The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity

New Phytologist

Volumn 202, Issue 1, 2014, Pages 259-269

  Lozano Durán, Rosa ^a   Bourdais, Gildas ^a   He, Sheng Yang ^b   Robatzek, Silke ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

14 3 3; Effector; HopM1; Immunity; Oxidative burst; PAMP MAMP; Stomata; TFT1

Indexed keywords

ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; BENZYLOXYCARBONYLLEUCYL LEUCYL LEUCINE ALDEHYDE; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; EFFECTOR; FLAGELLIN; LEUPEPTIN; PATTERN RECOGNITION RECEPTOR; PROTEASOME; PROTEIN 14 3 3; REACTIVE OXYGEN METABOLITE;

14-3-3; ARABIDOPSIS; ARTICLE; CELL NUCLEUS; DRUG EFFECT; GENE SILENCING; HOPM1; IMMUNITY; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PAMP/MAMP; PLANT IMMUNITY; PLANT STOMA; PSEUDOMONAS SYRINGAE; RESPIRATORY BURST; STOMATA; TFT1; TOBACCO; TOMATO;

14-3-3; EFFECTOR; HOPM1; IMMUNITY; OXIDATIVE BURST; PAMP/MAMP; STOMATA; TFT1;

14-3-3 PROTEINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; CELL NUCLEUS; FLAGELLIN; GENE KNOCKDOWN TECHNIQUES; LEUPEPTINS; LYCOPERSICON ESCULENTUM; PLANT IMMUNITY; PLANT STOMATA; PROTEASOME ENDOPEPTIDASE COMPLEX; PSEUDOMONAS SYRINGAE; REACTIVE OXYGEN SPECIES; RECEPTORS, PATTERN RECOGNITION; RESPIRATORY BURST; TOBACCO;

EID: 84894430322     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12651     Document Type: Article

References (47)

1. Albrecht C, Boutrot F, Segonzac C, Schwessinger B, Gimenez-Ibanez S, Chinchilla D, Rathjen JP, de Vries SC, Zipfel C. 2012. Brassinosteroids inhibit pathogen-associated molecular pattern-triggered immune signaling independent of the receptor kinase BAK1. Proceedings of the National Academy of Sciences, USA 109: 303-308.
2. Angot A, Vergunst A, Genin S, Peeters N. 2007. Exploitation of eukaryotic ubiquitin signaling pathways by effectors translocated by bacterial type III and type IV secretion systems. PLoS Pathogens 3: e3.
3. Badel JL, Shimizu R, Oh HS, Collmer A. 2006. A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Molecular Plant-Microbe Interactions 19: 99-111.
4. Belkhadir Y, Jaillais Y, Epple P, Balsemao-Pires E, Dangl JL, Chory J. 2012. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proceedings of the National Academy of Sciences, USA 109: 297-302.
5. Boller T, Felix G. 2009. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60: 379-406.
6. Collmer A, Badel JL, Charkowski AO, Deng WL, Fouts DE, Ramos AR, Rehm AH, Anderson DM, Schneewind O, van Dijk K et al. 2000. Pseudomonas syringae Hrp type III secretion system and effector proteins. Proceedings of the National Academy of Sciences, USA 97: 8770-8777.
7. Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, Collmer A. 2011. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proceedings of the National Academy of Sciences, USA 108: 2975-2980.
8. Cunnac S, Lindeberg M, Collmer A. 2009. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Current Opinion in Microbiology 12: 53-60.
9. DebRoy S, Thilmony R, Kwack YB, Nomura K, He SY. 2004. A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proceedings of the National Academy of Sciences, USA 101: 9927-9932.
10. Elmayan T, Fromentin J, Riondet C, Alcaraz G, Blein JP, Simon-Plas F. 2007. Regulation of reactive oxygen species production by a 14-3-3 protein in elicited tobacco cells. Plant, Cell & Environment 30: 722-732.
11. Gampala SS, Kim TW, He JX, Tang W, Deng Z, Bai MY, Guan S, Lalonde S, Sun Y, Gendron JM et al. 2007. An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Developmental Cell 13: 177-189.
12. Giska F, Lichocka M, Piechocki M, Dadlez M, Schmelzer E, Hennig J, Krzymowska M. 2013. Phosphorylation of HopQ1, a type III effector from Pseudomonas syringae, creates a binding site for host 14-3-3 proteins. Plant Physiology 161: 2049-2061.
13. Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Current Biology 18: 1824-1832.
14. Grefen C, Donald N, Hashimoto K, Kudla J, Schumacher K, Blatt MR. 2010. A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant Journal 64: 355-365.
15. Kvitko BH, Park DH, Velasquez AC, Wei CF, Russell AB, Martin GB, Schneider DJ, Collmer A. 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathogens 5: e1000388.
16. Li W, Yadeta KA, Elmore JM, Coaker G. 2013. The Pseudomonas syringae effector HopQ1 promotes bacterial virulence and interacts with tomato 14-3-3 proteins in a phosphorylation-dependent manner. Plant Physiology 161: 2062-2074.
17. Liu D, Shi L, Han C, Yu J, Li D, Zhang Y. 2012. Validation of reference genes for gene expression studies in virus-infected Nicotiana benthamiana using quantitative real-time PCR. PLoS ONE 7: e46451.
18. Lozano-Duran R, Rosas-Diaz T, Luna AP, Bejarano ER. 2011. Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS ONE 6: e22383.
19. Manosalva PM, Bruce M, Leach JE. 2011. Rice 14-3-3 protein (GF14e) negatively affects cell death and disease resistance. Plant Journal 68: 777-787.
20. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980.
21. Mersmann S, Bourdais G, Rietz S, Robatzek S. 2010. Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiology 154: 391-400.
22. Nakagawa T, Kurose T, Hino T, Tanaka K, Kawamukai M, Niwa Y, Toyooka K, Matsuoka K, Jinbo T, Kimura T. 2007. Development of series of gateway binary vectors, pGWBs, for realizing efficient construction of fusion genes for plant transformation. Journal of Bioscience and Bioengineering 104: 34-41.
23. Nemhauser JL, Mockler TC, Chory J. 2004. Interdependency of brassinosteroid and auxin signaling in Arabidopsis. PLoS Biology 2: E258.
24. Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F, Westedt I, Staiger D, Alfano JR, Zipfel C. 2013. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO Journal 32: 701-712.
25. Nicaise V, Roux M, Zipfel C. 2009. Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiology 150: 1638-1647.
26. Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY. 2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313: 220-223.
27. Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. 2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. Proceedings of the National Academy of Sciences, USA 108: 10 774-10 779.
28. Oh CS, Martin GB. 2011. Tomato 14-3-3 protein TFT7 interacts with a MAP kinase kinase to regulate immunity-associated programmed cell death mediated by diverse disease resistance proteins. Journal of Biological Chemistry 286: 14 129-14 136.
29. Oh CS, Pedley KF, Martin GB. 2010. Tomato 14-3-3 protein 7 positively regulates immunity-associated programmed cell death by enhancing protein abundance and signaling ability of MAPKKK-α. Plant Cell 22: 260-272.
30. Oh HS, Collmer A. 2005. Basal resistance against bacteria in Nicotiana benthamiana leaves is accompanied by reduced vascular staining and suppressed by multiple Pseudomonas syringae type III secretion system effector proteins. Plant Journal 44: 348-359.
31. Paul AL, Denison FC, Schultz ER, Zupanska AK, Ferl RJ. 2012. 14-3-3 phosphoprotein interaction networks - does isoform diversity present functional interaction specification? Frontiers in Plant Science 3: 190.
32. Paul AL, Sehnke PC, Ferl RJ. 2005. Isoform-specific subcellular localization among 14-3-3 proteins in Arabidopsis seems to be driven by client interactions. Molecular Biology of the Cell 16: 1735-1743.
33. Robatzek S, Chinchilla D, Boller T. 2006. Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes & Development 20: 537-542.
34. Roberts MR, de Bruxelles GL. 2002. Plant 14-3-3 protein families: evidence for isoform-specific functions? Biochemical Society Transactions 30: 373-378.
35. Ryu H, Kim K, Cho H, Park J, Choe S, Hwang I. 2007. Nucleocytoplasmic shuttling of BZR1 mediated by phosphorylation is essential in Arabidopsis brassinosteroid signaling. Plant Cell 19: 2749-2762.
36. Salomon S, Grunewald D, Stuber K, Schaaf S, MacLean D, Schulze-Lefert P, Robatzek S. 2010. High-throughput confocal imaging of intact live tissue enables quantification of membrane trafficking in Arabidopsis. Plant Physiology 154: 1096-1104.
37. Schellenberg B, Ramel C, Dudler R. 2010. Pseudomonas syringae virulence factor syringolin A counteracts stomatal immunity by proteasome inhibition. Molecular Plant-Microbe Interactions 23: 1287-1293.
38. Segonzac C, Feike D, Gimenez-Ibanez S, Hann DR, Zipfel C, Rathjen JP. 2011. Hierarchy and roles of pathogen-associated molecular pattern-induced responses in Nicotiana benthamiana. Plant Physiology 156: 687-699.
39. Shan L, He P, Li J, Heese A, Peck SC, Nurnberger T, Martin GB, Sheen J. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host & Microbe 4: 17-27.
40. Spallek T, Robatzek S, Gohre V. 2009. How microbes utilize host ubiquitination. Cellular Microbiology 11: 1425-1434.
41. Sun Y, Fan XY, Cao DM, Tang W, He K, Zhu JY, He JX, Bai MY, Zhu S, Oh E et al. 2010. Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell 19: 765-777.
42. Taylor KW, Kim JG, Su XB, Aakre CD, Roden JA, Adams CM, Mudgett MB. 2012. Tomato TFT1 is required for PAMP-triggered immunity and mutations that prevent T3S effector XopN from binding to TFT1 attenuate Xanthomonas virulence. PLoS Pathogens 8: e1002768.
43. Thwaites R, Spanu PD, Panopoulos NJ, Stevens C, Mansfield JW. 2004. Transcriptional regulation of components of the type III secretion system and effectors in Pseudomonas syringae pv. phaseolicola. Molecular Plant-Microbe Interactions 17: 1250-1258.
44. de Torres M, Mansfield JW, Grabov N, Brown IR, Ammouneh H, Tsiamis G, Forsyth A, Robatzek S, Grant M, Boch J. 2006. Pseudomonas syringae effector AvrPtoB suppresses basal defence in Arabidopsis. Plant Journal 47: 368-382.
45. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J et al. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Current Biology 18: 74-80.
46. Zipfel C, Robatzek S. 2010. Pathogen-associated molecular pattern-triggered immunity: veni, vidi...? Plant Physiology 154: 551-554.
47. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T. 2004. Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767.