The Secreted Peptide PIP1 Amplifies Immunity through Receptor-Like Kinase 7

English version České info

Both animals and plants have evolved mechanisms to trigger innate immunity through perception of exogenous and endogenous molecules. In the model plant Arabidopsis thaliana, endogenous molecules such as the peptide elicitor PEP1 activate the immune response by means of cell surface-located receptors. Here we describe a new gene family in A. thaliana named prePIPs, whose members encode secreted peptide precursors, and show that one of its members, prePIP1, is secreted into extracellular space and cleaved at the C-terminus. Exogenous application of PIP1, the synthetic 13-amino acid peptide corresponding to the conserved C-terminal region of prePIP1, triggered immune responses and led to enhanced pathogen resistance in A. thaliana. We further provide evidence showing that PIP1 signals via the receptor-like kinase 7 (RLK7) and employs both shared and distinct components with the PEP1 signaling pathway. Both PIP1 and PEP1 cooperatively amplify the immune response triggered by flg22, the active epitope of bacterial flagellin.

Vyšlo v časopise: The Secreted Peptide PIP1 Amplifies Immunity through Receptor-Like Kinase 7. PLoS Pathog 10(9): e32767. doi:10.1371/journal.ppat.1004331
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004331

Souhrn

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. HuffakerA, PearceG, RyanCA (2006) An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci USA 103: 10098–10103.

4. SanabriaN, GoringD, NurnbergerT, DuberyI (2008) Self/nonself perception and recognition mechanisms in plants: a comparison of self-incompatibility and innate immunity. New Phytol 178: 503–514.

5. ShiuSH, BleeckerAB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98: 10763–10768.

6. DunningFM, SunW, JansenKL, HelftL, BentAF (2007) Identification and mutational analysis of Arabidopsis FLS2 leucine-rich repeat domain residues that contribute to flagellin perception. Plant Cell 19: 3297–3313.

7. ChinchillaD, ZipfelC, RobatzekS, KemmerlingB, NurnbergerT, et al. (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448: 497–500.

8. HeeseA, HannDR, Gimenez-IbanezS, JonesAM, HeK, et al. (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104: 12217–12222.

9. LuD, WuS, GaoX, ZhangY, ShanL, et al. (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107: 496–501.

10. ZhangJ, LiW, XiangT, LiuZ, LalukK, et al. (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe 7: 290–301.

11. SegonzacC, ZipfelC (2011) Activation of plant pattern-recognition receptors by bacteria. Curr Opin Microbiol 14: 54–61.

12. DubiellaU, SeyboldH, DurianG, KomanderE, LassigR, et al. (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci USA 110: 8744–8749.

13. BoudsocqM, WillmannMR, McCormackM, LeeH, ShanL, et al. (2010) Differential innate immune signalling via Ca(2+) sensor protein kinases. Nature 464: 418–422.

14. AsaiT, TenaG, PlotnikovaJ, WillmannMR, ChiuWL, et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977–983.

15. YamaguchiY, PearceG, RyanCA (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 USA 103: 10104–10109.

16. YamaguchiY, HuffakerA, BryanAC, TaxFE, RyanCA (2010) PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell 22: 508–522.

17. LiuZ, WuY, YangF, ZhangY, ChenS, et al. (2013) BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc Natl Acad Sci USA 110: 6205–6210.

18. TintorN, RossA, KaneharaK, YamadaK, FanL, et al. (2013) Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc Natl Acad Sci USA 110: 6211–6216.

19. RyanCA, HuffakerA, YamaguchiY (2007) New insights into innate immunity in Arabidopsis. Cell Microbiol 9: 1902–1908.

20. MatsubayashiY (2011) Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol 52: 5–13.

21. MurphyE, SmithS, De SmetI (2012) Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. Plant Cell 24: 3198–3217.

22. HarutaM, SabatG, SteckerK, MinkoffBB, SussmanMR (2014) A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343: 408–411.

23. LeeH, ChahOK, SheenJ (2011) Stem-cell-triggered immunity through CLV3p-FLS2 signalling. Nature 473: 376–379.

24. IgarashiD, TsudaK, KatagiriF (2012) The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J 71: 194–204.

25. MosherS, SeyboldH, RodriguezP, StahlM, DaviesKA, et al. (2013) The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J 73: 469–482.

26. LeaseKA, WalkerJC (2006) The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol 142: 831–838.

27. 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.

28. BendtsenJD, NielsenH, von HeijneG, BrunakS (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783–795.

29. StuhrwohldtN, DahlkeRI, SteffensB, JohnsonA, SauterM (2011) Phytosulfokine-alpha controls hypocotyl length and cell expansion in Arabidopsis thaliana through phytosulfokine receptor 1. PloS One 6: e21054.

30. AmanoY, TsubouchiH, ShinoharaH, OgawaM, MatsubayashiY (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci USA 104: 18333–18338.

31. ButenkoMA, PattersonSE, GriniPE, StenvikGE, AmundsenSS, et al. (2003) Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15: 2296–2307.

32. ItoY, NakanomyoI, MotoseH, IwamotoK, SawaS, et al. (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313: 842–845.

33. KondoT, SawaS, KinoshitaA, MizunoS, KakimotoT, et al. (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313: 845–848.

34. OhyamaK, OgawaM, MatsubayashiY (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J 55: 152–160.

35. StenvikGE, TandstadNM, GuoY, ShiCL, KristiansenW, et al. (2008) The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20: 1805–1817.

36. MilletYA, DannaCH, ClayNK, SongnuanW, SimonMD, et al. (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22: 973–990.

37. ClayNK, AdioAM, DenouxC, JanderG, AusubelFM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323: 95–101.

38. OgawaM, ShinoharaH, SakagamiY, MatsubayashiY (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294.

39. PostelS, KufnerI, BeuterC, MazzottaS, SchwedtA, et al. (2010) The multifunctional leucine-rich repeat receptor kinase BAK1 is implicated in Arabidopsis development and immunity. Eur J Cell Biol 89: 169–174.

40. LiebrandTW, van den BergGC, ZhangZ, SmitP, CordewenerJH, et al. (2013) Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci USA 110: 10010–10015.

41. ZhangW, FraitureM, KolbD, LoffelhardtB, 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.

42. ZhangL, KarsI, EssenstamB, LiebrandTW, WagemakersL, et al. (2013) Fungal endopolygalacturonases are recognized as MAMPs by the Arabidopsis Receptor-Like Protein RBPG1. Plant Physiol 164: 352–364.

43. RouxM, SchwessingerB, AlbrechtC, ChinchillaD, JonesA, et al. (2011) The Arabidopsis leucine-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.

44. KunzeG, ZipfelC, RobatzekS, NiehausK, BollerT, et al. (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16: 3496–3507.

45. JehleAK, LipschisM, AlbertM, Fallahzadeh-MamaghaniV, FurstU, et al. (2013) The receptor-like protein ReMAX of Arabidopsis detects the microbe-associated molecular pattern eMax from Xanthomonas. Plant Cell 25: 2330–2340.

46. SrivastavaR, LiuJX, HowellSH (2008) Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J 56: 219–227.

47. 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.

48. DannaCH, ZhangXC, KhatriA, BentAF, RonaldPC, et al. (2012) FLS2-mediated responses to Ax21-derived peptides: response to the Mueller et al. commentary. Plant Cell 24: 3174–3176.

49. BollerT, HeSY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742–744.

50. RossA, YamadaK, HirumaK, Yamashita-YamadaM, LuX, et al. (2014) The Arabidopsis PEPR pathway couples local and systemic plant immunity. EMBO J 33: 62–75.

51. YamaguchiY, HuffakerA (2011) Endogenous peptide elicitors in higher plants. Curr Opin Plant Biol 14: 351–357.

52. MedzhitovR (2010) Inflammation 2010: new adventures of an old flame. Cell 140: 771–776.

53. HuffakerA, RyanCA (2007) Endogenous peptide defense signals in Arabidopsis differentially amplify signaling for the innate immune response. Proc Natl Acad Sci USA 104: 10732–10736.

54. BelkhadirY, JaillaisY, EppleP, Balsemao-PiresE, DanglJL, et al. (2012) Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci USA 109: 297–302.

55. PitorreD, LlauroC, JobetE, GuilleminotJ, BrizardJP, et al. (2010) RLK7, a leucine-rich repeat receptor-like kinase, is required for proper germination speed and tolerance to oxidative stress in Arabidopsis thaliana. Planta 232: 1339–1353.

56. VickersCE, SchenkPM, LiD, MullineauxPM, GresshoffPM (2007) pGFPGUSPlus, a new binary vector for gene expression studies and optimising transformation systems in plants. Biotech Lett 29: 1793–1796.

57. WanJ, TanakaK, ZhangXC, SonGH, BrechenmacherL, et al. (2012) LYK4, a lysin motif receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol 160: 396–406.

58. NiJ, GuoY, JinH, HartsellJ, ClarkSE (2011) Characterization of a CLE processing activity. Plant Mol Biol 75: 67–75.

59. WangY, LiJ, HouS, WangX, LiY, et al. (2010) A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22: 2033–2044.

60. TuszynskiGP, KnightLC, KorneckiE, SrivastavaS (1983) Labeling of platelet surface proteins with 125I by the iodogen method. Anal Biochem 130: 166–170.

61. ZipfelC, RobatzekS, NavarroL, OakeleyEJ, JonesJD, et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764–767.

62. Lopez-BergesMS, CapillaJ, TurraD, SchaffererL, MatthijsS, et al. (2012) HapX-mediated iron homeostasis is essential for rhizosphere competence and virulence of the soilborne pathogen Fusarium oxysporum. Plant Cell 24: 3805–3822.

63. Di PietroA, Garcia-MacEiraFI, MegleczE, RonceroMI (2001) A MAP kinase of the vascular wilt fungus Fusarium oxysporum is essential for root penetration and pathogenesis. Mol Microbiol 39: 1140–1152.