-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
The Activation of Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
Phytophthora sojae, an oomycete pathogen that causes the Phytophthora root and stem rot disease of soybean, delivers variety of effectors into host cell to reprogram host immunity. Genome sequencing uncovers that P. sojae genome encode several hundreds of effector genes. However, the mode of action of most of the P. sojae effectors remains unknown. The investigation of effector-interacting proteins provides opportunities to better understand the pathogenesis mechanism of the pathogen and the defense mechanism of the host plants. Previously, we reported that P. sojae avirulence effector Avr3b modulates plant immunity through its Nudix hydrolase activity. Interestingly, the enzymatic activity is required for its virulence but not required for recognition by resistant gene. In this study, we identified soybean cyclophilin protein GmCYP1 as an Avr3b interactor. The enzymatic activity of GmCYP1 is required for the maturation Avr3b, which is directly related to both virulence and avirulence functions of Avr3b. This work provides a novel insight into how Phytophthora pathogens recruit host proteins to activate the enzymatic activity of effectors in order to gain successful infection.
Vyšlo v časopise: The Activation of Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b. PLoS Pathog 11(8): e32767. doi:10.1371/journal.ppat.1005139
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005139Souhrn
Phytophthora sojae, an oomycete pathogen that causes the Phytophthora root and stem rot disease of soybean, delivers variety of effectors into host cell to reprogram host immunity. Genome sequencing uncovers that P. sojae genome encode several hundreds of effector genes. However, the mode of action of most of the P. sojae effectors remains unknown. The investigation of effector-interacting proteins provides opportunities to better understand the pathogenesis mechanism of the pathogen and the defense mechanism of the host plants. Previously, we reported that P. sojae avirulence effector Avr3b modulates plant immunity through its Nudix hydrolase activity. Interestingly, the enzymatic activity is required for its virulence but not required for recognition by resistant gene. In this study, we identified soybean cyclophilin protein GmCYP1 as an Avr3b interactor. The enzymatic activity of GmCYP1 is required for the maturation Avr3b, which is directly related to both virulence and avirulence functions of Avr3b. This work provides a novel insight into how Phytophthora pathogens recruit host proteins to activate the enzymatic activity of effectors in order to gain successful infection.
Zdroje
1. Jones JD, Dangl JL The plant immune system. Nature. 2006; 444 : 323–329. 17108957
2. Zipfel C Plant pattern-recognition receptors. Trends Immunol. 2014; 35 : 345–351. doi: 10.1016/j.it.2014.05.004 24946686
3. Dodds PN, Rathjen JP Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. 2010; 11 : 539–548. doi: 10.1038/nrg2812 20585331
4. Win J, Chaparro-Garcia A, Belhaj K, Saunders DG, Yoshida K, Dong S, et al. Effector biology of plant-associated organisms: concepts and perspectives. Cold Spring Harb Symp Quant Biol. 2012; 77 : 235–247. doi: 10.1101/sqb.2012.77.015933 23223409
5. Bozkurt TO, Schornack S, Banfield MJ, Kamoun S Oomycetes, effectors, and all that jazz. Curr Opin Plant Biol. 2012; 15 : 483–492. doi: 10.1016/j.pbi.2012.03.008 22483402
6. Okmen B, Doehlemann G Inside plant: biotrophic strategies to modulate host immunity and metabolism. Curr Opin Plant Biol. 2014; 20 : 19–25. doi: 10.1016/j.pbi.2014.03.011 24780462
7. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, et al. Metabolic priming by a secreted fungal effector. Nature. 2011; 478 : 395–398. doi: 10.1038/nature10454 21976020
8. Liu T, Song T, Zhang X, Yuan H, Su L, Li W, et al. Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun. 2014; 5 : 4686. doi: 10.1038/ncomms5686 25156390
9. Dou D, Kale SD, Wang X, Chen Y, Wang Q, Jiang RH, et al. Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. Plant Cell. 2008; 20 : 1118–1133. doi: 10.1105/tpc.107.057067 18390593
10. Wang Q, Han C, Ferreira AO, Yu X, Ye W, Tripathy S, et al. Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell. 2011; 23 : 2064–2086. doi: 10.1105/tpc.111.086082 21653195
11. Yin W, Dong S, Zhai L, Lin Y, Zheng X, Wang Y The Phytophthora sojae Avr1d gene encodes an RxLR-dEER effector with presence and absence polymorphisms among pathogen strains. Mol Plant Microbe Interact. 2013; 26 : 958–968. doi: 10.1094/MPMI-02-13-0035-R 23594349
12. Yu X, Tang J, Wang Q, Ye W, Tao K, Duan S, et al. The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol. 2012; 196 : 247–260. doi: 10.1111/j.1469-8137.2012.04241.x 22816601
13. Zheng X, McLellan H, Fraiture M, Liu X, Boevink PC, Gilroy EM, et al. Functionally redundant RXLR effectors from Phytophthora infestans act at different steps to suppress early flg22-triggered immunity. Plos Pathogens. 2014; 10: e1004057. doi: 10.1371/journal.ppat.1004057 24763622
14. King SR, McLellan H, Boevink PC, Armstrong MR, Bukharova T, Sukarta O, et al. Phytophthora infestans RXLR Effector PexRD2 Interacts with Host MAPKKK{varepsilon} to Suppress Plant Immune Signaling. Plant Cell. 2014.
15. Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M, Oliva R, et al. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc Natl Acad Sci U S A. 2011; 108 : 20832–20837. doi: 10.1073/pnas.1112708109 22143776
16. McLellan H, Boevink PC, Armstrong MR, Pritchard L, Gomez S, Morales J, et al. An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. Plos Pathogens. 2013; 9: e1003670. doi: 10.1371/journal.ppat.1003670 24130484
17. Qiao Y, Liu L, Xiong Q, Flores C, Wong J, Shi J, et al. Oomycete pathogens encode RNA silencing suppressors. Nat Genet. 2013; 45 : 330–333. doi: 10.1038/ng.2525 23377181
18. Xiong Q, Ye W, Choi D, Wong J, Qiao Y, Tao K, et al. Phytophthora Suppressor of RNA Silencing 2 Is a Conserved RxLR Effector that Promotes Infection in Soybean and Arabidopsis thaliana. Mol Plant Microbe Interact. 2014; 27 : 1379–1389. doi: 10.1094/MPMI-06-14-0190-R 25387135
19. Dong S, Yin W, Kong G, Yang X, Qutob D, Chen Q, et al. Phytophthora sojae avirulence effector Avr3b is a secreted NADH and ADP-ribose pyrophosphorylase that modulates plant immunity. Plos Pathogens. 2011; 7: e1002353. doi: 10.1371/journal.ppat.1002353 22102810
20. McLennan AG The Nudix hydrolase superfamily. Cell Mol Life Sci. 2006; 63 : 123–143. 16378245
21. Jambunathan N, Penaganti A, Tang Y, Mahalingam R Modulation of redox homeostasis under suboptimal conditions by Arabidopsis nudix hydrolase 7. BMC Plant Biol. 2010; 10 : 173. doi: 10.1186/1471-2229-10-173 20704736
22. Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, et al. 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. 2006; 18 : 1038–1051. 16531493
23. Ge X, Li GJ, Wang SB, Zhu H, Zhu T, Wang X, et al. AtNUDT7, a negative regulator of basal immunity in Arabidopsis, modulates two distinct defense response pathways and is involved in maintaining redox homeostasis. Plant Physiol. 2007; 145 : 204–215. 17660350
24. Ge X, Xia Y The role of AtNUDT7, a Nudix hydrolase, in the plant defense response. Plant Signal Behav. 2008; 3 : 119–120. 19704728
25. Wang H, Lu Y, Liu P, Wen W, Zhang J, Ge X, et al. The ammonium/nitrate ratio is an input signal in the temperature-modulated, SNC1-mediated and EDS1-dependent autoimmunity of nudt6-2 nudt7. Plant J. 2012.
26. Bhadauria V, Banniza S, Vandenberg A, Selvaraj G, Wei Y Overexpression of a novel biotrophy-specific Colletotrichum truncatum effector, CtNUDIX, in hemibiotrophic fungal phytopathogens causes incompatibility with their host plants. Eukaryot Cell. 2013; 12 : 2–11. doi: 10.1128/EC.00192-12 22962277
27. Tamura N, Murata Y, Mukaihara T 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. 2005; 151 : 2873–2884. 16151200
28. Fischer G, Wittmann-Liebold B, Lang K, Kiefhaber T, Schmid FX Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature. 1989; 337 : 476–478. 2492638
29. Takahashi N, Hayano T, Suzuki M Peptidyl-Prolyl Cis-Trans Isomerase Is the Cyclosporin-a-Binding Protein Cyclophilin. Nature. 1989; 337 : 473–475. 2644542
30. Watashi K, Shimotohno K Cyclophilin and viruses: cyclophilin as a cofactor for viral infection and possible anti-viral target. Drug Target Insights. 2007; 2 : 9–18. 21901058
31. Li M, Ma X, Chiang YH, Yadeta KA, Ding P, Dong L, et al. Proline Isomerization of the Immune Receptor-Interacting Protein RIN4 by a Cyclophilin Inhibits Effector-Triggered Immunity in Arabidopsis. Cell Host Microbe. 2014; 16 : 473–483. doi: 10.1016/j.chom.2014.09.007 25299333
32. Zhang Y, Li B, Xu Y, Li H, Li S, Zhang D, et al. The cyclophilin CYP20-2 modulates the conformation of BRASSINAZOLE-RESISTANT1, which binds the promoter of FLOWERING LOCUS D to regulate flowering in Arabidopsis. Plant Cell. 2013; 25 : 2504–2521. doi: 10.1105/tpc.113.110296 23897924
33. Coaker G, Falick A, Staskawicz B Activation of a phytopathogenic bacterial effector protein by a eukaryotic cyclophilin. Science. 2005; 308 : 548–550. 15746386
34. Coaker G, Zhu G, Ding Z, Van Doren SR, Staskawicz B Eukaryotic cyclophilin as a molecular switch for effector activation. Mol Microbiol. 2006; 61 : 1485–1496. 16968222
35. Watashi K, Ishii N, Hijikata M, Inoue D, Murata T, Miyanari Y, et al. Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase. Mol Cell. 2005; 19 : 111–122. 15989969
36. Matouschek A, Rospert S, Schmid K, Glick BS, Schatz G Cyclophilin catalyzes protein folding in yeast mitochondria. Proc Natl Acad Sci U S A. 1995; 92 : 6319–6323. 7603990
37. Bru R, Walde P Product inhibition of alpha-chymotrypsin in reverse micelles. Eur J Biochem. 1991; 199 : 95–103. 1712303
38. Kofron JL, Kuzmic P, Kishore V, Colon-Bonilla E, Rich DH Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochemistry. 1991; 30 : 6127–6134. 2059621
39. Zydowsky LD, Etzkorn FA, Chang HY, Ferguson SB, Stolz LA, Ho SI, et al. Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci. 1992; 1 : 1092–1099. 1338979
40. Shan W, Cao M, Leung D, Tyler BM 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. 2004; 17 : 394–403. 15077672
41. Howard BR, Vajdos FF, Li S, Sundquist WI, Hill CP Structural insights into the catalytic mechanism of cyclophilin A. Nat Struct Biol. 2003; 10 : 475–481. 12730686
42. Piotukh K, Gu W, Kofler M, Labudde D, Helms V, Freund C Cyclophilin A binds to linear peptide motifs containing a consensus that is present in many human proteins. J Biol Chem. 2005; 280 : 23668–23674. 15845542
43. Wang P, Heitman J The cyclophilins. Genome Biol. 2005; 6 : 226. 15998457
44. Mainali H, Chapman P, Dhaubhadel S Genome-wide analysis of Cyclophilin gene family in soybean (Glycine max). BMC Plant Biol. 2014; 14 : 282. doi: 10.1186/s12870-014-0282-7 25348509
45. Harrison RK, Stein RL Substrate specificities of the peptidyl prolyl cis-trans isomerase activities of cyclophilin and FK-506 binding protein: evidence for the existence of a family of distinct enzymes. Biochemistry. 1990; 29 : 3813–3816. 1693856
46. Gamble TR, Vajdos FF, Yoo S, Worthylake DK, Houseweart M, Sundquist WI, et al. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell. 1996; 87 : 1285–1294. 8980234
47. Rovenich H, Boshoven JC, Thomma BP Filamentous pathogen effector functions: of pathogens, hosts and microbiomes. Curr Opin Plant Biol. 2014; 20C: 96–103.
48. Liu Y, Schiff M, Marathe R, Dinesh-Kumar SP Tobacco Rar1, EDS1 and NPR1/NIM1 like genes are required for N-mediated resistance to tobacco mosaic virus. Plant J. 2002; 30 : 415–429. 12028572
Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium
Článek The Hos2 Histone Deacetylase Controls Virulence through Direct Regulation of Mating-Type GenesČlánek Transgenic Mouse Bioassay: Evidence That Rabbits Are Susceptible to a Variety of Prion IsolatesČlánek -Associated Polyomavirus Uses a Displaced Binding Site on VP1 to Engage Sialylated GlycolipidsČlánek Parsimonious Determination of the Optimal Infectious Dose of a Pathogen for Nonhuman Primate Models
Článok vyšiel v časopisePLOS Pathogens
Najčítanejšie tento týždeň
2015 Číslo 8- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
-
Všetky články tohto čísla
- The Long and Winding Road (Apologies to the Beatles)
- The Ebola Virus: From Basic Research to a Global Health Crisis
- Riding the R Train into the Cell
- The Two-Phase Emergence of Non Pandemic HIV-1 Group O in Cameroon
- Tumor Progression Locus 2 Promotes Induction of IFNλ, Interferon Stimulated Genes and Antigen-Specific CD8 T Cell Responses and Protects against Influenza Virus
- Type VI Secretion System Toxins Horizontally Shared between Marine Bacteria
- Incomplete Neutralization and Deviation from Sigmoidal Neutralization Curves for HIV Broadly Neutralizing Monoclonal Antibodies
- E3 Ubiquitin Ligase NEDD4 Promotes Influenza Virus Infection by Decreasing Levels of the Antiviral Protein IFITM3
- The Hos2 Histone Deacetylase Controls Virulence through Direct Regulation of Mating-Type Genes
- Hyperinvasive Meningococci Induce Intra-nuclear Cleavage of the NF-κB Protein p65/RelA by Meningococcal IgA Protease
- Active Transport of Phosphorylated Carbohydrates Promotes Intestinal Colonization and Transmission of a Bacterial Pathogen
- HTLV-1 Tax Stimulates Ubiquitin E3 Ligase, Ring Finger Protein 8, to Assemble Lysine 63-Linked Polyubiquitin Chains for TAK1 and IKK Activation
- Transgenic Mouse Bioassay: Evidence That Rabbits Are Susceptible to a Variety of Prion Isolates
- Widespread Reassortment Shapes the Evolution and Epidemiology of Bluetongue Virus following European Invasion
- Inhibiting the Recruitment of PLCγ1 to Kaposi’s Sarcoma Herpesvirus K15 Protein Reduces the Invasiveness and Angiogenesis of Infected Endothelial Cells
- Goblet Cell Derived RELM-β Recruits CD4 T Cells during Infectious Colitis to Promote Protective Intestinal Epithelial Cell Proliferation
- HLA Class-II Associated HIV Polymorphisms Predict Escape from CD4+ T Cell Responses
- An siRNA Screen Identifies the U2 snRNP Spliceosome as a Host Restriction Factor for Recombinant Adeno-associated Viruses
- Extracellular Adenosine Protects against Lung Infection by Regulating Pulmonary Neutrophil Recruitment
- : Adaptations to the Dixenous Life Cycle Analyzed by Genome Sequencing, Transcriptome Profiling and Co-infection with
- Which Way In? The RalF Arf-GEF Orchestrates Host Cell Invasion
- Intracellular Uropathogenic . Exploits Host Rab35 for Iron Acquisition and Survival within Urinary Bladder Cells
- A Non-enveloped Virus Hijacks Host Disaggregation Machinery to Translocate across the Endoplasmic Reticulum Membrane
- Supporting Role for GTPase Rab27a in Hepatitis C Virus RNA Replication through a Novel miR-122-Mediated Effect
- -Associated Polyomavirus Uses a Displaced Binding Site on VP1 to Engage Sialylated Glycolipids
- The Activation of Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b
- A Pyranose-2-Phosphate Motif Is Responsible for Both Antibiotic Import and Quorum-Sensing Regulation in
- Double-Edge Sword of Sustained ROCK Activation in Prion Diseases through Neuritogenesis Defects and Prion Accumulation
- The Rsb Phosphoregulatory Network Controls Availability of the Primary Sigma Factor in and Influences the Kinetics of Growth and Development
- Inhibits Virulence through Suppression of Pyochelin and Pyoverdine Biosynthesis
- Illuminating Targets of Bacterial Secretion
- Chemical Signals and Mechanosensing in Bacterial Responses to Their Environment
- Interdisciplinarity and Infectious Diseases: An Ebola Case Study
- Fungi That Infect Insects: Altering Host Behavior and Beyond
- Plasticity and Redundancy in Proteins Important for Invasion
- Are Human Intestinal Eukaryotes Beneficial or Commensals?
- A Novel Virus Causes Scale Drop Disease in
- STAT2 Knockout Syrian Hamsters Support Enhanced Replication and Pathogenicity of Human Adenovirus, Revealing an Important Role of Type I Interferon Response in Viral Control
- Parsimonious Determination of the Optimal Infectious Dose of a Pathogen for Nonhuman Primate Models
- Twenty-Eight Years of Poliovirus Replication in an Immunodeficient Individual: Impact on the Global Polio Eradication Initiative
- AAV-Delivered Antibody Mediates Significant Protective Effects against SIVmac239 Challenge in the Absence of Neutralizing Activity
- Interferon-γ Promotes Inflammation and Development of T-Cell Lymphoma in HTLV-1 bZIP Factor Transgenic Mice
- Transgenic Rabbits Expressing Ovine PrP Are Susceptible to Scrapie
- Mitochondrial Activity and Cyr1 Are Key Regulators of Ras1 Activation of . Virulence Pathways
- Human Non-neutralizing HIV-1 Envelope Monoclonal Antibodies Limit the Number of Founder Viruses during SHIV Mucosal Infection in Rhesus Macaques
- Serine Phosphorylation of HIV-1 Vpu and Its Binding to Tetherin Regulates Interaction with Clathrin Adaptors
- Inhibition of mTORC1 Enhances the Translation of Chikungunya Proteins the Activation of the MnK/eIF4E Pathway
- Nanoformulations of Rilpivirine for Topical Pericoital and Systemic Coitus-Independent Administration Efficiently Prevent HIV Transmission
- Arming of MAIT Cell Cytolytic Antimicrobial Activity Is Induced by IL-7 and Defective in HIV-1 Infection
- sRNA-Mediated Regulation of P-Fimbriae Phase Variation in Uropathogenic
- Evolutionary and Functional Analysis of Old World Primate TRIM5 Reveals the Ancient Emergence of Primate Lentiviruses and Convergent Evolution Targeting a Conserved Capsid Interface
- Hepcidin and Host Defense against Infectious Diseases
- Type I IFN Induction via Poly-ICLC Protects Mice against Cryptococcosis
- Mucosal B Cells Are Associated with Delayed SIV Acquisition in Vaccinated Female but Not Male Rhesus Macaques Following SIV Rectal Challenge
- PLOS Pathogens
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Human Non-neutralizing HIV-1 Envelope Monoclonal Antibodies Limit the Number of Founder Viruses during SHIV Mucosal Infection in Rhesus Macaques
- Type VI Secretion System Toxins Horizontally Shared between Marine Bacteria
- Illuminating Targets of Bacterial Secretion
- Are Human Intestinal Eukaryotes Beneficial or Commensals?
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy