Endophytic colonization and biocontrol performance of Pseudomonas fluorescensPICF7 in olive (Olea europaea L.) are determined neither by pyoverdine production nor swimming motility

Environmental Microbiology

Volumn 17, Issue 9, 2015, Pages 3139-3153

  Maldonado González, M Mercedes ^a   Schilirò, Elisabetta ^a   Prieto, Pilar ^a   Mercado Blanco, Jesús ^a  

^a INSTITUTO DE AGRICULTURA SOSTENIBLE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BIOLOGICAL CONTROL AGENT; CYSTEINE; FLII PROTEIN, BACTERIA; OLIGOPEPTIDE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATASE; PYOVERDINE; SIDEROPHORE;

ANTIBIOSIS; BIOLOGICAL CONTROL AGENT; BIOSYNTHESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; OLIVE TREE; PHENOTYPE; PHYSIOLOGY; PLANT DISEASE; PLANT ROOT; PREVENTION AND CONTROL; PSEUDOMONAS FLUORESCENS; RHIZOSPHERE; VERTICILLIUM;

ANTIBIOSIS; BACTERIAL PROTEINS; BIOLOGICAL CONTROL AGENTS; CYSTEINE; OLEA; OLIGOPEPTIDES; PHENOTYPE; PLANT DISEASES; PLANT ROOTS; PROTON-TRANSLOCATING ATPASES; PSEUDOMONAS FLUORESCENS; RHIZOSPHERE; SIDEROPHORES; VERTICILLIUM;

EID: 84927140497     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12725     Document Type: Article

References (85)

1. Ali, S., Duan, J., Charles, T.C., and Glick, B.R. (2014) A bioinformatics approach to the determination of genes involved in endophytic behavior in Burkholderia spp. J Theor Biol 343: 193-198.
2. Alit-Susanta, W.G.N., and Takikawa, Y. (2006) Phenotypic characterization of Pseudomonas fluorescens PfG32R and its spontaneous gacS mutants and biocontrol activity against bacterial wilt disease of tomato. J Gen Plant Pathol 72: 168-175.
3. Alström, S. (2001) Characteristics of bacteria from oilseed rape in relation to their biocontrol activity against Verticillium dahliae. J Phytopathol 149: 57-64.
4. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
5. Antonopoulos, D.F., Tjamos, S.E., Antoniou, P.P., Rafeletos, P., and Tjamos, E.C. (2008) Effect of Paenibacillus alvei, strain K165, on the germination of Verticillium dahliae microsclerotia in planta. Biol Control 46: 166-170.
6. Aranda, S., Montes-Borrego, M., Jiménez-Díaz, R.M., and Landa, B.B. (2011) Microbial communities associated with the root system of wild olives (Olea europaea L. subsp europaea var. sylvestris) are good reservoirs of bacteria with antagonistic potential against Verticillium dahliae. Plant Soil 343: 329-345.
7. Audenaert, K., Pattery, T., Cornelis, P., and Höfte, M. (2002) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol Plant Microbe Interact 15: 1147-1156.
8. Bacon, C.W., and Hinton, D.M. (2006) Bacterial endophytes: the endophytic niche, its occupants, and its utility. In Plant-Associated Bacteria. Gnanamanickam, S.S. (ed.). Dordrecht, The Netherlands: Springer, pp. 155-194.
9. Bais, H.P., Weir, T.L., Perry, L.G., Gilroy, S., and Vivanco, J.M. (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57: 233-266.
10. Bakker, P.A.H.M., Ran, L.X., and Mercado-Blanco, J. (2014) Rhizobacterial salicylate production provokes headaches! Plant Soil 382: 1-16.
11. Barahona, E., Navazo, A., Martínez-Granero, F., Zea-Bonilla, T., Pérez-Jiménez, R.M., Martín, M., and Rivilla, R. (2011) Pseudomonas fluorescens F113 mutant with enhanced competitive colonization ability and improved biocontrol activity against fungal root pathogens. Appl Environ Microbiol 77: 5412-5419.
12. Berg, G., Opelt, K., Zachow, C., Lottmann, J., Götz, M., Costa, R., and Smalla, K. (2006) The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol 56: 250-261.
13. 2-fixing endophyte Azoarcus sp. strain BH72. Mol Plant Microbe Interact 20: 526-533.
14. Bultreys, A. (2007) Siderotyping, a tool to characterize, classify and identify fluorescent Pseudomonas. In Microbial Siderophores. Varma, A., and Chincholkar, S. (eds). Berlin, Germany: Springer-Verlag, pp. 67-89.
15. Buysens, S., Heungens, K., Poppe, J., and Höfte, M. (1996) Involvement of pyochelin and pyoverdine in suppression of Pythium-induced damping-off of tomato by Pseudomonas aeruginosa 7NSK2. Appl Environ Microbiol 62: 865-871.
16. Caetano-Anollés, G. (1993) Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl 3: 85-92.
17. Campbell, C.L., and Madden, L.V. (1990) Introduction to Plant Disease Epidemiology. New York, NY, USA: John Wiley and Sons.
18. Capdevila, S., Martínez-Granero, F.M., Sánchez-Contreras, M., Rivilla, R., and Martín, M. (2004) Analysis of Pseudomonas fluorescens F113 genes implicated in flagellar filament synthesis and their role in competitive root colonization. Microbiology 150: 3889-3897.
19. Chen, C., Bauske, E.M., Musson, G., Rodríguez-Kabana, R., and Kloepper, J.W. (1995) Biological control of Fusarium wilt on cotton by use of endophytic bacteria. Biol Control 5: 83-91.
20. Chin-A-Woeng, T.F.C., Bloemberg, G.V., Mulders, I.H.M., Dekkers, L.C., and Lugtenberg, B.J.J. (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol Plant Microbe Interact 13: 1340-1345.
21. Collado-Romero, M., Mercado-Blanco, J., Olivares-García, C., Valverde-Corredor, A., and Jiménez-Díaz, R.M. (2006) Molecular variability within and among Verticillium dahliae vegetative compatibility groups determined by fluorescent amplified fragment length polymorphism and polymerase chain reaction markers. Phytopathology 96: 485-495.
22. Compant, S., Duffy, B., Nowak, J., Clément, C., and Barka, E.A. (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71: 4951-4959.
23. Conn, V.M., Walker, A.R., and Franco, C.M.M. (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant Microbe Interact 21: 208-218.
24. Cornelis, P., and Matthijs, S. (2002) Diversity of siderophore-mediated iron uptake systems in fluorescent pseudomonads: not only pyoverdines. Environ Microbiol 4: 787-798.
25. Dennis, P.G., Miller, A.J., and Hirsch, P.R. (2010) Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? FEMS Microbiol Ecol 72: 313-327.
26. Déziel, E., Comeau, Y., and Villemur, R. (2001) Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J Bacteriol 183: 1195-1204.
27. Djavaheri, M., Mercado-Blanco, J., Versluis, C., Meyer, J.M., Van Loon, L.C., and Bakker, P.A.H.M. (2012) Iron-regulated metabolites produced by Pseudomonas fluorescens WCS374 are not required for eliciting induced systemic resistance against Pseudomonas syringae pv. tomato in Arabidopsis. MicrobiologyOpen 1: 311-325.
28. Durland, R.H., and Helinski, D.R. (1987) The sequence encoding the 43-kilodalton trfA protein is required for efficient replication or maintenance of minimal RK2 replicons in Pseudomonas aeruginosa. Plasmid 18: 164-169.
29. El Hadrami, A., Adam, L.R., and Daayf, F. (2011) Biocontrol treatments confer protection against Verticillium dahliae infection of potato by inducing antimicrobial metabolites. Mol Plant Microbe Interact 24: 328-335.
30. Gaworzewska, E.T., and Carlile, M.J. (1982) Positive chemotaxis of Rhizobium leguminosarum and other bacteria towards root exudates from legumes and other plants. J Gen Microbiol 128: 1179-1188.
31. Gitte, R.R., Rai, P.V., and Patil, R.B. (1978) Chemotaxis of Rhizobium sp. towards root exudate of Cicer arietinum L. Plant Soil 50: 553-566.
32. Gómez-Lama Cabanás, C., Schilirò, E., Valverde-Corredor, A., and Mercado-Blanco, J. (2014) The biocontrol endophytic bacterium Pseudomonas fluorescens PICF7 induces systemic defense responses in aerial tissues upon colonization of olive roots. Front Microbiol 5: 427. doi:10.3389/fmicb.2014.00427.
33. Hallmann, J., Quadt-Hallmann, A., Mahafee, W.F., and Kloepper, J.W. (1997) Bacterial endophytes in agricultural crops. Can J Microbiol 43: 895-914.
34. Hamdan, H., Weller, D.M., and Thomashow, L.S. (1991) Relative importance of fluorescent siderophores and other factors in biological control of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens 2-79 and M4-80R. Appl Environ Microbiol 57: 3270-3277.
35. Hardoim, P.R., van Overbeek, L.S., and Elsas, J.D.V. (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16: 463-471.
36. Howie, W.J., Cook, R.J., and Weller, D.M. (1987) Effects of soil matric potential and cell motility on wheat root colonization by fluorescent pseudomonads suppressive to take-all. Phytopathology 77: 286-292.
37. Hynes, M.F., Quandt, J., O'Connell, M.P., and Pühler, A. (1989) Direct selection for curing and deletion of Rhizobium plasmids using transposons carrying the Bacillus subtilis sacB gene. Gene 78: 111-120.
38. King, E.O., Ward, M.K., and Raney, D.E. (1954) Two simple media for demonstration of pyocyanin and fluorescein. J Lab Clin Med 44: 301-307.
39. Kloepper, J.W., and Ryu, C.M. (2006) Bacterial endophytes as elicitors of induced systemic resistance. In Microbial Root Endophytes. Schulz, B.J.E., Boyle, C.J.C., and Sieber, T.N. (eds). Berlin, Germany: Springer-Verlag, pp. 33-52.
40. Kraus, J., and Loper, J.E. (1992) Lack of evidence for a role of antifungal metabolite production by Pseudomonas fluorescens Pf-5 in biological control of Pythium damping-off of cucumber. Phytopathology 82: 264-271.
41. Kuklinsky-Sobral, H.L., Araujo, W.L., Mendes, R., Geraldi, I.O., Pizzirani-Kleiner, A.A., and Azevedo, J.L. (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6: 1244-1251.
42. Lemanceau, P., Expert, D., Gaymard, F., Bakker, P.A.H.M., and Briat, J.F. (2009) Role of iron in plant-microbe interactions. Adv Bot Res 51: 491-549.
43. Lindow, S.E. (1988) Lack of correlation of in vitro antibiosis with antagonism of ice nucleation active bacteria on leaf surfaces by non-ice nucleation active bacteria. Phytopathology 78: 444-450.
44. López-Escudero, F.J., and Mercado-Blanco, J. (2011) Verticillium wilt of olive: a case study to implement an integrated strategy to control a soil-borne pathogen. Plant Soil 344: 1-50.
45. López-Escudero, F.J., Del Rio, C., Caballero, J.M., and Blanco-López, M.A. (2004) Evaluation of olive cultivars for resistance to Verticillium dahliae. Eur J Plant Pathol 110: 79-85.
46. Loper, J.E., Hassan, K.A., Mavrodi, D.V., Davis, E.W., II, Lim, C.K., Shaffer, B.T., etal. (2012) Comparative genomics of plant-associated Pseudomonas spp.: Insights into diversity and inheritance of traits involved in multitrophic interactions. PLoS Genet 8: e1002784.
47. Lugtenberg, B.J., Dekkers, L., and Bloemberg, G.V. (2001) Molecular determinants of rhizosphere colonization by Pseudomonas. Annu Rev Phytopathol 39: 461-490.
48. Lugtenberg, B.J.J., and Bloemberg, G.V. (2004) Life in the rhizosphere. In Pseudomonas, Vol. 1. Ramos, J.L. (ed.). New York, USA: Kluwer Academic/Plenum Publishers, pp. 403-430.
49. Maldonado-González, M.M., Prieto, P., Ramos, C., and Mercado-Blanco, J. (2013) From the root to the stem: interaction between the biocontrol root endophyte Pseudomonas fluorescens PICF7 and the pathogen Pseudomonas savastanoi NCPPB 3335 in olive knots. Microb Biotechnol 6: 275-287.
50. Martínez-Granero, F., Rivilla, R., and Martín, M. (2006) Rhizosphere selection of highly motile phenotypic variants of Pseudomonas fluorescens with enhanced competitive colonization ability. Appl Environ Microbiol 72: 3429-3434.
51. Mavrodi, O.V., Mavrodi, D.V., Park, A.A., Weller, D.M., and Thomashow, L.S. (2006) The role of dsbA in colonization of the wheat rhizosphere by Pseudomonas fluorescens Q8r1-96. Microbiology 152: 863-872.
52. Mercado-Blanco, J., and Bakker, P.A. (2007) Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection. Antonie Van Leeuwenhoek 92: 367-389.
53. Mercado-Blanco, J., and López-Escudero, F.J. (2012) Verticillium wilt of olive and its control: the heat is on. Plant Soil 355: 17-21.
54. Mercado-Blanco, J., and Lugtenberg, B.J.J. (2014) Biotechnological applications of bacterial endophytes. Curr Biotechnol 3: 60-75.
55. Mercado-Blanco, J., Van der Drift, K.M., Olsson, P.E., Thomas-Oates, J.E., Van Loon, L.C., and Bakker, P.A. (2001) Analysis of the pmsCEAB gene cluster involved in biosynthesis of salicylic acid and the siderophore pseudomonine in the biocontrol strain Pseudomonas fluorescens WCS374. J Bacteriol 183: 1909-1920.
56. Mercado-Blanco, J., Rodríguez-Jurado, D., Hervás, A., and Jiménez-Díaz, R.M. (2004) Suppression of Verticillium wilt in olive planting stocks by root-associated fluorescent Pseudomonas spp. Biol Control 30: 474-486.
57. Meschke, H., Walter, S., and Schrempf, H. (2012) Characterization and localization of prodiginines from Streptomyces lividans suppressing Verticillium dahliae in the absence or presence of Arabidopsis thaliana. Environ Microbiol 14: 940-952.
58. Meyer, J.A., and Abdallah, M.A. (1978) The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification and physicochemical properties. J Gen Microbiol 107: 319-328.
59. Meyer, J.M. (2000) Pyoverdines: pigments, siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Arch Microbiol 174: 135-142.
60. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY, USA: Cold Spring Harbor Laboratory.
61. Mitter, B., Petric, A., Shin, M.W., Chain, P.S.G., Hauberg-Lotte, L., Reinhold-Hurek, B., etal. (2013) Comparative genome analysis of Burkholderia phytofirmans PsJN reveals a wide spectrum of endophytic lifestyles based on interaction strategies with host plants. Front Plant Sci 4: 120.
62. Müller, H., Tejedor-González, E., Mercado-Blanco, J., Rodríguez-Jurado, D., Jiménez-Díaz, R.M., and Berg, G. (2007) Effect of the biological control strain Serratia plymuthica HRO-C48 on Verticillium wilt of olive trees cv. Arbequina. In Fundamental and Practical Approaches to Increase Biocontrol Efficacy. Elad, Y., Ongena, M., Höfte, M., and Haïssan Jijakli, M. (eds). Dijon, France: IOBC/WPRS, pp. 173-177. IOBC/wprs Bulletin 30.
63. Navazo, A., Barahona, E., Redondo-Nieto, M., Martínez-Granero, F., Rivilla, R., and Martín, M. (2009) Three independent signalling pathways repress motility in Pseudomonas fluorescens F113. Microb Biotechnol 2: 489-498.
64. Nejad, P., and Johnson, P.A. (2000) Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biol Control 18: 208-215.
65. Ongena, M., Daayf, F., Jacques, P., Thonart, P., Benhamou, N., Paulitz, T.C., etal. (1999) Protection of cucumber against Pythium root rot by fluorescent pseudomonads: predominant role of induced resistance over siderophores and antibiosis. Plant Pathol 48: 66-76.
66. Ormeño-Orrillo, E., Rosenblueth, M., Luyten, E., Vanderleyden, J., and Martínez-Romero, E. (2008) Mutations in lipopolysaccharide biosynthetic genes impair maize rhizosphere and root colonization of Rhizobium tropici CIAT899. Environmen microbiol 10: 1271-1284.
67. Overhage, J., Lewenza, S., Marr, A.K., and Hancock, R.E. (2007) Identification of genes involved in swarming motility using a Pseudomonas aeruginosa PAO1 mini-Tn5-lux mutant library. J Bacteriol 189: 2164-2169.
68. Pegg, G.F., and Brady, B.L. (2002) Verticillium Wilts. Wallingford, UK: CAB International, pp. 293-340.
69. Pieterse, C.M.J., Zamioudis, C., Berendsen, R.L., Weller, D.M., Van Wees, S.C.M., and Bakker, P.A.H.M. (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52: 347-375.
70. Prieto, P., and Mercado-Blanco, J. (2008) Endophytic colonization of olive roots by the biocontrol strain Pseudomonas fluorescens PICF7. FEMS Microbiol Ecol 64: 297-306.
71. Prieto, P., Navarro-Raya, C., Valverde-Corredor, A., Amyotte, S.G., Dobinson, K.F., and Mercado-Blanco, J. (2009) Colonization process of olive tissues by Verticillium dahliae and its in planta interaction with the biocontrol root endophyte Pseudomonas fluorescens PICF7. Microb Biotechnol 2: 499-511.
72. Prieto, P., Schilirò, E., Maldonado-González, M.M., Valderrama, R., Barroso-Albarracín, J.B., and Mercado-Blanco, J. (2011) Root hairs play a key role in the endophytic colonization of olive roots by Pseudomonas spp. with biocontrol activity. Microbial Ecol 62: 435-445.
73. Raaijmakers, J.M., Paulitz, T.C., Steinberg, C., Alabouvette, C., and Moënne-Loccoz, Y. (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321: 341-361.
74. Reinhold-Hurek, B., and Hurek, T. (2011) Living inside plants: bacterial endophytes. Curr Opin Plant Biol 14: 435-443.
75. Rodríguez-Moreno, L., Jiménez, A.J., and Ramos, C. (2009) Endopathogenic lifestyle of Pseudomonas savastanoi pv. savastanoi in olive knots. Microb Biotechnol 2: 476-488.
76. Sanei, S.J., and Razavi, S.E. (2011) Suppression of Verticillium wilt of olive by Pseudomonas fluorescens. Am J Exp Agri 1: 294-305.
77. Sang, M.K., and Kim, K.D. (2014) Biocontrol activity and root colonization by Pseudomonas corrugata strains CCR04 and CCR80 against Phytophthora blight of pepper. BioControl 59: 437-448.
78. Schilirò, E., Ferrara, M., Nigro, F., and Mercado-Blanco, J. (2012) Genetic responses induced in olive roots upon colonization by the biocontrol endophytic bacterium Pseudomonas fluorescens PICF7. PLoS ONE 7: e48646.
79. Schwyn, B., and Neilands, J.B. (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.
80. Simon, R., Priefer, U., and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat Biotechnol 1: 784-791.
81. Simons, M., Permentier, H.P., de Weger, L.A., Wijffelman, C.A., and Lugtenberg, B.J.J. (1997) Amino acid synthesis is necessary for tomato root colonization by Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact 10: 102-106.
82. Tjamos, E.C. (1993) Prospects and strategies in controlling Verticillium wilt of olive. OEPP/EPPO Bull 23: 505-512.
83. Tjamos, S.E., Flemetakis, E., Paplomatas, E.J., and Katinakis, P. (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18: 555-561.
84. Wang, Y.Q., Ohara, Y., Nakayashiki, H., Tosa, Y., and Mayama, S. (2005) Microarray analysis of the gene expression profile induced by the endophytic plant growth-promoting rhizobacteria, Pseudomonas fluorescens FPT9601-T5 in Arabidopsis. Mol Plant Microbe Interact 18: 385-396.
85. Weller, D.M. (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97: 250-256.