Recovery of nonpathogenic mutant bacteria from tumors caused by several Agrobacterium tumefaciens strains: A frequent event?

Applied and Environmental Microbiology

Volumn 75, Issue 20, 2009, Pages 6504-6514

  Llop, Pablo ^a   Murillo, Jesús ^b   Lastra, Beatriz ^c   López, María M ^a  

^a INSTITUTO VALENCIANO DE INVESTIGACIONES AGRARIAS IVIA   (Spain)

^b PUBLIC UNIVERSITY OF NAVARRE   (Spain)

^c UNIVERSITY OF SANTIAGO DE COMPOSTELA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AGROBACTERIA; AGROBACTERIUM TUMEFACIENS STRAIN; BACTERIAL STRAINS; HIGH VARIABILITY; MUTANT BACTERIA; NONPATHOGENIC STRAINS; PLANT HOSTS; PLASMID PROFILE; PREFERENTIAL GROWTH; RANDOMLY AMPLIFIED POLYMORPHIC DNA; TRANSFERRED DNAS; TUMEFACIENS;

BACTERIOLOGY; DNA; FRUITS; GENES; NUCLEIC ACIDS; ONCOLOGY; PLANTS (BOTANY); TUMORS;

STRAIN;

DNA; ENDOPHYTE; FRUIT; GENE EXPRESSION; GENOTYPE; INOCULATION; MICROBIAL COMMUNITY; MUTAGENICITY; PATHOGENICITY; PLASMID; POLYMORPHISM; TUMOR;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CLONE; CONTROLLED STUDY; ECOLOGICAL NICHE; ENDOPHYTE; GENE INSERTION; IAAM GENE; INOCULATION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPPER; PLANT TUMOR; PLASMID; RANDOM AMPLIFIED POLYMORPHIC DNA; REPRODUCIBILITY; RHIZOBIUM RADIOBACTER; TOMATO;

BASE SEQUENCE; DNA PRIMERS; DNA, BACTERIAL; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; MUTATION; PLANT DISEASES; PLASMIDS; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; REPRODUCIBILITY OF RESULTS; RHIZOBIUM RADIOBACTER; VIRULENCE;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM;

EID: 70349921621     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01867-08     Document Type: Article

References (57)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Anderson, A. R., and L. W. Moore. 1979. Host specificity in the genus Agrobacterium. Phytopathology 69:320-323.
3. Bélanger, C., M. L. Canfield, L. W. Moore, and P. Dion. 1993. Detection of avirulent mutants of Agrobacterium tumefaciens in crown-gall tumors produced in vitro. p. 97-101. In E. W. Nester and D. P. S. Verma (ed.), Advances in molecular genetics of plant microbe interactions, vol.2. Kluwer Academic Publishers, Dordrecht, The Netherlands.
4. Bélanger, C., M. L. Canfield, L. W. Moore, and P. Dion. 1995. Genetic analysis of nonpathogenic Agrobacterium tumefaciens mutants arising in crown gall tumors. J. Bacteriol. 177:3752-3757.
5. Bouzar, H., D. Ouadah, Z. Krimi, J. B. Jones, M. Trovato, A. Petit, and Y. Dessaux. 1993. Correlative association between resident plasmids and the host chromosome in a diverse Agrobacterium soil population. Appl. Environ. Microbiol. 59:1310-1317.
6. Canfield, M. L., and L. W. Moore. 1991. Isolation and characterization of opine-utilizing strains of Agrobacterium tumefaciens and fluorescent strains of Pseudomonas spp. from rootstocks of Malus. Phytopathology 81:440-443.
7. Christie, P. J. 1997. Agrobacterium tumefaciens T-complex apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J. Bacteriol. 179:3085-3094.
8. De Bruijn, F. J. 1992. Use of repetitive (repetitive extragenic palindromic and enterobacterial repetitive intergeneric consensus) sequences and the polymerase chain reaction to fingerprint the genomes of Rhizobium meliloti isolates and other soil bacteria. Appl. Environ. Microbiol. 58:2180-2187.
9. De Cleene, M., and J. Ley. 1976. The host range of crown gall. Bot. Rev. 42:389-466.
10. Dion, P., C. Belanger, C. Marquis, W. Ream, and S. B. Gelvin. 1996. Ecological significance of avirulence in Agrobacterium, p. 44-58. In W. Ream and S. B. Gelvin (ed.), Crown gall: advances in understanding interkingdom gene transfer. APS Press, St. Paul, MN.
11. Duncan, A. V., H. W. Stokes, and G. Daggard. 1992. Genetic exchange in natural microbial communities, p. 383-429. In K. C. Marshall (ed.), Advances in microbial ecology, vol.12. Plenum Press, New York, NY.
12. Flores, M., P. Mavingui, X. Perret, W. J. Broughton, D. Romero, G. Hernández, G. Dávila, and R. Palacios. 2000. Prediction, identification, and artificial selection of DNA rearrangements in Rhizobium: toward a natural genomic design. Proc. Natl. Acad. Sci. USA 97:9138-9143.
13. Fortin, C., E. W. Nester, and P. Dion. 1992. Growth inhibition and loss of virulence in cultures of Agrobacterium tumefaciens treated with acetosyringone. J. Bacteriol. 174:5676-5685.
14. Fortin, C., C. Marquis, E. W. Nester, and P. Dion. 1993. Dynamic structure of Agrobacterium tumefaciens Ti plasmids. J. Bacteriol. 175:4790-4799.
15. Goodner, B., G. Hinkle, S. Gattung, N. Miller, M. Blanchard, B. Qurollo, B. S. Goldman, Y. Cao, M. Askenazi, C. Halling, L. Mullin, K. Houmiel, J. Gordon, M. Vaudin, O. Iartchouk, A. Epp, F. Liu, C. Wollam, M. Allinger, D. Doughty, C. Scott, C. Lappas, B. Markelz, C. Flanagan, C. Crowell, J. Gurson, C. Lomo, C. Sear, G. Strub, C. Cielo, and S. Slater. 2001. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323-2328.
16. Haas, J. H., L. W. Moore, W. Ream, and S. Manulis. 1995. Universal PCR primers for detection of phytopathogenic Agrobacterium strains. Appl. Environ. Microbiol. 61:2879-2884.
17. Hayman, G. T., and S. K. Farrand. 1988. Characterization and mapping of the agrocinopine-agrocin 84 locus on the nopaline Ti plasmid pTiC58. J. Bacteriol. 170:1759-1767.
18. Kado, C. I. 1991. Molecular mechanisms of crown gall tumorigenesis. Crit. Rev. Plant Sci. 10:1-32.
19. Kerr, A. 1969. Transfer of virulence between isolates of Agrobacterium. Nature 223:1175-1176.
20. Krimi, Z., A. Petit, C. Mougel, Y. Dessaux, and X. Nesme. 2002. Seasonal fluctuations and long-term persistence of pathogenic populations of Agrobacterium spp. in soils. Appl. Environ. Microbiol. 68:3358-3365.
21. LaPointe, G., C. S. Nautiyal, W. S. Chilton, S. K. Farrand, and P. Dion. 1992. Spontaneous mutation conferring the ability to catabolize mannopine in Agrobacterium tumefaciens. J. Bacteriol. 174:2631-2639.
22. Lelliot, R. A., and D. E. Stead. 1987. Methods for the diagnosis of bacterial diseases of plants, p. 216. In T. F. Preece (ed.), Methods in plant pathology, vol.2. Blackwell Scientific Publications, Oxford, United Kingdom.
23. Leloup, L., E. M. Lai, and C. I. Kado. 2002. Identification of a chromosomal tra-like region in Agrobacterium tumefaciens. Mol. Genet. Genomics 267:115-123.
24. Llop, P., B. Lastra, H. Marsal, J. Murillo, and M. M. López. 2003. Tracking Agrobacterium strains by a RAPD system to identify single colonies from plant tumors. Eur. J. Plant Pathol. 109:381-389.
25. Louws, F. J., D. W. Fulbright, C. T. Stephens, and F. J. De Bruijn. 1994. Specific genome fingerprints of phytopathogenic Xanthomonas and Pseudomonas pathovars and strains generated with repetitive sequences and PCR. Appl. Environ. Microbiol. 60:2286-2295.
26. Manahan, S. H., and T. R. Steck. 1997. The viable but nonculturable state in Agrobacterium tumefaciens and Rhizobium meliloti. FEMS Microbiol. Ecol. 22:29-37.
27. Martí, R., J. Cubero, A. Daza, J. Piquer, C. I. Salcedo, C. Morente, and M. M. López. 1999. Evidence of migration and endophytic presence of Agrobacterium tumefaciens in rose plants. Eur. J. Plant Pathol. 105:39-50.
28. Mavingui, P., M. Flores, X. Guo, G. Dávila, X. Perret, W. Broughton, and R. Palacios. 2002. Dynamics of genome architecture in Rhizobium sp. strain NGR234. J. Bacteriol. 184:171-176.
29. McManus, P. S., V. O. Stockwell, G. W. Sundin, and A. L. Jones. 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443-465.
30. Melchers, L. S., and P. J. J. Hooykaas. 1987. Virulence of Agrobacterium. Oxf. Surv. Plant Mol. Cell Biol. 4:167.
31. Michel, M. F., A. C. Miranda, C. Depierreux, L. Otten, F. Delmotte, and L. Jouanin. 1990. Identification of different Agrobacterium strains isolated from the same forest nursery. Appl. Environ. Microbiol. 56:3537-3545.
32. Moore, L. W., and D. A. Cooksey. 1981. Biology of Agrobacterium tumefaciens: plant interactions, p. 15-46. In K. L. Giles and A. C. Atherly (ed.), Biology of Rhizobiaceae. Academic Press, New York, NY.
33. Moore, L. W., and M. Canfield. 1996. Biology of Agrobacterium and management of crown gall disease, p. 153-191. In R. Hall (ed.), Principles and practice of managing soilborne plant pathogens. APS Press, St. Paul, MN.
34. Morris, J. W., and R. O. Morris. 1990. Identification of an Agrobacterium tumefaciens virulence gene inducer from the pinaceous gymnosperm Pseudotsuga menziesii. Proc. Natl. Acad. Sci. USA 87:3614-3618. (Pubitemid 20173687)
35. Mougel, C. 2000. Structure génétique des populations d'Agrobacterium spp.: effet sélectif de la plante et implication dans la diffusion conjugative du plasmide Ti. Ph.D. thesis. University of Lyon, France.
36. Mougel, C., B. Cournoyer, and X. Nesme. 2001. Novel tellurite-amended media and specific chromosomal and Ti plasmid probes for direct analysis of soil populations of Agrobacterium biovars 1 and 2. Appl. Environ. Microbiol. 67:65-74.
37. Nair, G. R., L. Zhenying, and A. N. Binns. 2003. Reexamining the role of the accessory plasmid pAtC58 in the virulence of Agrobacterium tumefaciens strain C58. Plant Physiol. 133:989-999.
38. Nesme, X., F. Michel, and B. Digat. 1987. Population heterogeneity of Agrobacterium tumefaciens in galls of Populus L. from a single nursery. Appl. Environ. Microbiol. 53:655-659.
39. Nesme, X., M. C. Leclerc, and R. Bardin. 1989. PCR detection of an original endosymbiont: the Ti plasmid of Agrobacterium tumefaciens, p. 47-50. In P. Nardon, V. Gianinazzi-Peason, A. M. Greines, L. Margulis, and D. C. Smith (ed.), Endocytobiology IV. Institut National de la Recherche Agronomique, Paris, France.
40. Paulus, F., J. Canaday, F. Vincent, G. Bonnard, C. Kares, and L. Otten. 1991. Sequence of the iaa and ipt region of different Agrobacterium tumefaciens biotype III octopine strains. Reconstruction of octopine Ti plasmid evolution. Plant Mol. Biol. 16:601-614.
41. Reed, K. C., and D. A. Mann. 1985. Rapid transfer of DNA from agarose gels to nylon membranes. Nucleic Acids Res. 25:7207-7221.
42. Schroth, M. N., J. P. Thompson, and D. C. Hildebrand. 1965. Isolation of A. tumefaciens-A. radiobacter group from the soil. Phytopathology 55:645-647.
43. Sheng, J., and V. Citovsky. 1996. Agrobacterium-plant cell DNA transport: have virulence proteins, will travel. Plant Cell 8:1699-1710.
44. Soberón-Chávez, G., R. Nájera, H. Olivera, and L. Segovia. 1986. Genetic rearrangements of a Rhizobium phaseoli symbiotic plasmid. J. Bacteriol. 167:487-491.
45. Stachel, S. E., and P. C. Zambryski. 1986. virA and virG control the plant-induced activation of the T-DNA transfer process of A. tumefaciens. Cell 46:325-333.
46. Stockwell, V. O., L. W. Moore, and J. E. Loper. 1993. Fate of Agrobacterium radiobacter K84 in the environment. Appl. Environ. Microbiol. 59:2112-2120.
47. Sullivan, J. T., and C. W. Ronson. 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proc. Natl. Acad. Sci. USA 95:5145-5149.
48. Sundin, G. W., and M. R. Weigand. 2007. The microbiology of mutability. FEMS Microbiol. Lett. 277:11-20.
49. Surette, M. A., A. V. Sturz, R. R. Lada, and J. Nowak. 2003. Bacterial endophytes in processing carrots (Daucus carota L. var. sativus): their localization, population density, biodiversity and their effects on plant growth. Plant Soil 253:381-390.
50. Thomas, P., S. Kumari, G. K. Swarna, and T. K. S. Gowda. 2007. Papaya shoot tip associated endophytic bacteria isolated from in vitro cultures and host-endophyte interaction in vitro and in vivo. Can. J. Microbiol. 53:380-390.
51. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
52. Vanderleyden, J., J. Desair, C. De Meirsman, K. Michiels, A. P. Van Gool, M. D. Chilton, and G. C. Jen. 1986. Nucleotide sequence of an insertion sequence (IS) element identified in the T-DNA region of a spontaneous variant of the Ti-plasmid pTiT37. Nucleic Acids Res. 14:6699-6709.
53. Wang, L. L., E. T. Wang, J. Liu, Y. Li, and W. X. Chen. 2006. Endophytic occupation of root nodules and roots of Melilotus dentatus by Agrobacterium tumefaciens. Microb. Ecol. 52:436-443.
54. Wood, D. W., J. C. Setubal, R. Kaul, D. E. Monks, J. P. Kitajima, V. K. Okura, Y. Zhou, L. Chen, G. E. Wood, N. F. Almeida, Jr., L. Woo, Y. Chen, I. T. Paulsen, J. A. Eisen, P. D. Karp, D. Bovee, Sr., P. Chapman, J. Clendenning, G. Deatherage, W. Gillet, C. Grant, T. Kutyavin, R. Levy, M. J. Li, E. McClelland, A. Palmieri, C. Raymond, G. Rouse, C. Saenphimmachak, Z. Wu, P. Romero, D. Gordon, S. Zhang, H. Yoo, Y. Tao, P. Biddle, M. Jung, W. Krespan, M. Perry, B. Gordon-Kamm, L. Liao, S. Kim, C. Hendrick, Z. Y. Zhao, M. Dolan, F. Chumley, S. V. Tingey, J. F. Tomb, M. P. Gordon, M. V. Olson, and E. W. Nester. 2001. The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317-2323.
55. Zhang, X., B. Kosier, and U. Priefer. 2001. Symbiotic plasmid rearrangement in Rhizobium leguminosarum bv. viciae VF39SM. J. Bacteriol. 183:2141-2144.
56. Zhou, C., Y. Yang, and A. Y. Jong. 1990. Miniprep in ten minutes. Bio- Techniques 8:172-173.
57. Zoina, A., A. Raio, R. Peluso, and A. Spasiano. 2001. Characterization of agrobacteria from weeping fig (Ficus benjamina). Plant Pathol. 50:620-627.