HopAS1 recognition significantly contributes to Arabidopsis nonhost resistance to Pseudomonas syringae pathogens

New Phytologist

Volumn 193, Issue 1, 2012, Pages 58-66

  Sohn, Kee Hoon ^a   Saucet, Simon B ^a   Clarke, Christopher R ^b   Vinatzer, Boris A ^b   O'Brien, Heath E ^c   Guttman, David S ^c   Jones, Jonathan D G ^a  

^a SAINSBURY LABORATORY   (United Kingdom)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Arabidopsis; Effector triggered immunity; Nonhost resistance; Pseudomonas; Type III effector

Indexed keywords

BACTERIAL PROTEIN;

BACTERIUM; DICOTYLEDON; DISEASE RESISTANCE; FRUIT; HOST-PATHOGEN INTERACTION; IMMUNITY; MOLECULAR ANALYSIS;

ALLELE; ARABIDOPSIS; ARTICLE; DISEASE RESISTANCE; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; MUTATION; PATHOGENICITY; PLANT IMMUNITY; PSEUDOMONAS SYRINGAE; TOMATO; VIRULENCE;

ALLELES; ARABIDOPSIS; BACTERIAL PROTEINS; DISEASE RESISTANCE; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MUTATION; PLANT IMMUNITY; PSEUDOMONAS SYRINGAE; VIRULENCE;

ARABIDOPSIS; LYCOPERSICON ESCULENTUM; PSEUDOMONAS; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TOMATO; SOLANUM;

EID: 82955213433     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2011.03950.x     Document Type: Article

References (42)

1. Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ, Condon B, Liu H, Viana CJ, Warren A, Evans C et al. 2009. 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 22: 52-62.
2. Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ. 1994. RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance genes. Science 265: 1856-1860.
3. Bittner-Eddy PD, Beynon JL. 2001. The Arabidopsis downy mildew resistance gene, RPP13-Nd, functions independently of NDR1 and EDS1 and does not require the accumulation of salicylic acid. Molecular Plant-Microbe Interactions 14: 416-421.
4. Brooks DM, Hernandez-Guzman G, Kloek AP, Alarcon-Chaidez F, Sreedharan A, Rangaswamy V, Penaloza-Vazquez A, Bender CL, Kunkel BN. 2004. Identification and characterization of a well-defined series of coronatine biosynthetic mutants of Pseudomonas syringae pv. tomato DC3000. Molecular Plant-Microbe Interactions 17: 162-174.
5. Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proceedings of the National Academy of Sciences, USA 100: 10181-10186.
6. Bull CT, Manceau C, Lydon J, Kong H, Vinatzer BA, Fischer-Le Saux M. 2010. Pseudomonas cannabina pv. cannabina pv. nov., and Pseudomonas cannabina pv. alisalensis (Cintas Koike and Bull, 2000) comb. nov., are members of the emended species Pseudomonas cannabina (ex Sutic & Dowson 1959) Gardan, Shafik, Belouin, Brosch, Grimont & Grimont 1999. Systematic and Applied Microbiology 33: 105-115.
7. Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16: 735-743.
8. Debener T, Lehnackers H, Arnold M, Dangl JL. 1991. Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate. Plant Journal 1: 289-302.
9. Fan J, Crooks C, Creissen G, Hill L, Fairhurst S, Doerner P, Lamb C. 2011. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science 331: 1185-1188.
10. Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, Copeland A, Lykidis A, Trong S, Nolan M, Goltsman E et al. 2005. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proceedings of the National Academy of Sciences, USA 102: 11064-11069.
11. Ferrante P, Clarke CR, Cavanaugh KA, Michelmore RW, Buonaurio R, Vinatzer BA. 2009. Contributions of the effector gene hopQ1-1 to differences in host range between Pseudomonas syringae pv. phaseolicola and P. syringae pv. tabaci. Molecular Plant Pathology 10: 837-842.
12. Ham JH, Kim MG, Lee SY, Mackey D. 2007. Layered basal defenses underlie non-host resistance of Arabidopsis to Pseudomonas syringae pv. phaseolicola. Plant Journal 51: 604-616.
13. Hirano SS, Upper CD. 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae - a pathogen, ice nucleus, and epiphyte. Microbiology and Molecular Biology Reviews 64: 624-653.
14. Holub EB, Cooper A. 2004. Matrix, reinvention in plants: how genetics is unveiling secrets of non-host disease resistance. Trends in Plant Science 9: 211-214.
15. Jones JD, Dangl JL. 2006. The plant immune system. Nature 444: 323-329.
16. Kearney B, Staskawicz BJ. 1990. Widespread distribution and fitness contribution of Xanthomonas campestris avirulence gene avrBs2. Nature 346: 385-386.
17. Keen NT, Tamaki S, Kobayashi D, Trollinger D. 1988. Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70: 191-197.
18. Kobayashi DY, Tamaki SJ, Keen NT. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proceedings of the National Academy of Sciences, USA 86: 157-161.
19. Lacombe S, Rougon-Cardoso A, Sherwood E, Peeters N, Dahlbeck D, van Esse HP, Smoker M, Rallapalli G, Thomma BP, Staskawicz B et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnology 28: 365-369.
20. 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.
21. McDowell JM, Cuzick A, Can C, Beynon J, Dangl JL, Holub EB. 2000. Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1 and salicylic acid accumulation. Plant Journal 22: 523-529.
22. McNellis TW, Mudgett MB, Li K, Aoyama T, Horvath D, Chua NH, Staskawicz BJ. 1998. Glucocorticoid-inducible expression of a bacterial avirulence gene in transgenic Arabidopsis induces hypersensitive cell death. Plant Journal 14: 247-257.
23. Mindrinos M, Katagiri F, Yu G-L, Ausubel FM. 1994. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78: 1089-1099.
24. Mohr TJ, Liu H, Yan S, Morris CE, Castillo JA, Jelenska J, Vinatzer BA. 2008. Naturally occurring nonpathogenic isolates of the plant pathogen Pseudomonas syringae lack a type III secretion system and effector gene orthologues. Journal of Bacteriology 190: 2858-2870.
25. Mudgett MB, Staskawicz BJ. 1999. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Molecular Microbiology 32: 927-941.
26. Muskett PR, Kahn K, Austin MJ, Moisan LJ, Sadanandom A, Shirasu K, Jones JD, Parker JE. 2002. Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defenses against multiple pathogens. Plant Cell 14: 979-992.
27. Nurnberger T, Lipka V. 2005. Non-host resistance in plants: new insights into an old phenomenon. Molecular Plant Pathology 6: 335-345.
28. Rohmer L, Kjemtrup S, Marchesini P, Dangl JL. 2003. Nucleotide sequence, functional characterization and evolution of pFKN, a virulence plasmid in Pseudomonas syringae pathovar maculicola. Molecular Microbiology 47: 1545-1562.
29. Schulze-Lefert P, Panstruga R. 2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends in Plant Science 16: 117-125.
30. Segonzac C, Zipfel C. 2011. Activation of plant pattern-recognition receptors by bacteria. Current Opinion in Microbiology 14: 54-61.
31. Sohn KH, Lei R, Nemri A, Jones JD. 2007. The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. Plant Cell 19: 4077-4090.
32. Sohn KH, Zhang Y, Jones JD. 2009. The Pseudomonas syringae effector protein, AvrRPS4, requires in planta processing and the KRVY domain to function. Plant Journal 57: 1079-1091.
33. Staskawicz B, Dahlbeck D, Keen N, Napoli C. 1987. Molecular characterization of cloned avirulence genes from race 0 and race 1 of Pseudomonas syringae pv. glycinea. Journal of Bacteriology 169: 5789-5794.
34. Swingle B, Thete D, Moll M, Myers CR, Schneider DJ, Cartinhour S. 2008. Characterization of the PvdS-regulated promoter motif in Pseudomonas syringae pv. tomato DC3000 reveals regulon members and insights regarding PvdS function in other pseudomonads. Molecular Microbiology 68: 871-889.
35. Thomas WJ, Thireault CA, Kimbrel JA, Chang JH. 2009. Recombineering and stable integration of the Pseudomonas syringae pv. syringae 61 hrp/hrc cluster into the genome of the soil bacterium Pseudomonas fluorescens Pf0-1. Plant Journal 60: 919-928.
36. Tornero P, Merritt P, Sadanandom A, Shirasu K, Innes RW, Dangl JL. 2002. RAR1 and NDR1 contribute quantitatively to disease resistance in Arabidopsis, and their relative contributions are dependent on the R gene assayed. Plant Cell 14: 1005-1015.
37. Wei CF, Kvitko BH, Shimizu R, Crabill E, Alfano JR, Lin NC, Martin GB, Huang HC, Collmer A. 2007. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant Journal 51: 32-46.
38. Whalen MC, Innes RW, Bent AF, Staskawicz BJ. 1991. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean. Plant Cell 3: 49-59.
39. Wroblewski T, Caldwell KS, Piskurewicz U, Cavanaugh KA, Xu H, Kozik A, Ochoa O, McHale LK, Lahre K, Jelenska J et al. 2009. Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiology 150: 1733-1749.
40. Yan S, Liu H, Mohr TJ, Jenrette J, Chiodini R, Zaccardelli M, Setubal JC, Vinatzer BA. 2008. Role of recombination in the evolution of the model plant pathogen Pseudomonas syringae pv. tomato DC3000, a very atypical tomato strain. Applied and Environmental Microbiology 74: 3171-3181.
41. Zhang J, Lu H, Li X, Li Y, Cui H, Wen CK, Tang X, Su Z, Zhou JM. 2010. Effector-triggered and pathogen-associated molecular pattern-triggered immunity differentially contribute to basal resistance to Pseudomonas syringae. Molecular Plant-Microbe Interactions 23: 940-948.
42. 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.