The Activation of Effector Avr3b by Plant Cyclophilin is Required for the Nudix Hydrolase Activity of Avr3b

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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.1005139

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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