rice bacterial blight disease resistance locus, Xa21. Mol. Gen. Genet. 236, 113-120.
129. Roux, M., Schwessinger, B., Albrecht, C., Chinchilla, D., Jones, A., Holton, N., et al. (2011). The Arabidopsisleucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23, 2440-2455.
130. Ruiz-Ferrer, V., and Voinnet, O. (2009). Roles of plant small RNAs in biotic stress responses. Annu. Rev. Plant Biol. 60, 485-510.
131. Russinova, E., Borst, J.-W., Kwaaitaal, M., Cano-Delgado, A., Yin, Y., Chory, J., et al. (2004). Heterodimerization and endocytosis of Arabidopsis brassinosteroid receptors BRI1 and AtSERK3 (BAK1). Plant Cell 16, 3216-3229.
132. Ryals, J. A., Neuenschwander, U. H., Willits, M. G., Molina, A., Steiner, H.-Y., and Hunt, M. D. (1996). Systemic acquired resistance. Plant Cell 8, 1809-1819.
133. Scheer, J. M., and Ryan, C. A. (1999). A 160-kD systemin receptor on the Surface of Lycopersicon peruvianumsuspension-cultured cells. Plant Cell 11, 1525-1535.
134. Scheer, J. M., and Ryan, C. A. (2002). The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc. Natl. Acad. Sci. U.S.A. 99, 9585-9590.
135. Schneider, M., Schweizer, P., Meuwly, P., and Metraux, J. P. (1996). Systemic acquired resistance in plants. Int. Rev. Cytol. 168, 303-340.
136. Schromm, A., Brandenburg, K., Loppnow, H., Moran, A., Koch, M., Rietschel, E., et al. (2000). Biological activities of lipopolysaccharides are determined by the shape of their lipid A portion. Eur. J. Biochem. 267, 2008-2013.
137. Schromm, A., Brandenburg, K., Loppnow, H., Zahringer, U., Rietschel, E., Carroll, S., et al. (1998). The charge of endotoxin molecules influences their conformation and IL-6-inducing capacity. J. Immunol. 161, 5464-5471.
138. Schulze, B., Mentzel, T., Jehle, A. K., Mueller, K., Beeler, S., Boller, T., et al. (2010). Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J. Biol. Chem. 285, 9444-9451.
139. Schweizer, P., Felix, G., Buchala, A., Müller, C., and Métraux, J. P. (1996). Perception of free cutin monomers by plant cells. Plant J. 10, 331-341.
140. Séjalon-Delmas, N., Mateos, F. V., Bottin, A., Rickauer, M., Dargent, R., and Esquerré-Tugayé, M. T. (1997). Purification, elicitor activity, and cell wall localization of a glycoprotein from phytophthora parasitica var. nicotianae, a fungal pathogen of tobacco. Phytopathology 9, 899-909.
141. Seong, S. Y., and Matzinger, P. (2004). Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Immunol. 4, 469-478.
142. Shen, Y., Sharma, P., da Silva, F. G., and Ronald, P. (2002). The Xanthomonas oryzae pv. oryzae raxP and raxQ genes encode an ATP sulphurylase and adenosine-5'-phosphosulphate kinase that are required for AvrXa21 avirulence activity. Mol. Microbiol. 44, 37-48.
143. Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., et al. (2010). Two Lys M receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204-214.
144. Shinya, T., Motoyama, N., Ikeda, A., Wada, M., Kamiya, K., Hayafune, M., et al. (2012). Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol. 53, 1696-1706.
145. Shiu, S. H., and Bleecker, A. B. (2003). Expansion of the receptor-like kinase/pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 132, 530-543.
146. Shiu, S.-H., Karlowski, W. M., Pan, R., Tzeng, Y.-H., Mayer, K. F. X., and Li, W.-H. (2004). Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16, 1220-1234.
147. Shuguo, H., Wei, Z., Chao, Z., and Daoji, W. (2012). One-step expression and tyrosine O-sulfonation of Ax21 in Escherichia coli. Appl. Biochem. Biotechnol. 166, 1368-1379.
148. Silipo, A., Leone, M. R., Erbs, G., Lanzetta, R., Parrilli, M., Chang, W.-S., et al. (2011). A unique bicyclic monosaccharide from the Bradyrhizobium lipopolysaccharide and its role in the molecular interaction with plants. Angew. Chem. 50, 12610-12612.
149. Silipo, A., Molinaro, A., Sturiale, L., Dow, J. M., Erbs, G., Lanzetta, R., et al. (2005). The elicitation of plant innate immunity by lipooligosaccharide of Xanthomonas campestris. J. Biol. Chem. 280, 33660-33668.
150. Silipo, A., Sturiale, L., Garozzo, D., de Castro, C., Lanzetta, R., Parrilli, M., et al. (2004). Structure elucidation of the highly heterogeneous lipid A from the lipopolysaccharide of the Gram-negative extremophile bacterium Halomonas magadiensis strain 21 M1. Eur. J. Org. Chem. 2004, 2263-2271.
151. Silipo, A., Sturiale, L., Garozzo, D., Erbs, G., Tandrup Jensen, T., Lanzetta, R., et al. (2008). The acylation and phosphorylation pattern of lipid A from Xanthomonas campestris strongly influence its ability to trigger the innate immune response in Arabidopsis. Chembiochem 9, 896-904.
152. Smith, K. D., Andersen-Nissen, E., Hayashi, F., Strobe, K., Bergman, M. A., Rassoulian Barrett, S. L., et al. (2003). Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial mobility. Nat. Immunol. 4, 1247-1253.
153. Song, W. Y., Pi, L. Y., Wang, G. L., Gardner, J., Holsten, T., and Ronald, P. (1997). Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9, 1279-1287.
154. Song, W. Y., Wang, G. L., Chen, L. L., Kim, H. S., Pi, L. Y., Holsten, T., et al. (1995). A receptor kinase-like protein encoded by the rice disease resistance gene Xa21. Science 270, 1804-1806.
155. Sun, A. Z., Nie, S. J., and Xing, D. (2012). Nitric oxide-mediated maintenance of redox homeostasis contributes to NPR1-dependent plant innate immunity triggered by lipopolysaccharides. Plant Physiol. 160, 1081-1096.
156. Sun, W., Dunning, F. M., Pfund, C., Weingarten, R., and Bent, A. F. (2006). Within-species flagellin polymorphism in Xanthomonas campestris pv campestris and its impact on elicitation of Arabidopsis FLAGELLIN SENSING2-dependent defenses. Plant Cell 18, 764-779.
157. Takai, R., Isogai, A., Takayama, S., and Che, F. S. (2008). Analysis of flagellin perception mediated by flg22 receptor OsFLS2 in rice. Mol. Plant Microbe Interact. 21, 1635-1642.
158. Thomma, B. P. H. J., Nürnberger, T., and Joosten, M. H. A. J. (2011). Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23, 4-15.
159. Traub, S., von Aulock, S., Hartung, T., and Herman, C. (2006). MDP and other muropeptides-direct and synergistic effects on the immune system. J. Endotoxin Res. 12, 69-85.
160. Umemoto, N., Kakitani, M., Iwamatsu, A., Yoshikawa, M., Yamaoka, N., and Ishida, I. (1997). The structure and function of a soybean β-glucan-elicitor-binding protein. Proc. Natl. Acad. Sci. U.S.A. 94, 1029-1034.
161. van der Biezen, E. A., and Jones, J. D. (1998). Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23, 454-456.
162. van Loon, L. C., Bakker, P. A., and Pieterse, C. M. (1998). Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36, 453-483.
163. Wan, J., Tanaka, K., Zhang, X.-C., Son, G. H., Brechenmacher, L., Nguyen, T. H. N., et al. (2012). LYK4, a LysM receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 160, 396-406.
164. Wang, Y. H., Gehring, C., and Irving, H. R. (2011). Plant natriuretic peptides are apoplastic and paracrine stress response molecules. Plant Cell Physiol. 52, 837-850.
165. Wang, Y. S., Pi, L. Y., Chen, X., Chakrabarty, P. K., Jiang, J., De Leon, A. L., et al. (2006). Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18, 3635-3646.
166. Wang, G. L., Ruan, D. L., Song, W. Y., Sideris, S., Chen, L. L., Pi, L. Y., et al. (1998). Xa21D Encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell 10, 765-779.
167. Wang, G. L., Song, W. Y., Ruan, D. L., Sideris, S., and Ronald, P. C. (1996). The cloned gene, Xa21, confers resistance to multiple Xanthomonas oryzae pv. oryzae isolates in transgenic plants. Mol. Plant Microbe Interact. 9, 850-855.
168. Watt, S. A., Tellstrom, V., Patschkowski, T., and Niehaus, K. (2006). Identification of the bacterial superoxide dismutase (SodM) as plant-inducible elicitor of an oxidative burst reaction in tobacco cell suspension cultures. J. Biotechnol. 126, 78-86.
169. Willmann, R., Lajunen, H. M., Erbs, G., Newman, M.-A., Kolb, D., Tsuda, K., et al. (2011). Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl. Acad. Sci. U.S.A. 108, 19824-19829.
170. Wright, S. D., Ramos, R. A., Tobias, P. S., Ulevitch, R. J., and Mathison, J. C. (1990). CD14 serves as the cellular receptor for complexes of lipopolysaccharides with lipopolysaccharide binding protein. Science 249, 1431-1433.
171. Yamaguchi, Y., Huffaker, A., Bryan, A. C., Tax, F. E., and Ryan, C. A. (2010). PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22, 508-522.
172. Yamaguchi, Y., Pearce, G., and Ryan, C. A. (2006). The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc. Natl. Acad. Sci. U.S.A. 103, 10104-10109.
173. Zeidler, D., Dubery, I. A., Schmitt-Kopplin, P., Von Rad, U., and Durner, J. (2010). Lipopolysaccharide mobility in leaf tissue of Arabidopsis thaliana. Mol. Plant Pathol. 11, 747-755.
174. Zeidler, D., Zähringer, U., Gerber, I., Dubery, I., Hertung, T., Bors, W., et al. (2004). Innate immunity in Arabidopsis thaliana lipopolysaccharides activate nitric oxide synthase NOS and induce defense genes. Proc. Natl. Acad. Sci. U.S.A. 101, 15811-15816.
175. Zipfel, C., Kunze, G., Chinchilla, D., Caniard, A., Jones, J. D. G., Boller, T., et al. (2006). Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749-760.