AvrBsT Acetylates Arabidopsis ACIP1, a Protein that Associates with Microtubules and Is Required for Immunity

PLoS Pathogens

Volumn 10, Issue 2, 2014, Pages

  Cheong, Mi Sun ^a   Kirik, Angela ^b   Kim, Jung Gun ^a   Frame, Kenneth ^a   Kirik, Viktor ^b   Mudgett, Mary Beth ^a  

^a STANFORD UNIVERSITY   (United States)

^b ILLINOIS STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATED INTERACTING PROTEIN1; ACYLTRANSFERASE; AVRBST VIRULENCE FACTOR; PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ACETYLATION; ARABIDOPSIS THALIANA; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC ANALYSIS; INFECTION RESISTANCE; MICROTUBULE; MUTATION; NONHUMAN; PLANT IMMUNITY; PROTEIN LOCALIZATION; PSEUDOMONAS SYRINGAE PV. TOMATO; TYPE III SECRETION SYSTEM;

ACETYLATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; MICROTUBULES; PLANT DISEASES; PLANTS, GENETICALLY MODIFIED; POLYMERASE CHAIN REACTION; PSEUDOMONAS INFECTIONS; PSEUDOMONAS SYRINGAE; TWO-HYBRID SYSTEM TECHNIQUES; VIRULENCE FACTORS;

EID: 84895759238     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003952     Document Type: Article

References (61)

1. Buttner D, (2012) Protein export according to schedule: architecture, assembly, and regulation of type III secretion systems from plant- and animal-pathogenic bacteria. Microbiol Mol Biol Rev 76: 262-310.
2. Lewis JD, Lee A, Ma W, Zhou H, Guttman DS, et al. (2011) The YopJ superfamily in plant-associated bacteria. Mol Plant Pathol 12: 928-937.
3. Monack DM, Mecsas J, Ghori N, Falkow S, (1997) Yersinia signals macrophages to undergo apoptosis and YopJ is necessary for this cell death. Proc Natl Acad Sci U S A 94: 10385-10390.
4. Rawlings ND, Salvesen G (2013) Handbook of proteolytic enzymes. 3rd ed. London; Boston: Academic Press.
5. Orth K, Xu Z, Mudgett MB, Bao ZQ, Palmer LE, et al. (2000) Disruption of signaling by Yersinia effector YopJ, a ubiquitin-like protein protease. Science 290: 1594-1597.
6. Mukherjee S, Keitany G, Li Y, Wang Y, Ball HL, et al. (2006) Yersinia YopJ acetylates and inhibits kinase activation by blocking phosphorylation. Science 312: 1211-1214.
7. Trosky JE, Li Y, Mukherjee S, Keitany G, Ball H, et al. (2007) VopA inhibits ATP binding by acetylating the catalytic loop of MAPK kinases. J Biol Chem 282: 34299-34305.
8. Jones RM, Wu H, Wentworth C, Luo L, Collier-Hyams L, et al. (2008) Salmonella AvrA Coordinates Suppression of Host Immune and Apoptotic Defenses via JNK Pathway Blockade. Cell host & microbe 3: 233-244.
9. Tasset C, Bernoux M, Jauneau A, Pouzet C, Briere C, et al. (2010) Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLoS pathogens 6: e1001202.
10. Lee AH, Hurley B, Felsensteiner C, Yea C, Ckurshumova W, et al. (2012) A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLoS pathogens 8: e1002523.
11. Sharlach M, Dahlbeck D, Liu L, Chiu J, Jimenez-Gomez JM, et al. (2013) Fine genetic mapping of RXopJ4, a bacterial spot disease resistance locus from Solanum pennellii LA716. Theor Appl Genet 126: 601-609.
12. Whalen MC, Wang JF, Carland FM, Heiskell ME, Dahlbeck D, et al. (1993) Avirulence gene avrRxv from Xanthomonas campestris pv. vesicatoria specifies resistance on tomato line Hawaii 7998. Mol Plant Microbe Interact 6: 616-627.
13. Zhou H, Morgan RL, Guttman DS, Ma W, (2009) Allelic variants of the Pseudomonas syringae type III effector HopZ1 are differentially recognized by plant resistance systems. Mol Plant Microbe Interact 22: 176-189.
14. Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, et al. (2002) Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci U S A 99: 2404-2409.
15. 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.
16. Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, et al. (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci U S A 100: 8024-8029.
17. Lewis JD, Lee AH, Hassan JA, Wan J, Hurley B, et al. (2013) The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. Proc Natl Acad Sci U S A 110: 18722-18727.
18. Mittal R, Peak-Chew SY, McMahon HT, (2006) Acetylation of MEK2 and I kappa B kinase (IKK) activation loop residues by YopJ inhibits signaling. Proc Natl Acad Sci U S A 103: 18574-18579.
19. Meinzer U, Barreau F, Esmiol-Welterlin S, Jung C, Villard C, et al. (2012) Yersinia pseudotuberculosis effector YopJ subverts the Nod2/RICK/TAK1 pathway and activates caspase-1 to induce intestinal barrier dysfunction. Cell host & microbe 11: 337-351.
20. Akella JS, Wloga D, Kim J, Starostina NG, Lyons-Abbott S, et al. (2010) MEC-17 is an alpha-tubulin acetyltransferase. Nature 467: 218-222.
21. Shida T, Cueva JG, Xu Z, Goodman MB, Nachury MV, (2010) The major alpha-tubulin K40 acetyltransferase alphaTAT1 promotes rapid ciliogenesis and efficient mechanosensation. Proc Natl Acad Sci U S A 107: 21517-21522.
22. Cunnac S, Wilson A, Nuwer J, Kirik A, Baranage G, et al. (2007) A Conserved Carboxylesterase Is a SUPPRESSOR OF AVRBST-ELICITED RESISTANCE in Arabidopsis. Plant Cell 19: 688-705.
23. Kirik A, Mudgett MB, (2009) SOBER1 phospholipase activity suppresses phosphatidic acid accumulation and plant immunity in response to bacterial effector AvrBsT. Proc Natl Acad Sci U S A 106: 20532-20537.
24. Testerink C, Munnik T, (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62: 2349-2361.
25. Kelley LA, Sternberg MJ, (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nature protocols 4: 363-371.
26. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, et al. (2012) The Pfam protein families database. Nucleic Acids Res 40: D290-301.
27. Chuong SD, Good AG, Taylor GJ, Freeman MC, Moorhead GB, et al. (2004) Large-scale identification of tubulin-binding proteins provides insight on subcellular trafficking, metabolic channeling, and signaling in plant cells. Mol Cell Proteomics 3: 970-983.
28. He X, Hou X, Shen Y, Huang Z, (2011) TaSRG, a wheat transcription factor, significantly affects salt tolerance in transgenic rice and Arabidopsis. FEBS Lett 585: 1231-1237.
29. 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. J Biol Chem 285: 19927-19934.
30. Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL, (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389.
31. Axtell MJ, Staskawicz BJ, (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
32. Gomez-Gomez L, Felix G, Boller T, (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284.
33. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
34. Mudgett MB, Staskawicz BJ, (1999) Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol Microbiol 32: 927-941.
35. Andersson MX, Kourtchenko O, Dangl JL, Mackey D, Ellerstrom M, (2006) Phospholipase-dependent signalling during the AvrRpm1- and AvrRpt2-induced disease resistance responses in Arabidopsis thaliana. Plant J 47: 947-959.
36. Pleskot R, Li J, Zarsky V, Potocky M, Staiger CJ, (2013) Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Trends Plant Sci 18: 496-504.
37. Testerink C, Dekker HL, Lim ZY, Johns MK, Holmes AB, et al. (2004) Isolation and identification of phosphatidic acid targets from plants. Plant J 39: 527-536.
38. Zhang Q, Lin F, Mao T, Nie J, Yan M, et al. (2012) Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell 24: 4555-4576.
39. Xia P, Wang Z, Liu X, Wu B, Wang J, et al. (2012) EB1 acetylation by P300/CBP-associated factor (PCAF) ensures accurate kinetochore-microtubule interactions in mitosis. Proc Natl Acad Sci U S A 109: 16564-16569.
40. Grant BJ, Gheorghe DM, Zheng W, Alonso M, Huber G, et al. (2011) Electrostatically biased binding of kinesin to microtubules. PLoS biology 9: e1001207.
41. Zimmermann D, Abdel Motaal B, Voith von Voithenberg L, Schliwa M, Okten Z, (2011) Diffusion of myosin V on microtubules: a fine-tuned interaction for which E-hooks are dispensable. PLoS One 6: e25473.
42. Currie JD, Stewman S, Schimizzi G, Slep KC, Ma A, et al. (2011) The microtubule lattice and plus-end association of Drosophila Mini spindles is spatially regulated to fine-tune microtubule dynamics. Mol Biol Cell 22: 4343-4361.
43. Kim NH, Kim BS, Hwang BK, (2013) Pepper Arginine Decarboxylase Is Required for Polyamine and gamma-Aminobutyric Acid Signaling in Cell Death and Defense Response. Plant Physiol 162: 2067-2083.
44. Szczesny R, Buttner D, Escolar L, Schulze S, Seiferth A, et al. (2010) Suppression of the AvrBs1-specific hypersensitive response by the YopJ effector homolog AvrBsT from Xanthomonas depends on a SNF1-related kinase. New Phytol 187: 1058-1074.
45. Xing S, Poirier Y, (2012) The protein acetylome and the regulation of metabolism. Trends Plant Sci 17: 423-430.
46. Jiang S, Yao J, Ma KW, Zhou H, Song J, et al. (2013) Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLoS pathogens 9: e1003715.
47. Zhou H, Lin J, Johnson A, Morgan RL, Zhong W, et al. (2011) Pseudomonas syringae type III effector HopZ1 targets a host enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell host & microbe 9: 177-186.
48. Ma W, Dong FF, 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: e209.
49. Lewis JD, Wan J, Ford R, Gong Y, Fung P, et al. (2012) Quantitative Interactor Screening with next-generation Sequencing (QIS-Seq) identifies Arabidopsis thaliana MLO2 as a target of the Pseudomonas syringae type III effector HopZ2. BMC Genomics 13: 8.
50. Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, et al. (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15: 5118-5129.
51. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, et al. (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425: 973-977.
52. Hwang IS, Kim NH, Choi DS, Hwang BK, (2012) Overexpression of Xanthomonas campestris pv. vesicatoria effector AvrBsT in Arabidopsis triggers plant cell death, disease and defense responses. Planta 236: 1191-1204.
53. Kim NH, Choi HW, Hwang BK, (2010) Xanthomonas campestris pv. vesicatoria effector AvrBsT induces cell death in pepper, but suppresses defense responses in tomato. Mol Plant Microbe Interact 23: 1069-1082.
54. Turner P, Barber C, Daniels M, (1984) Behaviour of the transposons Tn5 and Tn7 in Xanthomonas campestris pv. campestris. Mol Gen Genet 195: 101-107.
55. Bent AF, (2000) Arabidopsis in Planta Transformation. Uses, Mechanisms, and Prospects for Transformation of Other Species. Plant Physiology (Rockville) 124: 1540-1547.
56. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
57. Gleave AP, (1992) A versatile binary vector system with a T-DNA organisational structure conducive to efficient integration of cloned DNA into the plant genome. Plant Mol Biol 20: 1203-1207.
58. Rizhsky L, Shulaev V, Mittler R, (2004) Measuring programmed cell death in plants. Methods Mol Biol 282: 179-189.
59. Earley KW, Haag JR, Pontes O, Opper K, Juehne T, et al. (2006) Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 45: 616-629.
60. Schneider CA, Rasband WS, Eliceiri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nature methods 9: 671-675.
61. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24: 1596-1599.