#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

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


Eukaryotic host immunity to microbial infection requires recognition systems sensing the presence of potential invaders. Microbial surface structures (patterns) or host breakdown products generated during microbial attack serve as ligands for host immune receptors (pattern recognition receptors) mediating activation of immune responses. Microbial pathogens employ, however, host-targeting effector proteins to establish infection, and the efficiencies of microbial pathogen attack and host defense mechanisms determine the outcome of microbe-host interactions. Necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLPs) from bacteria, oomycetes and fungi are cytotoxic virulence factors (effectors) that trigger plant immunity through toxin-induced host cell damage. Here we show that, in addition, numerous NLPs harbor a characteristic 20-mer sequence motif (nlp20) that is recognized by Brassicacae plant species and perception of which confers immunity to infection by bacterial, oomycete and fungal pathogens. Our findings provide evidence that cytotoxic NLPs are virulence factors that trigger plant immunity by pattern recognition and by inflicting host cell damage. We further conclude that NLPs from prokaryotic and eukaryotic microorganisms and from three organismal kingdoms evoke plant defense. Such an exceptionally wide taxonomic distribution of microbe-derived triggers of immunity has neither been reported before from metazoans nor from plants.


Vyšlo v časopise: A Conserved Peptide Pattern from a Widespread Microbial Virulence Factor Triggers Pattern-Induced Immunity in. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004491
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004491

Souhrn

Eukaryotic host immunity to microbial infection requires recognition systems sensing the presence of potential invaders. Microbial surface structures (patterns) or host breakdown products generated during microbial attack serve as ligands for host immune receptors (pattern recognition receptors) mediating activation of immune responses. Microbial pathogens employ, however, host-targeting effector proteins to establish infection, and the efficiencies of microbial pathogen attack and host defense mechanisms determine the outcome of microbe-host interactions. Necrosis and ethylene-inducing peptide 1 (Nep1)-like proteins (NLPs) from bacteria, oomycetes and fungi are cytotoxic virulence factors (effectors) that trigger plant immunity through toxin-induced host cell damage. Here we show that, in addition, numerous NLPs harbor a characteristic 20-mer sequence motif (nlp20) that is recognized by Brassicacae plant species and perception of which confers immunity to infection by bacterial, oomycete and fungal pathogens. Our findings provide evidence that cytotoxic NLPs are virulence factors that trigger plant immunity by pattern recognition and by inflicting host cell damage. We further conclude that NLPs from prokaryotic and eukaryotic microorganisms and from three organismal kingdoms evoke plant defense. Such an exceptionally wide taxonomic distribution of microbe-derived triggers of immunity has neither been reported before from metazoans nor from plants.


Zdroje

1. JonesJD, DanglJL (2006) The plant immune system. Nature 444: 323–329.

2. BollerT, FelixG (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. DoddsPN, RathjenJP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539–548.

4. OttmannC, LuberackiB, KüfnerI, KochW, BrunnerF, et al. (2009) A common toxin fold mediates microbial attack and plant defense. Proc Natl Acad Sci USA 106: 10359–10364.

5. DouD, ZhouJM (2012) Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12: 484–495.

6. SpoelSH, DongX (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. ChinchillaD, BauerZ, RegenassM, BollerT, FelixG (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18: 465–476.

9. NürnbergerT, NennstielD, JabsT, SacksWR, HahlbrockK, et al. (1994) High affinity binding of a fungal oligopeptide elicitor to parsley plasma membranes triggers multiple defense responses. Cell 78: 449–460.

10. BrunnerF, NürnbergerT (2012) Identification of immunogenic microbial patterns takes the fast lane. Proc Natl Acad Sci USA 109: 4029–4030.

11. MonaghanJ, ZipfelC (2012) Plant pattern recognition receptor complexes at the plasma membrane. Curr Opin Plant Biol 15: 349–357.

12. FliegmannJ, MithöferA, WannerG, EbelJ (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. ZipfelC, KunzeG, ChinchillaD, CaniardA, JonesJD, et al. (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749–760.

14. JehleAK, LipschisM, AlbertM, Fallahzadeh-MamaghaniV, FürstU, 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. ZhangW, FraitureM, KolbD, LöffelhardtB, DesakiY, 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. ClarkeCR, ChinchillaD, HindSR, TaguchiF, MikiR, 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. FurukawaT, InagakiH, TakaiR, HiraiH, CheFS (2014) Two Distinct EF-Tu Epitopes Induce Immune Responses in Rice and Arabidopsis. Mol Plant Microbe Interact 27: 113–124.

18. BauerZ, Gomez-GomezL, BollerT, FelixG (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. BöhmH, AlbertI, FanL, ReinhardA, NürnbergerT (2014) Immune receptor complexes at the plant cell surface. Curr Opin Plant Biol 20: 47–54.

20. ThommaBP, NürnbergerT, JoostenMH (2011) Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23: 4–15.

21. LorangJ, KidarsaT, BradfordCS, GilbertB, CurtisM, et al. (2012) Tricking the guard: exploiting plant defense for disease susceptibility. Science 338: 659–662.

22. van't SlotKAE, KnoggeW (2002) A dual role for microbial pathogen-derived effector proteins in plant disease and resistance. Critical Reviews in Plant Sciences 21: 229–271.

23. WolpertTJ, DunkleLD, CiuffettiLM (2002) Host-selective toxins and avirulence determinants: what's in a name? Annu Rev Phytopathol 40: 251–285.

24. DongS, KongG, QutobD, YuX, TangJ, 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. QutobD, KemmerlingB, BrunnerF, KüfnerI, EngelhardtS, et al. (2006) Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18: 3721–3744.

26. OomeS, Van den AckervekenG (2014) Comparative and functional analysis of the widely occurring family of nep1-like proteins. Mol Plant Microbe Interact 27: 1081–1094.

27. GijzenM, NürnbergerT (2006) Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67: 1800–1807.

28. ZaparoliG, BarsottiniMR, de OliveiraJF, DyszyF, TeixeiraPJ, 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. MariathasanS, WeissDS, NewtonK, McBrideJ, O'RourkeK, et al. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440: 228–232.

30. MatzingerP (2007) Friendly and dangerous signals: is the tissue in control? Nat Immunol 8: 11–13.

31. MotteramJ, KüfnerI, DellerS, BrunnerF, Hammond-KosackKE, 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. SanthanamP, van EsseHP, AlbertI, FainoL, NürnbergerT, et al. (2013) Evidence for functional diversification within a fungal NEP1-like protein family. Mol Plant Microbe Interact 26: 278–286.

33. CabralA, OomeS, SanderN, KüfnerI, NürnbergerT, 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. JudelsonHS, Ah-FongAM, AuxG, AvrovaAO, BruceC, 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. QutobD, KamounS, GijzenM (2002) Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J 32: 361–373.

36. WirthmuellerL, MaqboolA, BanfieldMJ (2013) On the front line: structural insights into plant-pathogen interactions. Nat Rev Microbiol 11: 761–776.

37. FellbrichG, RomanskiA, VaretA, BlumeB, BrunnerF, et al. (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J 32: 375–390.

38. MuellerK, ChinchillaD, AlbertM, JehleAK, KalbacherH, 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. NürnbergerT, BrunnerF, KemmerlingB, PiaterL (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249–266.

40. FelixG, DuranJD, VolkoS, BollerT (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18: 265–276.

41. Gomez-GomezL, BollerT (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5: 1003–1011.

42. PirhonenM, SaarilahtiHT, KarlssonMB, PalvaET (1991) Identification of pathogenicity determinants of Erwinia carotovora subsp. carotovora by transposon mutagenesis. Mol Plant-Microbe Interact 4: 276–283.

43. GustAA, BiswasR, LenzHD, RauhutT, RanfS, et al. (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282: 32338–32348.

44. LivakKJ, SchmittgenTD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25: 402–408.

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#