Functionally Redundant RXLR Effectors from Act at Different Steps to Suppress Early flg22-Triggered Immunity


Phytophthora species are among the most devastating crop pathogens worldwide. P. infestans is a pathogen of tomato and potato plants. The genome of P. infestans has been sequenced, revealing the presence of a large number of host-targeting RXLR effector proteins that are thought to manipulate cellular activities to the benefit of the pathogen. One step toward disease management comprises understanding the molecular basis of host susceptibility. In this paper, we used a protoplast-based system to analyze a subset of P. infestans RXLR (PiRXLR) effectors that interfere with plant immunity initiated by the recognition of microbial patterns (MAMP-triggered immunity - MTI). We identified PiRXLR effectors that suppress different stages early in the signaling cascade leading to MTI in tomato. By conducting a comparative functional analysis, we found that some of these effectors attenuate early MTI signaling in Arabidopsis, a plant that is not colonized by P. infestans. The PiRXLR effectors localize to different sub-cellular compartments, consistent with their ability to suppress different steps of the MTI signaling pathway. We conclude that the effector complement of P. infestans contains functional redundancy in the context of suppressing early signal transduction and gene activation associated with plant immunity.


Vyšlo v časopise: Functionally Redundant RXLR Effectors from Act at Different Steps to Suppress Early flg22-Triggered Immunity. PLoS Pathog 10(4): e32767. doi:10.1371/journal.ppat.1004057
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.ppat.1004057

Souhrn

Phytophthora species are among the most devastating crop pathogens worldwide. P. infestans is a pathogen of tomato and potato plants. The genome of P. infestans has been sequenced, revealing the presence of a large number of host-targeting RXLR effector proteins that are thought to manipulate cellular activities to the benefit of the pathogen. One step toward disease management comprises understanding the molecular basis of host susceptibility. In this paper, we used a protoplast-based system to analyze a subset of P. infestans RXLR (PiRXLR) effectors that interfere with plant immunity initiated by the recognition of microbial patterns (MAMP-triggered immunity - MTI). We identified PiRXLR effectors that suppress different stages early in the signaling cascade leading to MTI in tomato. By conducting a comparative functional analysis, we found that some of these effectors attenuate early MTI signaling in Arabidopsis, a plant that is not colonized by P. infestans. The PiRXLR effectors localize to different sub-cellular compartments, consistent with their ability to suppress different steps of the MTI signaling pathway. We conclude that the effector complement of P. infestans contains functional redundancy in the context of suppressing early signal transduction and gene activation associated with plant immunity.


Zdroje

1. AkiraS, UematsuS, TakeuchiO (2006) Pathogen recognition and innate immunity. Cell 124: 783–801.

2. ChisholmST, CoakerG, DayB, StaskawiczBJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803–814.

3. 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.

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

5. NurnbergerT, BrunnerF, KemmerlingB, PiaterL (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198: 249–266.

6. ZipfelC (2008) Pattern-recognition receptors in plant innate immunity. Curr Opin Immunol 20: 10–16.

7. 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.

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

10. HannDR, RathjenJP (2007) Early events in the pathogenicity of Pseudomonas syringae on Nicotiana benthamiana. Plant J 49: 607–618.

11. PeckSC, NuhseTS, HessD, IglesiasA, MeinsF, et al. (2001) Directed proteomics identifies a plant-specific protein rapidly phosphorylated in response to bacterial and fungal elicitors. Plant Cell 13: 1467–1475.

12. TaguchiF, ShimizuR, InagakiY, ToyodaK, ShiraishiT, et al. (2003) Post-translational modification of flagellin determines the specificity of HR induction. Plant Cell Physiol 44: 342–349.

13. 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.

14. ZhangWG, 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.

15. 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.

16. 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.

17. DeslandesL, RivasS (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 17: 644–655.

18. FengF, ZhouJM (2012) Plant-bacterial pathogen interactions mediated by type III effectors. Curr Opin Plant Biol 15: 469–476.

19. GohreV, RobatzekS (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annu Rev Phytopathol 46: 189–215.

20. ZhangJ, ShaoF, CuiH, ChenLJ, LiHT, et al. (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-Induced immunity in plants. Cell Host Microbe 1: 175–185.

21. WangYJ, LiJF, HouSG, WangXW, LiYA, et al. (2010) A Pseudomonas syringae ADP-Ribosyltransferase Inhibits Arabidopsis Mitogen-Activated Protein Kinase Kinases. Plant Cell 22: 2033–2044.

22. GohreV, SpallekT, HawekerH, MersmannS, MentzelT, et al. (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr Biol 18: 1824–1832.

23. ShanL, HeP, LiJ, HeeseA, PeckSC, et al. (2008) Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4: 17–27.

24. XiangT, ZongN, ZouY, WuY, ZhangJ, et al. (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr Biol 18: 74–80.

25. CanonneJ, MarinoD, JauneauA, PouzetC, BriereC, et al. (2011) The Xanthomonas Type III Effector XopD Targets the Arabidopsis Transcription Factor MYB30 to Suppress Plant Defense. Plant Cell 23: 3498–3511.

26. KimJG, TaylorKW, HotsonA, KeeganM, SchmelzEA, et al. (2008) XopD SUMO protease affects host transcription, promotes pathogen growth, and delays symptom development in Xanthomonas-infected tomato leaves. Plant Cell 20: 1915–1929.

27. JudelsonHS (2007) Genomics of the plant pathogenic oomycete Phytophthora: insights into biology and evolution. Adv Genet 57: 97–141.

28. HaasBJ, KamounS, ZodyMC, JiangRHY, HandsakerRE, et al. (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461: 393–398.

29. McDowellJM, BaxterL, TripathyS, IshaqueN, BootN, et al. (2010) Signatures of Adaptation to Obligate Biotrophy in the Hyaloperonospora arabidopsidis Genome. Science 330: 1549–1551.

30. TylerBM, TripathyS, ZhangX, DehalP, JiangRH, et al. (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313: 1261–1266.

31. HeinI, GilroyEM, ArmstrongMR, BirchPRJ (2009) The zig-zag-zig in oomycete-plant interactions. Mol Plant Pathol 10: 547–562.

32. WhissonSC, BoevinkPC, MolelekiL, AvrovaAO, MoralesJG, et al. (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450: 115–118.

33. AllenRL, Bittner-EddyPD, Grenville-BriggsLJ, MeitzJC, RehmanyAP, et al. (2004) Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306: 1957–1960.

34. ArmstrongMR, WhissonSC, PritchardL, BosJI, VenterE, et al. (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Natl Acad Sci U S A 102: 7766–7771.

35. BosJI, KannegantiTD, YoungC, CakirC, HuitemaE, et al. (2006) The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 48: 165–176.

36. BosJIB, ArmstrongMR, GilroyEM, BoevinkPC, HeinI, et al. (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci U S A 107: 9909–9914.

37. BosJIB, Chaparro-GarciaA, Quesada-OcampoLM, GardenerBBM, KamounS (2009) Distinct Amino Acids of the Phytophthora infestans Effector AVR3a Condition Activation of R3a Hypersensitivity and Suppression of Cell Death. Mol Plant-Microbe Interact 22: 269–281.

38. BozkurtTO, SchornackS, WinJ, ShindoT, IlyasM, et al. (2011) Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc Natl Acad Sci U S A 108: 20832–20837.

39. DongSM, YinWX, KongGH, YangXY, QutobD, et al. (2011) Phytophthora sojae Avirulence Effector Avr3b is a Secreted NADH and ADP-ribose Pyrophosphorylase that Modulates Plant Immunity. PLoS Pathog 7: e1002353.

40. DouD, KaleSD, WangX, ChenY, WangQ, et al. (2008) Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20: 1118–1133.

41. DouD, KaleSD, WangX, JiangRH, BruceNA, et al. (2008) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20: 1930–1947.

42. GilroyEM, TaylorRM, HeinI, BoevinkP, SadanandomA, et al. (2011) CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytol 190: 653–666.

43. McLellanH, BoevinkPC, ArmstrongMR, PritchardL, GomezS, et al. (2013) An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. PLoS Pathog 9: e1003670.

44. OhSK, YoungC, LeeM, OlivaR, BozkurtTO, et al. (2009) In Planta Expression Screens of Phytophthora infestans RXLR Effectors Reveal Diverse Phenotypes, Including Activation of the Solanum bulbocastanum Disease Resistance Protein Rpi-blb2. Plant Cell 21: 2928–2947.

45. RehmanyAP, GordonA, RoseLE, AllenRL, ArmstrongMR, et al. (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17: 1839–1850.

46. ShanW, CaoM, LeungD, TylerBM (2004) The Avr1b locus of Phytophthora sojae encodes an elicitor and a regulator required for avirulence on soybean plants carrying resistance gene Rps1b. Mol Plant Microbe Interact 17: 394–403.

47. SohnKH, LeiR, NemriA, JonesJD (2007) The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19: 4077–4090.

48. HeP, ShanL, LinNC, MartinGB, KemmerlingB, et al. (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125: 563–575.

49. LiXY, LinHQ, ZhangWG, ZouY, ZhangJ, et al. (2005) Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci U S A 102: 12990–12995.

50. RobatzekS, BittelP, ChinchillaD, KochnerP, FelixG, et al. (2007) Molecular identification and characterization of the tomato flagellin receptor LeFLS2, an orthologue of Arabidopsis FLS2 exhibiting characteristically different perception specificities. Plant Mol Biol 64: 539–547.

51. PedleyKF, MartinGB (2004) Identification of MAPKs and their possible MAPK kinase activators involved in the Pto-mediated defense response of tomato. J Biol Chem 279: 49229–49235.

52. NguyenHP, ChakravarthyS, VelasquezAC, McLaneHL, ZengLR, et al. (2010) Methods to Study PAMP-Triggered Immunity Using Tomato and Nicotiana benthamiana. Mol Plant Microbe Interact 23: 991–999.

53. ShanLB, TharaVK, MartinGB, ZhouJM, TangXY (2000) The pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 12: 2323–2337.

54. van PoppelPM, GuoJ, van de VondervoortPJ, JungMW, BirchPR, et al. (2008) The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector. Mol Plant Microbe Interact 21: 1460–1470.

55. ChampouretN, BouwmeesterK, RietmanH, van der LeeT, MaliepaardC, et al. (2009) Phytophthora infestans Isolates Lacking Class I ipiO Variants Are Virulent on Rpi-blb1 Potato. Mol Plant Microbe Interact 22: 1535–1545.

56. VleeshouwersVG, RietmanH, KrenekP, ChampouretN, YoungC, et al. (2008) Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora infestans avirulence genes. PLoS one 3: e2875.

57. CookeDEL, CanoLM, RaffaeleS, BainRA, CookeLR, et al. (2012) Genome Analyses of an Aggressive and Invasive Lineage of the Irish Potato Famine Pathogen. PLoS Pathog 8: e1002940.

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

59. PitzschkeA, SchikoraA, HirtH (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12: 421–426.

60. del PozoO, PedleyKF, MartinGB (2004) MAPKKK alpha is a positive regulator of cell death associated with both plant immunity and disease. Embo J 23: 3072–3082.

61. Melech-BonfilS, SessaG (2010) Tomato MAPKKK epsilon is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J 64: 379–391.

62. TakahashiY, NasirKH, ItoA, KanzakiH, MatsumuraH, et al. (2007) A high-throughput screen of cell-death-inducing factors in Nicotiana benthamiana identifies a novel MAPKK that mediates INF1-induced cell death signaling and non-host resistance to Pseudomonas cichorii. Plant J 49: 1030–1040.

63. Schulze-LefertP, PanstrugaR (2011) A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci 16: 117–125.

64. FabroG, SteinbrennerJ, CoatesM, IshaqueN, BaxterL, et al. (2011) Multiple Candidate Effectors from the Oomycete Pathogen Hyaloperonospora arabidopsidis Suppress Host Plant Immunity. PLoS Pathog 7: e1002348.

65. MukhtarMS, CarvunisAR, DrezeM, EppleP, SteinbrennerJ, et al. (2011) Independently Evolved Virulence Effectors Converge onto Hubs in a Plant Immune System Network. Science 333: 596–601.

66. XuX, PanSK, ChengSF, ZhangB, MuDS, et al. (2011) Genome sequence and analysis of the tuber crop potato. Nature 475: 189–194.

67. SatoS, TabataS, HirakawaH, AsamizuE, ShirasawaK, et al. (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485: 635–641.

68. BombarelyA, RosliHG, VrebalovJ, MoffettP, MuellerL, et al. (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25: 1523–1530.

69. KvitkoBH, ParkDH, VelasquezAC, WeiCF, RussellAB, et al. (2009) Deletions in the Repertoire of Pseudomonas syringae pv. tomato DC3000 Type III Secretion Effector Genes Reveal Functional Overlap among Effectors. PLoS Pathog 5: e1000388.

70. YooSD, ChoYH, SheenJ (2007) Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat Protoc 2: 1565–1572.

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Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

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