Acetylation of an NB-LRR Plant Immune-Effector Complex Suppresses Immunity

Overview

Journal Cell Rep

Publisher Cell Press

Specialties Biology
Cell Biology
Molecular Biology

Date 2015 Nov 21

PMID 26586425

Citations 32

Authors

Jiyoung Lee

Andrew J Manning

Donald Wolfgeher

Joanna Jelenska

Keri A Cavanaugh

Huaqin Xu

Sandra M Fernandez

Richard W Michelmore

Stephen J Kron

Jean T Greenberg

Affiliations

Soon will be listed here.

Abstract

Modifications of plant immune complexes by secreted pathogen effectors can trigger strong immune responses mediated by the action of nucleotide binding-leucine-rich repeat immune receptors. Although some strains of the pathogen Pseudomonas syringae harbor effectors that individually can trigger immunity, the plant's response may be suppressed by other virulence factors. This work reveals a robust strategy for immune suppression mediated by HopZ3, an effector in the YopJ family of acetyltransferases. The suppressing HopZ3 effector binds to and can acetylate multiple members of the RPM1 immune complex, as well as two P. syringae effectors that together activate the RPM1 complex. These acetylations modify serine, threonine, lysine, and/or histidine residues in the targets. Through HopZ3-mediated acetylation, it is possible that the whole effector-immune complex is inactivated, leading to increased growth of the pathogen.

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References

MacDonald J, Haas A, London R . Novel mechanism of surface catalysis of protein adduct formation. NMR studies of the acetylation of ubiquitin. J Biol Chem. 2000; 275(41):31908-13. DOI: 10.1074/jbc.M000684200. View

Mital J, Miller N, Fischer E, Hackstadt T . Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network. Cell Microbiol. 2010; 12(9):1235-49. PMC: 2923664. DOI: 10.1111/j.1462-5822.2010.01465.x. View

Mackey D, Belkhadir Y, Alonso J, Ecker J, Dangl J . Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell. 2003; 112(3):379-89. DOI: 10.1016/s0092-8674(03)00040-0. View

Ellis J, Dodds P . Plant pathology: monitoring a pathogen-targeted host protein. Curr Biol. 2003; 13(10):R400-2. DOI: 10.1016/s0960-9822(03)00321-x. View

Nimchuk Z, Marois E, Kjemtrup S, Leister R, Katagiri F, Dangl J . Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell. 2000; 101(4):353-63. DOI: 10.1016/s0092-8674(00)80846-6. View

Jiang S, Yao J, Ma K, Zhou H, Song J, He S . Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathog. 2013; 9(10):e1003715. PMC: 3814404. DOI: 10.1371/journal.ppat.1003715. View

Sun X, Greenwood D, Templeton M, Libich D, McGhie T, Xue B . The intrinsically disordered structural platform of the plant defence hub protein RPM1-interacting protein 4 provides insights into its mode of action in the host-pathogen interface and evolution of the nitrate-induced domain protein family. FEBS J. 2014; 281(17):3955-79. DOI: 10.1111/febs.12937. View

Gabriel D, Burges A, Lazo G . Gene-for-gene interactions of five cloned avirulence genes from Xanthomonas campestris pv. malvacearum with specific resistance genes in cotton. Proc Natl Acad Sci U S A. 1986; 83(17):6415-9. PMC: 386514. DOI: 10.1073/pnas.83.17.6415. View

Mukherjee S, Keitany G, Li Y, Wang Y, Ball H, Goldsmith E . Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science. 2006; 312(5777):1211-4. DOI: 10.1126/science.1126867. View

10.

Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D, Kraut A . A receptor pair with an integrated decoy converts pathogen disabling of transcription factors to immunity. Cell. 2015; 161(5):1074-1088. DOI: 10.1016/j.cell.2015.04.025. View

11.

Simonich M, Innes R . A disease resistance gene in Arabidopsis with specificity for the avrPph3 gene of Pseudomonas syringae pv. phaseolicola. Mol Plant Microbe Interact. 1995; 8(4):637-40. DOI: 10.1094/mpmi-8-0637. View

12.

Gassmann M, Grenacher B, Rohde B, Vogel J . Quantifying Western blots: pitfalls of densitometry. Electrophoresis. 2009; 30(11):1845-55. DOI: 10.1002/elps.200800720. View

13.

Tsiamis G, Mansfield J, Hockenhull R, Jackson R, Sesma A, Athanassopoulos E . Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 2000; 19(13):3204-14. PMC: 313945. DOI: 10.1093/emboj/19.13.3204. View

14.

Zhang J, Li W, Xiang T, Liu Z, Laluk K, Ding X . Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host Microbe. 2010; 7(4):290-301. DOI: 10.1016/j.chom.2010.03.007. View

15.

Kim H, Desveaux D, Singer A, Patel P, Sondek J, Dangl J . The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Natl Acad Sci U S A. 2005; 102(18):6496-501. PMC: 1088372. DOI: 10.1073/pnas.0500792102. View

16.

Nuhse T, Stensballe A, Jensen O, Peck S . Phosphoproteomics of the Arabidopsis plasma membrane and a new phosphorylation site database. Plant Cell. 2004; 16(9):2394-405. PMC: 520941. DOI: 10.1105/tpc.104.023150. View

17.

Paquette N, Conlon J, Sweet C, Rus F, Wilson L, Pereira A . Serine/threonine acetylation of TGFβ-activated kinase (TAK1) by Yersinia pestis YopJ inhibits innate immune signaling. Proc Natl Acad Sci U S A. 2012; 109(31):12710-5. PMC: 3411953. DOI: 10.1073/pnas.1008203109. View

18.

Vinatzer B, Teitzel G, Lee M, Jelenska J, Hotton S, Fairfax K . The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Mol Microbiol. 2006; 62(1):26-44. DOI: 10.1111/j.1365-2958.2006.05350.x. View

19.

Jamir Y, Guo M, Oh H, Petnicki-Ocwieja T, Chen S, Tang X . Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J. 2004; 37(4):554-65. DOI: 10.1046/j.1365-313x.2003.01982.x. View

20.

Sarris P, Duxbury Z, Huh S, Ma Y, Segonzac C, Sklenar J . A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors. Cell. 2015; 161(5):1089-1100. DOI: 10.1016/j.cell.2015.04.024. View