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Crystal structures of the type III effector protein AvrPphF and its chaperone reveal residues required for plant pathogenesis.

Singer AU, Desveaux D, Betts L, Chang JH, Nimchuk Z, Grant SR, Dangl JL, Sondek J
Structure 12 1669-81 (2004)
Cited: 50 times
EuropePMC logo PMID: 15341731

Abstract

The avrPphF locus from Pseudomonas syringae pv. phaseolicola, the causative agent of bean halo-blight disease, encodes proteins which either enhance virulence on susceptible hosts or elicit defense responses on hosts carrying the R1 resistance gene. Here we present the crystal structures of the two proteins from the avrPphF operon. The structure of AvrPphF ORF1 is strikingly reminiscent of type III chaperones from bacterial pathogens of animals, indicating structural conservation of these specialized chaperones, despite high sequence divergence. The AvrPphF ORF2 effector adopts a novel "mushroom"-like structure containing "head" and "stalk" subdomains. The head subdomain possesses limited structural homology to the catalytic domain of bacterial ADP-ribosyltransferases (ADP-RTs), though no ADP-RT activity was detected for AvrPphF ORF2 in standard assays. Nonetheless, this structural similarity identified two clusters of conserved surface-exposed residues important for both virulence mediated by AvrPphF ORF2 and recognition of this effector by bean plants expressing the R1 resistance gene.

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  1. The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Guo M, Tian F, Wamboldt Y, Alfano JR. Mol Plant Microbe Interact 22 1069-1080 (2009)
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  4. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F, Westedt I, Staiger D, Alfano JR, Zipfel C. EMBO J 32 701-712 (2013)
  5. The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D. Proc Natl Acad Sci U S A 107 2349-2354 (2010)
  6. The Pseudomonas syringae effector HopF2 suppresses Arabidopsis immunity by targeting BAK1. Zhou J, Wu S, Chen X, Liu C, Sheen J, Shan L, He P. Plant J 77 235-245 (2014)
  7. Protein structure database search and evolutionary classification. Yang JM, Tung CH. Nucleic Acids Res 34 3646-3659 (2006)
  8. Structure function analysis of an ADP-ribosyltransferase type III effector and its RNA-binding target in plant immunity. Jeong BR, Lin Y, Joe A, Guo M, Korneli C, Yang H, Wang P, Yu M, Cerny RL, Staiger D, Alfano JR, Xu Y. J Biol Chem 286 43272-43281 (2011)
  9. A pathogen type III effector with a novel E3 ubiquitin ligase architecture. Singer AU, Schulze S, Skarina T, Xu X, Cui H, Eschen-Lippold L, Egler M, Srikumar T, Raught B, Lee J, Scheel D, Savchenko A, Bonas U. PLoS Pathog 9 e1003121 (2013)
  10. The Pseudomonas syringae pv. tomato DC3000 type III effector HopF2 has a putative myristoylation site required for its avirulence and virulence functions. Robert-Seilaniantz A, Shan L, Zhou JM, Tang X. Mol Plant Microbe Interact 19 130-138 (2006)
  11. Distinct regions of the Pseudomonas syringae coiled-coil effector AvrRps4 are required for activation of immunity. Sohn KH, Hughes RK, Piquerez SJ, Jones JD, Banfield MJ. Proc Natl Acad Sci U S A 109 16371-16376 (2012)
  12. The Pseudomonas syringae type III effector HopF2 suppresses Arabidopsis stomatal immunity. Hurley B, Lee D, Mott A, Wilton M, Liu J, Liu YC, Angers S, Coaker G, Guttman DS, Desveaux D. PLoS One 9 e114921 (2014)
  13. Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Seto D, Koulena N, Lo T, Menna A, Guttman DS, Desveaux D. Nat Plants 3 17027 (2017)
  14. Bacterial effector HopF2 suppresses arabidopsis innate immunity at the plasma membrane. Wu S, Lu D, Kabbage M, Wei HL, Swingle B, Records AR, Dickman M, He P, Shan L. Mol Plant Microbe Interact 24 585-593 (2011)
  15. Computational Structural Genomics Unravels Common Folds and Novel Families in the Secretome of Fungal Phytopathogen Magnaporthe oryzae. Seong K, Krasileva KV. Mol Plant Microbe Interact 34 1267-1280 (2021)
  16. AvrRpm1 Functions as an ADP-Ribosyl Transferase to Modify NOI Domain-Containing Proteins, Including Arabidopsis and Soybean RPM1-Interacting Protein4. Redditt TJ, Chung EH, Karimi HZ, Rodibaugh N, Zhang Y, Trinidad JC, Kim JH, Zhou Q, Shen M, Dangl JL, Mackey D, Innes RW. Plant Cell 31 2664-2681 (2019)
  17. Chlamydia trachomatis Slc1 is a type III secretion chaperone that enhances the translocation of its invasion effector substrate TARP. Brinkworth AJ, Malcolm DS, Pedrosa AT, Roguska K, Shahbazian S, Graham JE, Hayward RD, Carabeo RA. Mol Microbiol 82 131-144 (2011)
  18. Crystal structure of Yersinia enterocolitica type III secretion chaperone SycT. Büttner CR, Cornelis GR, Heinz DW, Niemann HH. Protein Sci 14 1993-2002 (2005)
  19. The Escherichia coli effector EspJ blocks Src kinase activity via amidation and ADP ribosylation. Young JC, Clements A, Lang AE, Garnett JA, Munera D, Arbeloa A, Pearson J, Hartland EL, Matthews SJ, Mousnier A, Barry DJ, Way M, Schlosser A, Aktories K, Frankel G. Nat Commun 5 5887 (2014)
  20. Pseudomonas syringae type III chaperones ShcO1, ShcS1, and ShcS2 facilitate translocation of their cognate effectors and can substitute for each other in the secretion of HopO1-1. Guo M, Chancey ST, Tian F, Ge Z, Jamir Y, Alfano JR. J Bacteriol 187 4257-4269 (2005)
  21. Changes in race-specific virulence in Pseudomonas syringae pv. phaseolicola are associated with a chimeric transposable element and rare deletion events in a plasmid-borne pathogenicity island. Rivas LA, Mansfield J, Tsiamis G, Jackson RW, Murillo J. Appl Environ Microbiol 71 3778-3785 (2005)
  22. Structure of the HopA1(21-102)-ShcA chaperone-effector complex of Pseudomonas syringae reveals conservation of a virulence factor binding motif from animal to plant pathogens. Janjusevic R, Quezada CM, Small J, Stebbins CE. J Bacteriol 195 658-664 (2013)
  23. Structure-based mutagenesis of SigE verifies the importance of hydrophobic and electrostatic residues in type III chaperone function. Knodler LA, Bertero M, Yip C, Strynadka NC, Steele-Mortimer O. Mol Microbiol 62 928-940 (2006)
  24. AvrRpm1 missense mutations weakly activate RPS2-mediated immune response in Arabidopsis thaliana. Cherkis KA, Temple BR, Chung EH, Sondek J, Dangl JL. PLoS One 7 e42633 (2012)
  25. A solvent-exposed patch in chaperone-bound YopE is required for translocation by the type III secretion system. Rodgers L, Mukerjea R, Birtalan S, Friedberg D, Ghosh P. J Bacteriol 192 3114-3122 (2010)
  26. Nuclear Import of Arabidopsis Poly(ADP-Ribose) Polymerase 2 Is Mediated by Importin-α and a Nuclear Localization Sequence Located Between the Predicted SAP Domains. Chen C, Masi R, Lintermann R, Wirthmueller L. Front Plant Sci 9 1581 (2018)
  27. A substrate-inspired probe monitors translocation, activation, and subcellular targeting of bacterial type III effector protease AvrPphB. Lu H, Wang Z, Shabab M, Oeljeklaus J, Verhelst SH, Kaschani F, Kaiser M, Bogyo M, van der Hoorn RA. Chem Biol 20 168-176 (2013)
  28. Context-dependent protein folding of a virulence peptide in the bacterial and host environments: structure of an SycH-YopH chaperone-effector complex. Vujanac M, Stebbins CE. Acta Crystallogr D Biol Crystallogr 69 546-554 (2013)
  29. Pseudomonas syringae pv. phaseolicola effector HopF1 inhibits pathogen-associated molecular pattern-triggered immunity in a RIN4-independent manner in common bean (Phaseolus vulgaris). Hou S, Mu R, Ma G, Xu X, Zhang C, Yang Y, Wu D. FEMS Microbiol Lett 323 35-43 (2011)
  30. Lessons learned from type III effector transgenic plants. Wilton M, Desveaux D. Plant Signal Behav 5 746-748 (2010)
  31. Interfacial residues of SpcS chaperone affects binding of effector toxin ExoT in Pseudomonas aeruginosa: novel insights from structural and computational studies. Dey S, Datta S. FEBS J 281 1267-1280 (2014)


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