#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Avirulence Effector Avr3b is a Secreted NADH and ADP-ribose Pyrophosphorylase that Modulates Plant Immunity


Plants have evolved pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) to protect themselves from infection by diverse pathogens. Avirulence (Avr) effectors that trigger plant ETI as a result of recognition by plant resistance (R) gene products have been identified in many plant pathogenic oomycetes and fungi. However, the virulence functions of oomycete and fungal Avr effectors remain largely unknown. Here, we combined bioinformatics and genetics to identify Avr3b, a new Avr gene from Phytophthora sojae, an oomycete pathogen that causes soybean root rot. Avr3b encodes a secreted protein with the RXLR host-targeting motif and C-terminal W and Nudix hydrolase motifs. Some isolates of P. sojae evade perception by the soybean R gene Rps3b through sequence mutation in Avr3b and lowered transcript accumulation. Transient expression of Avr3b in Nicotiana benthamiana increased susceptibility to P. capsici and P. parasitica, with significantly reduced accumulation of reactive oxygen species (ROS) around invasion sites. Biochemical assays confirmed that Avr3b is an ADP-ribose/NADH pyrophosphorylase, as predicted from the Nudix motif. Deletion of the Nudix motif of Avr3b abolished enzyme activity. Mutation of key residues in Nudix motif significantly impaired Avr3b virulence function but not the avirulence activity. Some Nudix hydrolases act as negative regulators of plant immunity, and thus Avr3b might be delivered into host cells as a Nudix hydrolase to impair host immunity. Avr3b homologues are present in several sequenced Phytophthora genomes, suggesting that Phytophthora pathogens might share similar strategies to suppress plant immunity.


Vyšlo v časopise: Avirulence Effector Avr3b is a Secreted NADH and ADP-ribose Pyrophosphorylase that Modulates Plant Immunity. PLoS Pathog 7(11): e32767. doi:10.1371/journal.ppat.1002353
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002353

Souhrn

Plants have evolved pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) and effector-triggered immunity (ETI) to protect themselves from infection by diverse pathogens. Avirulence (Avr) effectors that trigger plant ETI as a result of recognition by plant resistance (R) gene products have been identified in many plant pathogenic oomycetes and fungi. However, the virulence functions of oomycete and fungal Avr effectors remain largely unknown. Here, we combined bioinformatics and genetics to identify Avr3b, a new Avr gene from Phytophthora sojae, an oomycete pathogen that causes soybean root rot. Avr3b encodes a secreted protein with the RXLR host-targeting motif and C-terminal W and Nudix hydrolase motifs. Some isolates of P. sojae evade perception by the soybean R gene Rps3b through sequence mutation in Avr3b and lowered transcript accumulation. Transient expression of Avr3b in Nicotiana benthamiana increased susceptibility to P. capsici and P. parasitica, with significantly reduced accumulation of reactive oxygen species (ROS) around invasion sites. Biochemical assays confirmed that Avr3b is an ADP-ribose/NADH pyrophosphorylase, as predicted from the Nudix motif. Deletion of the Nudix motif of Avr3b abolished enzyme activity. Mutation of key residues in Nudix motif significantly impaired Avr3b virulence function but not the avirulence activity. Some Nudix hydrolases act as negative regulators of plant immunity, and thus Avr3b might be delivered into host cells as a Nudix hydrolase to impair host immunity. Avr3b homologues are present in several sequenced Phytophthora genomes, suggesting that Phytophthora pathogens might share similar strategies to suppress plant immunity.


Zdroje

1. JonesJDDanglJL 2006 The plant immune system. Nature 444 323 329

2. De WitPJMehrabiRVan den BurgHAStergiopoulosI 2009 Fungal effector proteins: past, present and future. Mol Plant Pathol 10 735 747

3. RehmanyAPGordonARoseLEAllenRLArmstrongMR 2005 Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell 17 1839 1850

4. BirchPRRehmanyAPPritchardLKamounSBeynonJL 2006 Trafficking arms: oomycete effectors enter host plant cells. Trends Microbiol 14 8 11

5. JiangRHYTripathySGoversFTylerBM 2008 RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving super-family with more than 700 members. Proc Natl Acad Sci U S A 105 4874 4879

6. TylerBMTripathySZhangXDehalPJiangRH 2006 Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313 1261 1266

7. WhissonSCBoevinkPCMolelekiLAvrovaAOMoralesJG 2007 A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450 115 118

8. DouDKaleSDWangX JiangRHBruceNA 2008 RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20 1930 1947

9. SchornackSvan DammeMBozkurtTOCanoLMSmokerM 2010 Ancient class of translocated oomycete effectors targets the host nucleus. Proc Natl Acad Sci U S A 107 17421 17426

10. KaleSDGuBCapellutoDGDouDFeldmanE 2010 External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142 284 295

11. OhSKYoungCLeeMOlivaRBozkurtTO 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

12. DongSQutobDTedman-JonesJKufluKWangY 2009 The Phytophthora sojae avirulence locus Avr3c encodes a multi-copy RXLR effector with sequence polymorphisms among pathogen strains. PLoS One 4 e5556

13. ShanWCaoMLeungDTylerBM 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

14. QutobDTedman-JonesJDongSKufluKPhamH 2009 Copy number variation and transcriptional polymorphisms of Phytophthora sojae RXLR effector genes Avr1a and Avr3a. PLoS One 4 e5066

15. DouDKaleSDLiuTTangQWangX 2010 Different domains of Phytophthora sojae effector Avr4/6 are recognized by soybean resistance genes Rps4 and Rps6. Mol Plant Microbe Interact 23 425 435

16. ArmstrongMRWhissonSCPritchardLBosJIVenterE 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

17. van PoppelPMGuoJvan de VondervoortPJJungMWBirchPR 2008 The Phytophthora infestans avirulence gene Avr4 encodes an RXLR-dEER effector. Mol Plant Microbe Interact 21 1460 1470

18. AllenRLBittner-EddyPDGrenville-BriggsLJMeitzJCRehmanyAP 2004 Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science 306 1957 1960

19. DongSYuDCuiLQutobDTedman-JonesJ 2011 Sequence Variants of the Phytophthora sojae RXLR Effector Avr3a/5 Are Differentially Recognized by Rps3a and Rps5 in Soybean. PLoS One 6 e20172

20. GilroyEMBreenSWhissonSCSquiresJHeinI 2011 Presence/absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants. New Phytol 191 763 776

21. BaileyKCevikVHoltonNByrne-RichardsonJSohnKH 2011 Molecular cloning of ATR5(Emoy2) from Hyaloperonospora arabidopsidis, an avirulence determinant that triggers RPP5-mediated defense in Arabidopsis. Mol Plant Microbe Interact 24 827 838

22. BaxterLTripathySIshaqueNBootNCabralA 2010 Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome. Science 330 1549 1551

23. HaasBJKamounSZodyMC JiangRHHandsakerRE 2009 Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461 393 398

24. van EsseHPVan't KloosterJWBoltonMDYadetaKAvan BaarlenP 2008 The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20 1948 1963

25. van EsseHPBoltonMDStergiopoulosIde WitPJThommaBP 2007 The chitin-binding Cladosporium fulvum effector protein Avr4 is a virulence factor. Mol Plant Microbe Interact 20 1092 1101

26. JiaYMcAdamsSABryanGTHersheyHPValentB 2000 Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19 4004 4014

27. BohnertHUFudalIDiohWTharreauDNotteghemJL 2004 A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell 16 2499 2513

28. CatanzaritiAMDoddsPNLawrenceGJAyliffeMAEllisJG 2006 Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18 243 256

29. HoutermanPMCornelissenBJRepM 2008 Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathog 4 e1000061

30. DouDKaleSDWangXChenYWangQ 2008 Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell 20 1118 1133

31. WangQHanCFerreiraAOYuXYeW 2011 Transcriptional Programming and Functional Interactions within the Phytophthora sojae RXLR Effector Repertoire. Plant Cell 23 2064 2086

32. SohnKHLeiRNemriA JonesJD 2007 The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19 4077 4090

33. BosJIArmstrongMRGilroyEMBoevinkPCHeinI 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

34. MayKJWhissonSCZwartRSSearleIRIrwinJA 2002 Inheritance and mapping of 11 avirulence genes in Phytophthora sojae. Fungal Genet Biol 37 1 12

35. YeWWangXTaoKLuYZhaoW 2011 Digital gene expression profiling of the Phytophthora sojae transcriptome. Mol Plant Microbe Interact

36. ForsterHTylerBMCoffeyMD 1994 Phytophthora sojae races have arisen by clonal evolution and by rare outcrosses. Mol Plant Microbe Interact 7 780 791

37. QutobDKamounSGijzenM 2002 Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. Plant J 32 361 373

38. BosJIKannegantiTDYoungCCakirCHuitemaE 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

39. MildvanASXiaZAzurmendiHFSaraswatVLeglerPM 2005 Structures and mechanisms of Nudix hydrolases. Arch Biochem Biophys 433 129 143

40. GeXLiGJWangSBZhuHZhuT 2007 AtNUDT7, a negative regulator of basal immunity in Arabidopsis, modulates two distinct defense response pathways and is involved in maintaining redox homeostasis. Plant Physiol 145 204 215

41. BosJIBArmstrongMWhissonSCTortoTOchwoM 2003 Intraspecific comparative genomics to identify avirulence genes from Phytophthora. New Phytologist 159 63 72

42. JiangRHTripathySGoversFTylerBM 2008 RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proc Natl Acad Sci U S A 105 4874 4879

43. RafiqiMGanPHRavensdaleMLawrenceGJEllisJG 2010 Internalization of flax rust avirulence proteins into flax and tobacco cells can occur in the absence of the pathogen. Plant Cell 22 2017 2032

44. KhangCHBerruyerRGiraldoMCKankanalaPParkSY 2010 Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell 22 1388 1403

45. TianMWinJSavoryEBurkhardtAHeldM 2011 454 Genome Sequencing of Pseudoperonospora cubensis Reveals Effector Proteins with a QXLR Translocation Motif. Mol Plant Microbe Interact 24 543 553

46. OlivaRWinJRaffaeleSBoutemyLBozkurtTO 2010 Recent developments in effector biology of filamentous plant pathogens. Cell Microbiol 12 1015

47. LevesqueCABrouwerHCanoLHamiltonJPHoltC 2010 Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol 11 R73

48. BessmanMJFrickDNO'HandleySF 1996 The MutT proteins or "Nudix" hydrolases, a family of versatile, widely distributed, "housecleaning" enzymes. J Biol Chem 271 25059 25062

49. KraszewskaE 2008 The plant Nudix hydrolase family. Acta Biochim Pol 55 663 671

50. OgawaTUedaYYoshimuraKShigeokaS 2005 Comprehensive analysis of cytosolic Nudix hydrolases in Arabidopsis thaliana. J Biol Chem 280 25277 25283

51. BartschMGobbatoEBednarekPDebeySSchultzeJL 2006 Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell 18 1038 1051

52. TamuraNMurataYMukaiharaT 2005 Isolation of Ralstonia solanacearum hrpB constitutive mutants and secretion analysis of hrpB-regulated gene products that share homology with known type III effectors and enzymes. Microbiology 151 2873 2884

53. IshikawaKOgawaTHirosueENakayamaYHaradaK 2009 Modulation of the poly(ADP-ribosyl)ation reaction via the Arabidopsis ADP-ribose/NADH pyrophosphohydrolase, AtNUDX7, is involved in the response to oxidative stress. Plant Physiol 151 741 754

54. JambunathanNPenagantiATangYMahalingamR 2010 Modulation of redox homeostasis under suboptimal conditions by Arabidopsis nudix hydrolase 7. BMC Plant Biol 10 173

55. OgawaTIshikawaKHaradaKFukusakiEYoshimuraK 2009 Overexpression of an ADP-ribose pyrophosphatase, AtNUDX2, confers enhanced tolerance to oxidative stress in Arabidopsis plants. Plant J 57 289 301

56. WinJKamounS 2008 Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Signal Behav 3 251 253

57. BirchPRBoevinkPCGilroyEMHeinIPritchardL 2008 Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Curr Opin Plant Biol 11 373 379

58. QutobDHraberPTSobralBWGijzenM 2000 Comparative analysis of expressed sequences in Phytophthora sojae. Plant Physiol 123 243 254

59. HuaCWangYZhengXDouDZhangZ 2008 A Phytophthora sojae G-protein alpha subunit is involved in chemotaxis to soybean isoflavones. Eukaryot Cell 7 2133 2140

60. ChenXShenGWangYZhengX 2007 Identification of Phytophthora sojae genes upregulated during the early stage of soybean infection. FEMS Microbiol Lett 269 280 288

61. Torto-AlaliboTATripathySSmithBMArredondoFDZhouL 2007 Expressed sequence tags from Phytophthora sojae reveal genes specific to development and infection. Mol Plant Microbe Interact 20 781 793

62. SchuhmacherTLemuthKHardimanTVacunGReussM 2010 Quantifying cytosolic messenger RNA concentrations in Escherichia coli using real-time polymerase chain reaction for a systems biology approach. Anal Biochem 398 212 217

63. DongSZhangZZhengXWangY 2008 Mammalian pro-apoptotic bax gene enhances tobacco resistance to pathogens. Plant Cell Rep 27 1559 1569

64. WhissonSCAvrovaAOPVANWJonesJT 2005 A method for double-stranded RNA-mediated transient gene silencing in Phytophthora infestans. Mol Plant Pathol 6 153 163

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 11
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

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#