Two serine residues in Pseudomonas syringae effector HopZ1a are required for acetyltransferase activity and association with the host co-factor

New Phytologist

Volumn 208, Issue 4, 2015, Pages 1157-1168

  Ma, Ka Wai ^a   Jiang, Shushu ^a   Hawara, Eva ^a   Lee, Donghyuk ^b   Pan, Songqin ^a   Coaker, Gitta ^b   Song, Jikui ^c   Ma, Wenbo ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Acetyltransferase; Arabidopsis thaliana; Bacterial virulence; Inositol hexakisphosphate (IP6); Pseudomonas syringae; Stomatal aperture; YopJ family type III effectors

Indexed keywords

CATALYSIS; ENZYME ACTIVITY; NUCLEAR MAGNETIC RESONANCE; PATHOGEN; STOMATAL CONDUCTANCE; VIRULENCE;

ARABIDOPSIS THALIANA; BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; PSEUDOMONAS SYRINGAE; RALSTONIA;

ACYLTRANSFERASE; ARABIDOPSIS PROTEIN; BACTERIAL PROTEIN; PHYTIC ACID; SERINE; VIRULENCE FACTOR;

ARABIDOPSIS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PLANT DISEASE; PROTEIN PROCESSING; PSEUDOMONAS SYRINGAE; RALSTONIA; VIRULENCE;

ACETYLTRANSFERASES; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BACTERIAL PROTEINS; HOST-PATHOGEN INTERACTIONS; PHYTIC ACID; PLANT DISEASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PSEUDOMONAS SYRINGAE; RALSTONIA; SERINE; VIRULENCE; VIRULENCE FACTORS;

EID: 84946491427     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13528     Document Type: Article

References (40)

1. Berndsen CE, Denu JM. 2005. Assays for mechanistic investigations of protein/histone acetyltransferases. Methods 36: 321-331.
2. Bohm H, Albert I, Fan L, Reinhard A, Nurnberger T. 2014. Immune receptor complexes at the plant cell surface. Current Opinion in Plant Biology 20: 47-54.
3. Cheong MS, Kirik A, Kim J-G, Frame K, Kirik V, Mudgett MB. 2014. AvrBsT acetylates Arabidopsis ACIP1, a protein that associates with microtubules and is required for immunity. PLoS Pathogens 10: e1003952.
4. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
5. 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.
6. Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J, Keinath NF, Weatherly B, Jiang L, Schumacher K, Hicks G et al. 2012. Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Research 22: 413-424.
7. Feng F, Zhou JM. 2012. Plant-bacterial pathogen interactions mediated by type III effectors. Current Opinion in Plant Biology 15: 469-476.
8. Galan JE, Lara-Tejero M, Marlovits TC, Wagner S. 2014. Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annual Review of Microbiology 68: 415-438.
9. Hebert AS, Richards AL, Bailey DJ, Ulbrich A, Coughlin EE, Westphall MS, Coon JJ. 2014. The one hour yeast proteome. Molecular & Cellular Proteomics: MCP 13: 339-347.
10. Hurley B, Lee D, Mott A, Wilton M, Liu J, Liu YC, Angers S, Coaker G, Guttman DS, Desveaux D. 2014. The Pseudomonas syringae type III effector HopF2 suppresses Arabidopsis stomatal immunity. PLoS One 9: e114921.
11. Jacob F, Vernaldi S, Maekawa T. 2013. Evolution and conservation of plant NLR functions. Frontiers in Immunology 4: 297.
12. Jiang S, Yao J, Ma K-W, Zhou H, Song J, He SY, Ma W. 2013. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS Pathogens 9: e1003715.
13. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444: 323-329.
14. Jones RM, Wu H, Wentworth C, Luo L, Collier-Hyams L, Neish AS. 2008. Salmonella AvrA coordinates suppression of host immune and apoptotic defenses via JNK pathway blockade. Cell Host & Microbe 3: 233-244.
15. Joung M-J, Mohan SK, Yu C. 2012. Molecular level interaction of inositol hexaphosphate with the C2B domain of human synaptotagmin I. Biochemistry 51: 3675-3683.
16. Lee AH-Y, Hurley B, Felsensteiner C, Yea C, Ckurshumova W, Bartetzko V, Wang PW, Quach V, Lewis JD, Liu YC et al. 2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLoS Pathogens 8: e1002523.
17. Lewis JD, Lee AH-Y, Hassan JA, Wan J, Hurley B, Jhingree JR, Wang PW, Lo T, Youn J-Y, Guttman DS et al. 2013. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. Proceedings of the National Academy of Sciences, USA 110: 18722-18727.
18. Lewis JD, Wu R, Guttman DS, Desveaux D. 2010. Allele-specific virulence attenuation of the Pseudomonas syringae HopZ1a type III effector via the Arabidopsis ZAR1 resistance protein. PLoS Genetics 6: e1000894.
19. +-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biology 7: e1000139.
20. Lozano-Duran R, Bourdais G, He SY, Robatzek S. 2014. The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytologist 202: 259-269.
21. Lupardus PJ, Shen A, Bogyo M, Garcia KC. 2008. Small molecule-induced allosteric activation of the Vibrio cholerae RTX cysteine protease domain. Science 322: 265-268.
22. Ma W, Dong FFT, Stavrinides J, Guttman DS. 2006. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genetics 2: e0020209.
23. Macbeth MR, Schubert HL, VanDemark AP, Lingam AT, Hill CP, Bass BL. 2005. Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 309: 1534-1539.
24. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980.
25. Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM. 2010. Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22: 973-990.
26. Mittal R, Peak-Chew S-Y, McMahon HT. 2006. Acetylation of MEK2 and IκB kinase (IKK) activation loop residues by YopJ inhibits signaling. Proceedings of the National Academy of Sciences, USA 103: 18574-18579.
27. Mittal R, Peak-Chew SY, Sade RS, Vallis Y, McMahon HT. 2010. The acetyltransferase activity of the bacterial toxin YopJ of Yersinia is activated by eukaryotic host cell inositol hexakisphosphate. Journal of Biological Chemistry 285: 19927-19934.
28. Morgan RL, Zhou H, Lehto E, Nguyen N, Bains A, Wang X, Ma W. 2010. Catalytic domain of the diversified Pseudomonas syringae type III effector HopZ1 determines the allelic specificity in plant hosts. Molecular Microbiology 76: 437-455.
29. Mukherjee S, Hao Y-H, Orth K. 2007. A newly discovered post-translational modification - the acetylation of serine and threonine residues. Trends in Biochemical Sciences 32: 210-216.
30. Mukherjee S, Keitany G, Li Y, Wang Y, Ball HL, Goldsmith EJ, Orth K. 2006. Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 1211-1214.
31. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, Bliska JB, Mangel WF, Staskawicz B, Dixon JE. 2000. Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
32. Pruitt RN, Chagot B, Cover M, Chazin WJ, Spiller B, Lacy DB. 2009. Structure-function analysis of inositol hexakisphosphate-induced autoprocessing in Clostridium difficile toxin A. Journal of Biological Chemistry 284: 21934-21940.
33. Qi D, Innes RW. 2013. Recent advances in plant NLR structure, function, localization, and signaling. Frontiers in Immunology 4: 348.
34. Spoel SH, Dong X. 2012. How do plants achieve immunity? Defence without specialized immune cells. Nature Reviews Immunology 12: 89-100.
35. Tasset C, Bernoux M, Jauneau A, Pouzet C, Brière C, Kieffer-Jacquinod S, Rivas S, Marco Y, Deslandes L. 2010. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLoS Pathogens 6: e1001202.
36. Trosky JE, Li Y, Mukherjee S, Keitany G, Ball H, Orth K. 2007. VopA Inhibits ATP binding by acetylating the catalytic loop of MAPK kinases. Journal of Biological Chemistry 282: 34299-34305.
37. Vinatzer BA, Teitzel GM, Lee M-W, Jelenska J, Hotton S, Fairfax K, Jenrette J, Greenberg JT. 2006. The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Molecular Microbiology 62: 26-44.
38. Zheng X-y, Spivey Natalie W, Zeng W, Liu P-P, Fu Zheng Q, Klessig Daniel F, He Sheng Y, Dong X. 2012. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host & Microbe 11: 587-596.
39. Zhuang T, Vishnivetskiy SA, Gurevich VV, Sanders CR. 2010. Elucidation of inositol hexaphosphate and heparin interaction sites and conformational changes in Arrestin-1 by solution nuclear magnetic resonance. Biochemistry 49: 10473-10485.
40. Zipfel C. 2014. Plant pattern-recognition receptors. Trends in Immunology 35: 345-351.