A Conserved Peptide Pattern from a Widespread Microbial Virulence Factor Triggers Pattern-Induced Immunity in Arabidopsis

PLoS Pathogens

Volumn 10, Issue 11, 2014, Pages

  Böhm, Hannah ^a   Albert, Isabell ^a   Oome, Stan ^b,c   Raaymakers, Tom M ^b   Van den Ackerveken, Guido ^b,c   Nürnberger, Thorsten ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CALCEIN; FLAGELLIN; PATTERN RECOGNITION RECEPTOR; PEPTIDE; PROTEIN NLP20; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION; HISTOCHEMISTRY; IMMUNE RESPONSE; IMMUNITY; IMMUNOGENICITY; MEMBRANE VESICLE; NONHUMAN; PATTERN INDUCED IMMUNITY; PECTOBACTERIUM CAROTOVORUM; PHYLOGENETIC TREE; PHYTOPHTHORA PARASITICA; PLANT DEFENSE; PLANT IMMUNITY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BACTERIUM; CYTOLOGY; IMMUNOLOGY; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT CELL;

ARABIDOPSIS;

ARABIDOPSIS; BACTERIA; FLAGELLIN; PEPTIDES; PLANT CELLS; PLANT IMMUNITY; VIRULENCE FACTORS;

EID: 84912117998     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004491     Document Type: Article

References (44)

1. Jones JD, Dangl JL, (2006) The plant immune system. Nature 444: 323–329.
2. Boller T, 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.
3. Dodds PN, Rathjen JP, (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539–548.
4. Ottmann C, Luberacki B, Küfner I, Koch W, Brunner F, et al. (2009) A common toxin fold mediates microbial attack and plant defense. Proc Natl Acad Sci USA 106: 10359–10364.
5. Dou D, Zhou JM, (2012) Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12: 484–495.
6. Spoel SH, Dong X, (2012) How do plants achieve immunity? Defence without specialized immune cells. Nat Rev Immunol 12: 89–100.
7. Nürnberger T, Kemmerling B (2009) PAMP-triggered basal immunity in plants. In: Van Loon LC, editor. Advances in Botanical Research: Elsevier Publishers. pp. 2–38.
8. Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G, (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465–476.
9. Nürnberger T, Nennstiel D, Jabs T, Sacks WR, Hahlbrock K, et al. (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78: 449–460.
10. Brunner F, Nürnberger T, (2012) Identification of immunogenic microbial patterns takes the fast lane. Proc Natl Acad Sci USA 109: 4029–4030.
11. Monaghan J, Zipfel C, (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15: 349–357.
12. Fliegmann J, Mithöfer A, Wanner G, Ebel J, (2004) An ancient enzyme domain hidden in the putative beta-glucan elicitor receptor of soybean may play an active part in the perception of pathogen-associated molecular patterns during broad host resistance. J Biol Chem 279: 1132–1140.
13. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, et al. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749–760.
14. Jehle AK, Lipschis M, Albert M, Fallahzadeh-Mamaghani V, Fürst U, et al. (2013) The receptor-like protein ReMAX of Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell 25: 2330–2340.
15. Zhang W, Fraiture M, Kolb D, Löffelhardt B, Desaki Y, et al. (2013) Arabidopsis receptor-like protein30 and receptor-like kinase suppressor of BIR1-1/EVERSHED mediate innate immunity to necrotrophic fungi. Plant Cell 25: 4227–4241.
16. Clarke CR, Chinchilla D, Hind SR, Taguchi F, Miki R, et al. (2013) Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol 200: 847–860.
17. Furukawa T, Inagaki H, Takai R, Hirai H, Che FS, (2014) Two Distinct EF-Tu Epitopes Induce Immune Responses in Rice and Arabidopsis. Mol Plant Microbe Interact 27: 113–124.
18. Bauer Z, Gomez-Gomez L, Boller T, Felix G, (2001) Sensitivity of different ecotypes and mutants of Arabidopsis thaliana toward the bacterial elicitor flagellin correlates with the presence of receptor-binding sites. J Biol Chem 276: 45669–45676.
19. Böhm H, Albert I, Fan L, Reinhard A, Nürnberger T, (2014) Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol 20: 47–54.
20. Thomma BP, Nürnberger T, Joosten MH, (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4–15.
21. Lorang J, Kidarsa T, Bradford CS, Gilbert B, Curtis M, et al. (2012) Tricking the guard: exploiting plant defense for disease susceptibility. Science 338: 659–662.
22. van't Slot KAE, Knogge W, (2002) A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Critical Reviews in Plant Sciences 21: 229–271.
23. Wolpert TJ, Dunkle LD, Ciuffetti LM, (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu Rev Phytopathol 40: 251–285.
24. Dong S, Kong G, Qutob D, Yu X, Tang J, et al. (2012) The NLP toxin family in Phytophthora sojae includes rapidly evolving groups that lack necrosis-inducing activity. Mol Plant Microbe Interact 25: 896–909.
25. Qutob D, Kemmerling B, Brunner F, Küfner I, Engelhardt S, et al. (2006) Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18: 3721–3744.
26. Oome S, Van den Ackerveken G, (2014) Comparative and functional analysis of the widely occurring family of nep1-like proteins. Mol Plant Microbe Interact 27: 1081–1094.
27. Gijzen M, Nürnberger T, (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67: 1800–1807.
28. Zaparoli G, Barsottini MR, de Oliveira JF, Dyszy F, Teixeira PJ, et al. (2011) The crystal structure of necrosis- and ethylene-inducing protein 2 from the causal agent of cacao's Witches' Broom disease reveals key elements for its activity. Biochemistry 50: 9901–9910.
29. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228–232.
30. Matzinger P, (2007) Friendly and dangerous signals: is the tissue in control? Nat Immunol 8: 11–13.
31. Motteram J, Küfner I, Deller S, Brunner F, Hammond-Kosack KE, et al. (2009) Molecular characterization and functional analysis of MgNLP, the sole NPP1 domain-containing protein, from the fungal wheat leaf pathogen Mycosphaerella graminicola. Mol Plant Microbe Interact 22: 790–799.
32. Santhanam P, van Esse HP, Albert I, Faino L, Nürnberger T, et al. (2013) Evidence for functional diversification within a fungal NEP1-like protein family. Mol Plant Microbe Interact 26: 278–286.
33. Cabral A, Oome S, Sander N, Küfner I, Nürnberger T, et al. (2012) Nontoxic Nep1-like proteins of the downy mildew pathogen Hyaloperonospora arabidopsidis: repression of necrosis-inducing activity by a surface-exposed region. Mol Plant Microbe Interact 25: 697–708.
34. Judelson HS, Ah-Fong AM, Aux G, Avrova AO, Bruce C, et al. (2008) Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome. Mol Plant Microbe Interact 21: 433–447.
35. Qutob D, Kamoun S, Gijzen M, (2002) Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J 32: 361–373.
36. Wirthmueller L, Maqbool A, Banfield MJ, (2013) On the front line: structural insights into plant-pathogen interactions. Nat Rev Microbiol 11: 761–776.
37. Fellbrich G, Romanski A, Varet A, Blume B, Brunner F, et al. (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J 32: 375–390.
38. Mueller K, Chinchilla D, Albert M, Jehle AK, Kalbacher H, 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.
39. Nürnberger T, Brunner F, Kemmerling B, Piater L, (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249–266.
40. Felix G, Duran JD, Volko S, Boller T, (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265–276.
41. Gomez-Gomez L, 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.
42. Pirhonen M, Saarilahti HT, Karlsson MB, Palva ET, (1991) Identification of pathogenicity determinants of Erwinia carotovora subsp. carotovora by transposon mutagenesis. Mol Plant-Microbe Interact 4: 276–283.
43. Gust AA, Biswas R, Lenz HD, Rauhut T, Ranf S, et al. (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282: 32338–32348.
44. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25: 402–408.