Two virulence determinants of type III effector AvrPto are functionally conserved in diverse Pseudomonas syringae pathovars

New Phytologist

Volumn 187, Issue 4, 2010, Pages 969-982

  Nguyen, Hanh P ^a,b   Yeam, Inhwa ^a   Angot, Aurelie ^a   Martin, Gregory B ^a,b  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

PAMP triggered immunity; Prf; Pseudomonas syringae; Pto; Tobacco; Tomato

Indexed keywords

AVRPTO PROTEIN, PSEUDOMONAS SYRINGAE; BACTERIAL PROTEIN;

AMINO ACID; BACTERIUM; DISEASE RESISTANCE; FRUIT; GENE EXPRESSION; GENOTYPE; HYPOTHESIS TESTING; IMMUNITY; PLANT DEFENSE; PROTEIN; TOBACCO; VIRULENCE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLANT DISEASE; PLANT GENE; PLANT IMMUNITY; PSEUDOMONAS SYRINGAE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TOBACCO; TOMATO;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLONING, MOLECULAR; GENES, BACTERIAL; GENES, PLANT; GENOTYPE; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PLANT DISEASES; PLANT IMMUNITY; PSEUDOMONAS SYRINGAE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TOBACCO;

LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO;

EID: 77953170391     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.03175.x     Document Type: Article

References (43)

1. Alfano JR, Collmer A. Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annual Review of Phytopathology 2004, 42:385-414.
2. Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ, Condon B, Liu H, Viana CJ, Warren A, Evans C. A draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a type III effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Molecular Plant-Microbe Interactions 2009, 22:52-62.
3. Anderson JC, Pascuzzi PE, Xiao F, Sessa G, Martin GB. Host-mediated phosphorylation of type III effector AvrPto promotes Pseudomonas virulence and avirulence in tomato. Plant Cell 2006, 18:502-514.
4. Badel JL, Shimizu R, Oh HS, Collmer A. A Pseudomonas syringae pv. tomato AvrE1/HopM1 mutant is severely reduced in growth and lesion formation in tomato. Molecular Plant-Microbe Interactions 2006, 19:99-111.
5. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF. The complete genome dequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proceedings of the National Academy of Sciences, USA 2003, 100:10181-10186.
6. Chang JH, Tobias CM, Staskawicz BJ, Michelmore RW. Functional studies of the bacterial avirulence protein AvrPto by mutational analysis. Molecular Plant-Microbe Interactions 2001, 14:451-459.
7. Chisholm ST, Dahlbeck D, Krishnamurthy N, Day B, Sjolander K, Staskawicz BJ. Molecular characterization of proteolytic cleavage sites of the Pseudomonas syringae effector AvrRpt2. Proceedings of the National Academy of Sciences, USA 2005, 102:2087-2092.
8. Chisholm ST, Coaker G, Day B, Staskawicz BJ. Host-microbe interactions: shaping the evolution of the plant immune response. Cell 2006, 124:803-814.
9. Cunnac S, Linderberg M, Collmer A. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Current Opinion in Microbiology 2009, 12:53-60.
10. Dawson JE, Šečkute J, De S, Schueler SA, Oswald AB, Nicholson LK. Elucidation of a pH-folding switch in the Pseudomonas syringae effector protein AvrPto. Proceedings of the National Academy of Sciences, USA 2009, 106:8543-8548.
11. Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR, Cartinhour S, Chatterjee AK, D'Ascenzo M, Gwinn ML, Lazarowitz SG. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. Proceedings of the National Academy of Sciences, USA 2002, 99:2275-2280.
12. He X, Anderson JC, Pozo Od O, Gu YQ, Tang X, Martin GB. Silencing of subfamily I of protein phosphatase 2a catalytic subunits results in activation of plant defense responses and localized cell death. Plant Journal 2004, 38:563-577.
13. He P, Shan L, Lin NC, Martin GB, Kemmerling B, Nurnberger T, Sheen J. Specific bacterial suppressors of Mamp signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 2006, 125:563-575.
14. Jamir Y, Guo M, Oh HS, Petnicki-Ocwieja T, Chen S, Tang X, Dickman MB, Collmer AR, Alfano J. Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant Journal 2004, 37:554-565.
15. Kvitko BH, Park DH, Velásquez AC, Wei CF, Russell AB, Martin GB, Schneider DJ, Collmer A. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathogens 2009, 5:e1000388.
16. Lin N-C, Martin GB. An AvrPto/AvrPtoB mutant of Pseudomonas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Molecular Plant-Microbe Interactions 2005, 18:43-51.
17. Lin N-C, Martin GB. Pto- and Prf-mediated recognition of AvrPto and AvrPtoB restricts the ability of diverse Pseudomonas syringae pathovars to infect tomato. Molecular Plant-Microbe Interactions 2007, 20:806-815.
18. Lin N-C, Abramovitch RB, Kim YJ, Martin GB. Diverse AvrPtoB homologs from several Pseudomonas syringae pathovars elicit Pto-dependent resistance and have similar virulence activities. Applied and Environmental Microbiology 2006, 72:702-712.
19. Lindeberg M, Myers CR, Collmer A, Schneider DJ. Roadmap to new virulence determinants in Pseudomonas syringae: insights from comparative genomics and genome organization. Molecular Plant-Microbe Interactions 2008, 21:685-700.
20. Ma W, Dong FF, Stavrinides J, Guttman DS. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLoS Genetics 2006, 2:e209.
21. Pascuzzi PE. Structure-based functional analyses of Pseudomonas type III effector protein AvrPto and evaluation of putative virulence targets in tomato 2006, PhD thesis, Cornell University, Ithaca, NY, USA
22. Reinhardt JA, Baltrus DA, Nishimura MT, Jeck WR, Jones CD, Dangl JL. De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Research 2009, 19:294-305.
23. Rohmer L, Guttman DS, Dangl JL. Diverse evolutionary mechanisms shape the type III effector virulence factor repertoire in the plant pathogen Pseudomonas syringae. Genetics 2004, 167:1341-1360.
24. Ronald PC, Salmeron JM, Carland FM, Staskawicz BJ. The cloned avirulence gene AvrPto induces disease resistance in tomato cultivars containing the Pto resistance gene. Journal of Bacteriology 1992, 174:1604-1611.
25. Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 2007, 448:370-374.
26. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual 1989, Cold Spring Harbor, NY, USA, Cold Spring Harbor Laboratory Press
27. Sarkar SF, Guttman DS. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Applied and Environmental Microbiology 2004, 70:1999-2012.
28. Sarkar SF, Gordon JS, Martin GB, Guttman DS. Comparative genomics of host-specific virulence in Pseudomonas syringae. Genetics 2006, 174:1041-1056.
29. Schechter LM, Roberts KA, Jamir Y, Alfano JR, Collmer A. Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. Journal of Bacteriology 2004, 186:543-555.
30. Scofield SR, Tobias CM, Rathjen JP, Chang JH, Lavelle DT, Michelmore RW, Staskawicz BJ. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science 1996, 274:2063-2065.
31. Shan L, He P, Zhou JM, Tang X. A cluster of mutations disrupt the avirulence but not the virulence function of AvrPto. Molecular Plant-Microbe Interactions 2000a, 13:592-598.
32. Shan L, Thara VK, Martin GB, Zhou JM, Tang X. The Pseudomonas AvrPto protein is differentially recognized by tomato and tobacco and is localized to the plant plasma membrane. Plant Cell 2000b, 12:2323-2338.
33. Shan L, He P, Li J, Heese A, Peck S, Nürnberger T, Martin GB, Sheen J. Bacterial effectors target BAK1 to disrupt Mamp receptor signaling complexes and impede plant innate immunity. Cell Host & Microbe 2008, 4:17-27.
34. Studholme DJ, Gimenez-Ibanez S, Maclean D, Dangl JL, Chang JH, Rathjen JP. A draft genome sequence and functional screen reveals the repertoire of type III secreted proteins of Pseudomonas syringae pv. tabaci 11528. BMC Genomics 2009, 10:395.
35. Tang X, Frederick RD, Zhou J, Halterman DA, Jia Y, Martin GB. Initiation of plant disease resistance by physical interaction of AvrPto and Pto kinase. Science 1996, 274:2060-2063.
36. Wulf J, Pascuzzi PE, Fahmy A, Martin GB, Nicholson LK. The solution structure of Type III effector protein AvrPto reveals conformational and dynamic features important for plant pathogenesis. Structure 2004, 12:1257-1268.
37. Xiang T, Zong N, Zou Y, Wu Y, Zhang J, Xing W, Li Y, Tang X, Zhu L, Chai J. Pseudomonas syringae effector Avrpto blocks innate immunity by targeting receptor kinases. Current Biology 2008, 18:74-80.
38. Xiao F, Giavilsco P, Martin GB. Pseudomonas Syringae type III effector AvrPtoB is phosphorylated in plant cells on serine 258 promoting its virulence activity. Journal of Biological Chemistry 2007a, 282:30737-30744.
39. Xiao F, He P, Abramovitch RB, Dawson JE, Nicholson LK, Sheen J, Martin GB. The N-terminal region of Pseudomonas type III effector AvrPtoB elicits Pto-dependent immunity and has two distinct virulence determinants. Plant Journal 2007b, 52:595-614.
40. Xing W, Zou Y, Liu Q, Liu J, Luo X, Huang Q, Chen S, Zhu L, Bi R, Hao Q. The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 2007, 449:243-247.
41. Yeam I, Nguyen HP, Martin GB. Phosphorylation of Pseudomonas syringae effector AvrPto is required for an FLS2/BAK1-independent virulence activity and recognition by tobacco. Plant Journal 2010, 61:16-24.
42. Zhou JM, Chai J. Plant pathogenic bacterial type III effectors subdue host responses. Current Opinion in Microbiology 2008, 11:179-185.
43. Zhou H, Morgan RL, Guttman DS, Ma W. Allelic variants of the Pseudomonas syringae type III effector HopZ1 are differentially recognized by plant resistance systems. Molecular Plant-Microbe Interactions 2009, 22:176-189.