A plant growth-promoting pseudomonad is closely related to the Pseudomonas syringae complex of plant pathogens

FEMS Microbiology Ecology

Volumn 77, Issue 3, 2011, Pages 546-557

  Blakney, Andrew J C ^a   Patten, Cheryl L ^a  

^a UNIVERSITY OF NEW BRUNSWICK   (Canada)

Author keywords

16S rRNA gene sequence; Multilocus sequence typing (MLST); Plant growth promoting rhizobacteria (PGPR); Pseudomonas; Type III secretion system genes

Indexed keywords

BACTERIUM; CANOLA; FRUIT; GENETIC ANALYSIS; HYBRIDIZATION; MUTUALISM; PHYLOGENETICS; SECRETION; TOBACCO; VIRULENCE;

ARTICLE; BRASSICA; CLASSIFICATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; PLANT DISEASE; PSEUDOMONAS SYRINGAE; TOBACCO; TOMATO; VIRULENCE;

BRASSICA; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT DISEASES; PSEUDOMONAS SYRINGAE; TOBACCO; VIRULENCE;

BRASSICA NAPUS; BRASSICA NAPUS VAR. NAPUS; LYCOPERSICON ESCULENTUM; NICOTIANA TABACUM; PSEUDOMONAS; PSEUDOMONAS PUTIDA; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. SYRINGAE; RHIZOBIALES; RHIZOBIUM;

EID: 79961169074     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2011.01136.x     Document Type: Article

References (81)

1. Acinas SG, Marcelino LA, Klepac-Ceraj V & Polz MF (2004) Divergence and redundancy of 16S rRNA sequences in genomes with multiple rrn operons. J Bacteriol 186: 2629-2635.
2. Alfano JR & Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42: 385-414.
3. Almeida NF, Yan S, Cai R et al. (2010) PAMDB, a multilocus sequence typing and analysis database and website for plant-associated microbes. Phytopathology 100: 208-215.
4. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
5. Anisimova M & Gascuel O (2006) Approximate likelihood ratio test for branchs: a fast, accurate and powerful alternative. Syst Biol 55: 539-552.
6. Anzai Y, Kim H, Park J, Wakabayashi H & Oyaizu H (2000) Phylogenetic affiliation of the pseudomonads based on 16S rRNA sequence. Int J Syst Evol Micr 50: 1563-1589.
7. Arnold DL, Jackson RW, Fillingham AJ, Goss SC, Taylor JD, Mansfield JW & Vivian A (2001) Highly conserved sequences flank avirulence genes: isolation of novel avirulence genes from Pseudomonas syringae pv. pisi. Microbiology 147: 1171-1182.
8. Baker GC, Smith JJ & Cowan DA (2003) Review and re-analysis of domain-specific 16S primers. J Microbiol Meth 55: 541-555.
9. Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J & Wheeler DS (2007) GenBank. Nucleic Acids Res 36: D25-D30.
10. Buell CR, Joardar V, Lindeberg M et al. (2003) The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. P Natl Acad Sci USA 100: 10181-10186.
11. Caron M, Patten CL & Ghosh S (1995) Effects of plant growth promoting rhizobacteria Pseudomonas putida GR12-2 on the physiology of canola roots. Plant Growth Regul Soc Am 7: 18-20.
12. Case RJ, Boucher Y, Dahllöf I, Holmström C, Doolittle WF & Kjelleberg S (2007) Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl Environ Microb 73: 278-288.
13. Chen Z, Agnew JL, Cohen JD, He P, Shan L, Sheen J & Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. P Natl Acad Sci USA 104: 20131-20136.
14. Chisholm ST, Coaker G, Day B & Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124: 803-814.
15. Clark CR, Cai R, Studholme DJ, Guttman DS & Vinatzer BA (2010) Pseudomonas syringae strains naturally lacking the classical P. syringaehrp/hrc locus are common leaf colonizers equipped with an atypical type III secretion system. Mol Plant Microbe In 23: 198-210.
16. Cuppels DA (1986) Generation and characterization of Tn5 insertion mutations in Pseudomonas syringae pv. tomato Appl Environ Microb 51: 323-327.
17. Dahllöf I, Baillie H & Kjelleberg S (2000) rpoB-based microbial community analysis avoids limitations inherent in 16S rRNA gene intraspecies heterogeneity. Appl Environ Microb 66: 3376-3380.
18. Feil H, Feil WS, Chain P et al. (2005) Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. P Natl Acad Sci USA 102: 11064-11069.
19. Felsenstein J (1985) Confidence limits on phylogenies: an approach using bootstraps. Evolution 39: 783-791.
20. 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. Mol Plant Pathol 10: 837-842.
21. Frapolli M, Défago G & Moënne-Loccoz Y (2007) Mulitlocus sequence analysis of biocontrol fluorescent Pseudomonas spp. producing the antifungal compound 2, 4-diacetylphloroglucinol. Environ Microbiol 9: 1939-1955.
22. Frey B, Pesaro M, Rüdt A & Widmer F (2008) Resilience of the rhizosphere Pseudomonas and ammonia-oxidizing bacterial populations during phytoextraction of heavy metal polluted soil with poplar. Environ Microbiol 10: 1433-1449.
23. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41: 109-117.
24. Glick BR, Jacobson CB, Schwarze MMK & Pasternak JJ (1994) 1-Aminocyclopropane-1- carboxylic acid deaminase mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 do not stimulate canola root elongation. Can J Microbiol 40: 911-915.
25. Glick BR, Liu C, Ghosh S & Dumbroff EB (1997) The effect of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 on the development of canola seedlings subjected to various stresses. Soil Biol Biochem 29: 1233-1239.
26. Gropp S & Guttman DS (2004) The PCR amplification and characterization of entire Pseudomonas syringaehrp/hrc clusters. Mol Plant Pathol 5: 137-140.
27. Guindon S, Lethiec F, Duroux P & Gascuel O (2005) PHYML online - a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33: W557-W559.
28. Guttman DS, Morgan RL & Wang PW (2008) The evolution of the pseudomonads. Pseudomonas syringae Pathovars and Related Pathogens (Fatmi M'B, et al, eds), pp. 307-319. Springer Science+Business Media B.V., Dordrecht.
29. Haas D & Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3: 307-319.
30. Hall JA, Peirson D, Ghosh S & Glick BR (1996) Root elongation in various agronomic crops by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Israel J Plant Sci 44: 37-42.
31. He P, Shan L & Sheen J (2007) Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol 9: 1385-1396.
32. Hontzeas N, Richardson AO, Belimov A, Safronova V, Abu-Omar MM & Glick BR (2005) Evidence for the horizontal gene transfer of 1-aminocyclopropane-1-carboxylate deaminase genes. Appl Environ Microbiol 71: 7556-7558.
33. Hwang MSH, Morgan RL, Sarkar SF, Wang PW & Guttman DS (2005) Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl Environ Microb 71: 5182-5191.
34. Hynes RK, Leung GCT, Hirkala DLM & Nelson LM (2008) Isolation, selection, and characterization of beneficial rhizobacteria from pea, lentil, and chickpea grown in western Canada. Can J Microbiol 54: 248-258.
35. Jamir Y, Guo M, Oh H, Petnicki-Ocwieja T, Chen S, Tang X, Dickman MB, Collmer A & Alfano JR (2004) Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J 37: 554-565.
36. Jelenska J, Yao N, Vinatzer BA, Wright CM, Brodsky JL & Greenberg JT (2007) A J domain virulence effector of Pseudomonas syringae remodels host chloroplasts and suppresses defenses. Curr Biol 17: 499-508.
37. Jin Q, Thilmony R, Zwiesler-Vollick J & He S (2003) Type III protein secretion in Pseudomonas syringae. Microbes Infect 5: 301-331.
38. Jones JDG & Dangl JL (2006) The plant immune system. Nature 444: 323-329.
39. Kim MG, Kim SY, Kim WY, Mackey D & Lee SY (2008) Responses of Arabidopsis thaliana to challenge by Pseudomonas syringae. Mol Cells 25: 323-331.
40. Kumar S, Nei M, Dudley J & Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9: 299-306.
41. Kvitko BH, Park DH, Velásquez 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 efffector genes reveal functional overlap among effectors. PLoS Pathog 5: 1-15.
42. Larkin MA, Blackshields G, Brown NP et al. (2007) ClustalW and ClustalX version 2. Bioinformatics 23: 2947-2948.
43. Lifshitz R, Kloepper JW, Kozlowski M, Simonson C, Carlson J, Tipping EM & Zaleska I (1987) Growth promotion of canola (Rapeseed) seedlings by a strain of Pseudomonas putida under gnotobiotic conditions. Can J Microbiol 33: 390-395.
44. Lin NC & Martin GB (2007) Pto- and Prf-mediated recognition of AvrPto and AvrPtoB restricts the ability of diverse Pseudomonas syringae pathovars to infect tomato. Mol Plant Microbe In 20: 806-815.
45. Lindeberg M, Cunnac S & Collmer A (2009) The evolution of Pseudomonas syringae host specificity and type III effector repertoires. Mol Plant Pathol 10: 767-775.
46. Loper JE & Lindow SE (1987) Lack of evidence for in situ fluorescent pigment production by Pseudomonas syringae pv. syringae on bean leaf surfaces. Phytopathology 77: 1449-1454.
47. Lytvynenko T, Zaetz I, Voznyuk T et al. (2006) A rationally assembled microbial community for growing Tagetes patula L. in a lunar greenhouse. Res Microbiol 157: 87-92.
48. 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 Genet 2: 2131-2142.
49. Maiden MCJ (2006) Multilocus sequence typing of bacteria. Annu Rev Microbiol 60: 561-588.
50. Mayak S, Tirosh T & Glick BR (1999) Effect of wild-type and mutant plant growth promoting rhizobacteria on the rooting of mung bean cuttings. J Plant Growth Regul 18: 49-53.
51. Mazurier S, Lemunier M, Siblot S, Mougel C & Lemanceau P (2004) Distribution and diversity of of type III secretion system-like genes in saprophytic and phytopathogenic fluorescent pseudomonads. FEMS Microbiol Ecol 49: 455-467.
52. McCann HC & Guttman DS (2008) Evolution of the type III secretion system and its effectors in plant-microbe interactions. New Phytol 177: 33-47.
53. Meyer AF, Lipson DA, Martin AP, Schadt CW & Schmidt SK (2004) Molecular and metabolic characterization of cold-tolerant alpine soil Pseudomonas sensu stricto. Appl Environ Microb 70: 483-489.
54. 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. J Bacteriol 190: 2858-2870.
55. Morris CE, Sands DC, Vinatzer BA, Glaux C, Guilbaud C, Buffière A, Yan S, Dominguez H & Thompson BM (2008) The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J 2: 321-334.
56. Mulet M, Lalucat J & García-Valdés E (2010) DNA sequence-analysis of the Pseudomonas species. Environ Microbiol 12: 1513-1530.
57. Mummey DL & Stahl PD (2004) Analysis of soil whole- and inner-microaggregate bacterial communities. Microb Ecol 48: 41-50.
58. Patten CL & Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microb 68: 3795-3801.
59. Posada D & Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817-818.
60. Reed MLE, Warner BG & Glick BR (2005) Plant growth-promoting bacteria facilitate the growth of the common reed Phragmites australis in the presence of copper or polycyclic aromatic hydrocarbons. Curr Microbiol 51: 425-429.
61. Rezzonico F, Défago G & Moënne-Loccoz Y (2004) Comparison of ATPase-encoding type III secretion system hrcN genes in biocontrol fluorescent Pseudomonads and in phytopathogenic proteobacteria. Appl Environ Microb 70: 5119-5131.
62. Ronquist F & Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
63. Sambrook K, Fritsch EF & Maniatis T (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
64. Santos SR & Ochman H (2004) Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ Microbiol 6: 754-759.
65. Sarkar SF & Guttman DS (2004) Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microb 70: 1999-2012.
66. Sawada H, Kanaya S, Tsuda M, Suzuki F, Azegami K & Saitou N (2002) A phylogenomic study of the OCTase genes in Pseudomonas syringae pathovars: the horizontal transfer of the argK-tox cluster and the evolutionary history of OCTase genes on their genomes. J Mol Evol 54: 437-457.
67. Schechter LM, Roberts KA, Jamir Y, Alfano JR & Collmer A (2004) Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a cya translocation reporter. J Bacteriol 186: 543-555.
68. Shan L, He P & Sheen J (2007) Endless hide-and-seek: dynamic co-evolution in plant-bacterium warfare. J Integr Plant Biol 49: 105-111.
69. Smit E, Leeflang P & Wernars K (1997) Detection of shifts in microbial community structure and diversity in soil caused by copper contamination using amplified ribosomal DNA restriction analysis. FEMS Microbiol Ecol 23: 249-261.
70. Staden R (1996) The Staden sequence analysis package. Mol Biotechnol 5: 233-241.
71. Stavrinides J, McCann HC & Guttman DS (2008) Host-pathogen interplay and the evolution of bacterial effectors. Cell Microbiol 10: 285-292.
72. Stuart A, Ord JK & Arnold S (1999) Kendall's Advanced Theory of Statistics. Oxford University Press, New York.
73. Vinatzer BA, Teitzel GM, Lee MW, 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. Mol Microbiol 62: 26-44.
74. Völksch B, Nüske J & May R (1996) Characterization of two epiphytic bacteria from soybean leaves with antagonistic activities against Pseudomonas syringae pv. glycinae J Basic Microbiol 36: 453-462.
75. Walsh DA, Bapteste E, Kamekura M & Doolittle WF (2004) Evolution of the RNA polymerase B9 subunit gene (rpoB9) in Halobacteriales: a complementary molecular marker to the SSU rRNA gene. Mol Biol Evol 21: 2340-2351.
76. Webster G, Newberry CJ, Fry JC & Weightman AJ (2003) Assessment of bacterial community structure in the deep sub-seafloor biosphere by 16S rDNA-based techniques: a cautionary tale. J Microbiol Meth 55: 155-164.
77. Wei CH, Kvitko BH, Shimizu R, Crabill E, Alfano JR, Lin NC & Martin GB (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 J 51: 32-46.
78. Xie H, Pasternak JJ & Glick BR (1996) Isolation and characterization of mutants of the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2 that overproduce indoleacetic acid. Curr Microbiol 32: 67-71.
79. Yamamoto S, Kasai H, Arnold DL, Jackson RW, Vivian A & Harayama S (2000) Phylogeny of the genus Pseudomonas: intrageneric structure reconstructed from the nucleotide sequences of gyrB and rpoD genes. Microbiol 146: 2385-2394.
80. 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. Appl Environ Microb 74: 3171-3181.
81. Yanisch-Perron C, Vieira J & Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33: 103-119.