Skip to main content
Log in

Molecular characterization of Algerian Erwinia amylovora strains by VNTR analysis and biocontrol efficacy of Bacillus spp. and Pseudomonas brassicacearum antagonists

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Samples of pear shoots, blossoms and leaves showing typical fire blight symptoms were collected from diseased pear trees during spring and summer over a period of 3 years from orchards situated in the Mitidja region, a main pear producing area in Northern Algeria. From all collected plant samples, thirty-seven putative Erwinia amylovora strains were isolated and identified by biochemical, serological and molecular tests. Molecular typing of these strains was performed using six variable number of tandem repeats sequences (VNTRs). Minimal spanning trees showed that four different haplotypes were present within the bacterial population analyzed. The efficacy of twenty potential bacterial antagonists was evaluated in vitro against two E. amylovora pathogenic strains. Four antagonists (Bacillus amyloliquefaciens, Bacillus methylotrophicus and two Pseudomonas brassicaceaurum) were selected to perform a biocontrol assay on immature pear fruits. Results showed that the two Pseudomonas strains were the most effective for preventive treatment on pear fruits, leading to a necrosis reduction of up to 90%. No curative effect was observed. The four selected antagonists were characterized for features linked to biocontrol activity, such as biofilm, siderophores and biosurfactant-production, motility, and effect of environmental conditions on bacterial growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Aandahl, R. Z., Reyes, J. F., Sisson, S. A., & Tanaka, M. M. (2012). A model-based Bayesian estimation of the rate of evolution of VNTR loci in Mycobacterium tuberculosis. PLoS Computational Biology, 8, e1002573.

    PubMed  PubMed Central  Google Scholar 

  • Ait Bahadou, S., Ouijja, A., Karfach, A., Tahiri, A., & Lahlali, R. (2018). New potential bacterial antagonists for the biocontrol of fire blight disease (Erwinia amylovora) in Morocco. Microbial Pathogenesis, 117, 7–15.

    CAS  PubMed  Google Scholar 

  • Aldwinckle, H. S., Bhaskara Reddy, M. V., & Norelli, J. L. (2002). Evaluation of control of fire blight infection of apple blossoms and shoots with SAR inducers, biological agents, a growth regulator, copper compounds, and other materials. Acta Horticulturae, 590, 325–331.

    CAS  Google Scholar 

  • Alnaasan, Y., Valentini, F., Balestra, G. M., Mazzaglia, A., D’Onghia, A. M., & Varvaro, L. (2017). Modification of a multiple-locus variable number tandem repeat analysis (MLVA) for typing isolates of Erwinia amylovora. Plant Pathology, 66, 1075–1080. https://doi.org/10.1111/ppa.12660.

    Article  CAS  Google Scholar 

  • Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R., & Daszak, P. (2004). Emerging infectious diseases of plants: Pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology and Evolution, 19, 535–544.

    PubMed  Google Scholar 

  • Ashmawy, NA. (2010). Pathological and molecular studies on Erwinia amylovora the causal agent of fire blight disease. Ph.D. Thesis, Alexandria University, Egypt.

  • Awais, M., Ali shah, A., Abdul, H., & Hasan, F. (2007). Isolation, identification and optimization of Bacillus sp. Pakistan Journal of Botany, 39, 1303–1312.

    Google Scholar 

  • Bereswill, S., Bugert, P., Bruchmuller, I., & Geider, K. (1995). Identification of the fire blight pathogen, Erwinia amylovora, by PCR assays with chromosomal DNA. Applied and Environmental Microbiology, 61, 2636–2642.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Billing, E., Crosse, J. E., & Garrett, C. M. E. (1960). Laboratory diagnosis of fire blight and bacterial blossom blight of pears. Plant Pathology, 9, 19–25.

    Google Scholar 

  • Billing, E., Baker, L. A. E., Crosse, J. E., & Garret, C. M. E. (1961). Characteristics of English isolates of Erwinia amylovora (Burrill) Winslow et al. Journal of Applied Bacteriology, 24, 195D211.

    Google Scholar 

  • Broggini-Schärer, G. A. L., Duffy, B., Holliger, E., Scharer, H. J., Gessler, C., & Patocchi, A. (2005). Detection of the fire blight biocontrol agent Bacillus subtilis BD170 (Biopro®) in a Swiss apple orchard. European Journal of Plant Pathology, 111, 93–100.

    Google Scholar 

  • Bühlmann, A., Dreo, T., Rezzonico, F., Pothier, J. F., Smits, T. H., Ravnikar, M., & Duffy, B. (2014). Phylogeography and population structure of the biologically invasive phytopathogen Erwinia amylovora inferred using minisatellites. Environmental Microbiology, 16(7), 2112–2125.

    PubMed  Google Scholar 

  • Bunster, L., Fokkema, N. J., & Schippers, B. (1989). Effect of surface-active Pseudomonas spp. on leaf wettability. Applied and Environmental Microbiology, 55, 1340–1345.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burrill, T. J. (1883). New species of Micrococcus (bacteria). The American Naturalist, 17, 319.

    Google Scholar 

  • Cabrefiga, J., & Montesinos, E. (2005). Analysis of aggressiveness of Erwinia amylovora using disease-dose and time relationships. Phytopathology, 95, 1430–1437.

    PubMed  Google Scholar 

  • Cabrefiga, J., Bonaterra, A., & Montesinos, E. (2007). Mechanism of antagonism of Pseudomonas fluorescens EPS62e against Erwinia amylovora, the causal agent of fire blight. International Microbiology, 10, 123–132.

    PubMed  Google Scholar 

  • Chakravarty, S., & Gregory, G. (2015). The genus Pseudomonas. In E. Goldman & L. H. Green (Eds.), Practical handbook of microbiol (pp. 321–344). New York: CRC Press.

    Google Scholar 

  • Cooksey, D. A., & Moore, L. W. (1980). Biological control of crown gall with fungal and bacterial antagonists. Phytopathology, 70, 506–509.

    Google Scholar 

  • Csonka, L. N. (1989). Physiological and genetic responses of bacteria to osmotic stress. Microbiological Reviews, 53, 121–147.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Daranas, N., Bonaterra, A., Francés, J., Cabrefiga, J., Montesinos, E., & Badosa, E. (2018). Monitoring viable cells of the biological control agent Lactobacillus plantarum PM411 in aerial plant surfaces by means of a strain-specific viability quantitative PCR method. Applied and Environmental Microbiology, 84(10), e00107–e00118.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dardouri, S., Chehimi, S., Murillo, J., & Hajlaoui, M. R. (2017). Molecular characterization of Tunisian strains of Erwinia amylovora. Journal of Plant Pathology, 99(2), 331–337.

    Google Scholar 

  • Davey, M. E., & O’Toole, G. A. (2000). Microbial biofilms: from ecology to molecular genetics. Microbiology and Molecular Biology Reviews, 64, 847–867.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dellagi, A., Brisset, M. N., Paulin, J. P., & Expert, D. (1998). Dual role of desferrioxamine in Erwinia amylovora pathogenicity. Molecular Plant-Microbe Interactions, 11, 734–742.

    CAS  PubMed  Google Scholar 

  • Déziel, E., Comeau, Y., & Villemur, R. (2001). Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with the emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming and twitching motilities. Journal of Bacteriology, 183, 1195–1204.

    PubMed  PubMed Central  Google Scholar 

  • D'Souza-Ault, M. R., Smith, L. T., & Smith, G. M. (1993). Roles of N-Acetylglutaminylglutamine amide and glycine betaine in adaptation of Pseudomonas aeruginosa to osmotic stress. Applied and Environmental Microbiology, 59, 473–478.

    CAS  PubMed  PubMed Central  Google Scholar 

  • EPPO (European and Mediterranean Plant Protection Organization). (2013). PM 7/20 (2) Erwinia amylovora. EPPO Bulletin. https://doi.org/10.1111/epp.12019.

  • Flemming, H. C. (1993). Biofilms and environmental protection. Wat Sci Technol, 27, 1–10.

    CAS  Google Scholar 

  • Foster, G. C., Gayle, C., Jones, A. L., & Sundin, G. W. (2004). Nucleotide sequences, genetic organization, and distribution of pEU30 and pEL60 from Erwinia amylovora. Applied and Environmental Microbiology, 70, 7539e7544.

    Google Scholar 

  • Fried, A., Schell, E., Moltman, E., & Wensing, A. (2013). Control of fire blight in Baden-Württenberg at the end of the streptomycin era. Acta Horticulturae, 1056, 55–56.

    Google Scholar 

  • Garrity, G. M. (2005). The Proteobacteria - part B: The Gammaproteobacteria. In Bergey’s manual of systematic bacteriology. Springer: New York.

    Google Scholar 

  • Gerami, E., Hassanzadeh, N., Abdollahi, H., Ghasemi, A., & Heydari, A. (2013). Evaluation of some bacterial antagonists for biological control of fire blight disease. Journal of Plant Pathology, 95, 127–134.

    Google Scholar 

  • Ghoul, M. (1990). Halotolerance de Escherichia coli: effet des osmoprotecteurs naturels. Thèse de Doctorat, Université de Rennes I, France.

  • Hannou, N., Llop, P., Faure, D., Lopez, M. M., & Moumni, M. (2013). Characterization of Erwinia amylovora strains from middle Atlas Mountains in Morocco by PCR based on tandem repeat sequences. European Journal of Plant Pathology, 136, 665–674.

    CAS  Google Scholar 

  • Harshey, R. M. (2003). Bacterial motility on a surface: many ways to a common goal. Annual Review of Microbiology, 57, 249–273.

    CAS  PubMed  Google Scholar 

  • Hildebrand, D. C., Schroth, M. N., & Sands, D. C. (1988). Pseudomonas. In N. W. Schaad (Ed.), Laboratory guide for identification of plant pathogenic Bacteria: 60–80. St. Paul: APS.

    Google Scholar 

  • Hunter, P. R., & Gaston, M. A. (1988). Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. Journal of Clinical Microbiology, 26, 2465–2466.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jalal, M. A. F., & Vander Helm, D. (1990). Isolation and spectroscopic identification of fungal siderophores. In G. Winklemann (Ed.), Handbook of microbial iron chelates (pp. 235–269). Oxford: Pegamon Press.

    Google Scholar 

  • Jones, A. L., & Geider, K. (2001). Erwinia amylovora group. In N. W. Schaad, J. B. Jones, & W. Chun (Eds.), Laboratory guide for identification of plant pathogenic Bacteria (pp. 40–55). St. Paul: APS Press.

    Google Scholar 

  • Kraus, J., & Loper, J. E. (1995). Characterization of a genomic region required for production of the antibiotic pyoluteorin by the biological control agent Pseudomonas fluorescens Pf-5. Applied and Environmental Microbiology, 61, 849–854.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krimi, Z., Alim, D., Djellout, H., Tafifet, L., Mohamed-Mahmoud, F., & Raio, A. (2016). Bacterial endophytes of weeds are effective biocontrol agents of Agrobacterium spp., Pectobacterium spp., and promote growth of tomato plants. Phytopathol. Mediterr, 55(2), 184–196.

    Google Scholar 

  • Laala, S., Manceau, C., Valentini, F., Kerkoud, M., & Kheddam, M. (2012). Fire blight survey and first characterization of Erwinia amylovora isolates from Algeria. Journal of Plant Pathology, 94, 693–696.

    Google Scholar 

  • Lashgarian, H. E., Marzban, A., Estaji, M., Gholami, M., Masoumi Asl, H., & Raheb, J. (2018). Multiple locus variable number tandem repeat analysis (MLVA) for typing Pseudomonas Aeruginosa isolated from urine samples of different patients. Journal of Babol University of Medical Sciences, 20(2), 56–63.

    Google Scholar 

  • Laurent, J., Barny, M. A., Kotoujansky, A., Dufriche, P., & Vanneste, J. L. (1989). Characterization of an ubiquitous plasmid in Erwinia amylovora. Molecular Plant–Microbe Interaction, 2, 160–164.

    Google Scholar 

  • 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. Phytopathol, 78, 444–450.

    Google Scholar 

  • Linget, C., Slylianou, D. G., Dell, A., Wolff, R. E., Piemont, Y., & Abdallah, M. A. (1992). Bacterial siderophores: the structure of a desferriferribactin produced by P. fluorescens ATCC 13525. Tetrahedron Letters, 33, 3851–3854.

    CAS  Google Scholar 

  • Loewen, P. C., Switala, J., Fernando, W. G. D., & de Kievit, T. (2014). Genome sequence of Pseudomonas brassicacearum DF41. Genome Announcements, 2(3), e00390–e00314.

    PubMed  PubMed Central  Google Scholar 

  • Maddula, V., Zhang, Z., Pierson, E. A., & Pierson, L. S. (2006). Quorum sensing and phenazines are involved in biofilm formation by Pseudomonas chlororaphis (aureofaciens) strain 30–84. Microbial Ecology, 52, 289–301.

    CAS  PubMed  Google Scholar 

  • Manjunatha, B. S., Asha, A. D., Nivetha, N., Bandeppa Govindasamy, V., Rathi, M. S., & Sangeeta, P. (2017). Evaluation of endophytic bacteria for their influence on plant growth and seed germination under water stress conditions. International Journal of Current Microbiology and Applied Sciences, 6(11), 4061–4067.

    Google Scholar 

  • Mann, R. A., Smits, T. H. M., Bühlmann, A., Blom, J., Goesmann, A., Frey, J. E., et al. (2013). Comparative genomics of 12 strains of Erwinia amylovora identifies a pan-genome with a large conserved core. PLoS One, 8, e55644.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mansfield, J., Genin, S., Magori, S., Citovsky, V., Sriariyanum, M., Ronald, P., Dow, M., Verdier, V., Beer, S. V., Machado, M. A., Toth, I., Salmond, G., & Foster, G. D. (2012). Top 10 plant pathogenic bacteria in molecular plant pathology: top 10 plant pathogenic bacteria. Molecular Plant Pathology, 13, 614–629.

    PubMed  PubMed Central  Google Scholar 

  • McGhee, G. C., & Jones, A. L. (2000). Complete nucleotide sequence of ubiquitous plasmid pEA29 from Erwinia amylovora strain Ea88: gene organization and interspecies variation. Applied and Environmental Microbiology, 66, 4897e4907.

    Google Scholar 

  • McManus, P. S., & Jones, A. L. (1995). Detection of Erwinia amylovora by nested PCR and PCR-dot-blot and reverse-blot hybridizations. Phytopathology, 85, 618–623.

    CAS  Google Scholar 

  • Mercier, J., & Lindow, S. E. (2001). Field performance of antagonistic bacteria identified in a novel laboratory assay for biological control of fire blight of pear. Biological Control, 22, 66–71.

    Google Scholar 

  • Meyer, J. M., & Abdallah, M. A. (1978). The fluorescent pigment of Pseudomonas fluorescens: biosynthesis, purification, and physicochemical properties. Journal of General Microbiology, 107, 319–328.

    CAS  Google Scholar 

  • Mikiciński, A., Sobiczewski, P., & Berczyn’ski, S. (2008). Selection of bacteria from epiphytic populations on apple trees and soil environment for ability to control fire blight (Erwinia amylovora). Phytopathologia Polonica, 47, 43–55.

  • Mikiciński, A., Sobiczewski, P., Puławska, J., & Malusa, E. (2016). Antagonistic potential of Pseudomonas graminis 49M against Erwinia amylovora, the causal agent of fire blight. Archives of Microbiology, 198, 531–539.

    PubMed  PubMed Central  Google Scholar 

  • Neilands, J. B. (1981). Microbial iron compounds. Annual Review of Biochemistry, 50, 715–731.

    CAS  PubMed  Google Scholar 

  • Norelli, J. L., Jones, A. L., & Aldwinckle, H. S. (2003). Fire blight management in the twenty-first century: Using new technologies that enhance host resistance in apple. Plant Disease, 87, 756–765.

    PubMed  Google Scholar 

  • Novinscak, A., Gadkar, V. J., Joly, D. L., & Filion, M. (2016). Complete genome sequence of Pseudomonas brassicacearum LBUM300, a disease-suppressive bacterium with antagonistic activity toward fungal, oomycete, and bacterial plant pathogens. Genome Announcements, 4(1), e01623–e01615 1–2.

    PubMed  PubMed Central  Google Scholar 

  • Ohike, T., Matsukawa, T., Okanami, M., Kajiyama, S.-i., & Ano, T. (2018). In vitro and in vivo assay for assessment of the biological control potential of Streptomyces sp. KT. Journal of Plant Studies, 7(1), 1–18.

    Google Scholar 

  • O'Toole, G. A., & Kolter, R. (1998). The initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Molecular Microbiology, 28, 449–461.

    CAS  PubMed  Google Scholar 

  • Paulin, M. M., Novinscak, A., Lanteigne, C., Gadkar, V. J., & Filion, M. (2017). Interaction between 2,4-diacetylphloroglucinol- and hydrogencyanide-producing Pseudomonas brassicacearum LBUM300 and Clavibacter michiganensis subsp .michiganensis in the tomato rhizosphere. Applied and Environmental Microbiology, 83, e00073–e00017. https://doi.org/10.1128/AEM.00073-17.

    Article  PubMed  PubMed Central  Google Scholar 

  • Piqué, N., Miñana-Galbis, D., Merino, S., & Tomás, J. M. (2015). Virulence factors of Erwinia amylovora: a review. International Journal of Molecular Sciences, 16, 12836–12854.

    PubMed  PubMed Central  Google Scholar 

  • Pocard, J. A., Smith, L. T., Smith, G. M., & Le Rudulien, D. (1994). A prominent role for glucosylglycerol in the adaptation of Pseudomonas mendocina SKB70 to osmotic stress. Journal of Bacteriology, 176, 6877–6884.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pourcel, C., Minandri, F., Hauck, Y., D’Arezzo, S., Imperi, F., Vergnaud, G., & Visca, P. (2011). Identification of variable-number tandem-repeat (VNTR) sequences in acinetobacter baumannii and interlaboratory validation of an optimized multiple-locus VNTR analysis typing scheme. Journal of Clinical Microbiology, 49(2), 539–548.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pusey, P. L., & Wend, C. (2012). Potential of osmoadaptation for improving Pantoea agglomerans E325 as biocontrol agent for fire blight of apple and pear. Biological Control, 62, 29–37.

    Google Scholar 

  • Rabhi, NH. (2011). Isolement de Pseudomonas spp. fluorescents d’un sol salé. Effet d’osmoprotecteurs naturels. Thes Mag, Gen microbiol .Univ Setif :121.

  • Refahi, M., Baghaee-Ravari, S., & Mahdikhani-Moghaddam, E. (2017). Exploring possible variation among Iranian Erwinia amylovora strains using multilocus typing and tandem repeat analysis. Journal of Agricultural Science and Technology, 19, 745–754.

    Google Scholar 

  • Rhodes, M. E. (1958). The cytology of Pseudomonas spp. as revealed by a silver-plating staining method. Journal of General Microbiology, 18, 639.

    CAS  PubMed  Google Scholar 

  • Roselló, G., Bonaterra, A., Francés, J., Montesinos, L., Badosa, E., & Montesinos, E. (2013). Biological control of fire blight of apple and pear with antagonistic Lactobacillus plantarum. European Journal of Plant Pathology, 137, 621–633.

    Google Scholar 

  • Sasirekha, B., & Srividya, S. (2016). Siderophore production by Pseudomonas aeruginosa FP6, a biocontrol strain for Rhizoctonia solani and Colletotrichum gloeosporioides causing diseases in chilli. Agriculture and Natural Resources, 50, 250–256.

    CAS  Google Scholar 

  • Schaad, NW., Hildebrand, DC., Schoth, MN., & Sands, DC. (1988). In plant pathologic bacteria, laboratory guide for identification. ed N°02. N. W. APS Minnesota. USA. 37–53.

  • Schouls, L. M., Spalburg, E. C., van Luit, M., Huijsdens, X. W., Pluister, G. N., et al. (2009). Multiple-locus variable number tandem repeat analysis of Staphylococcus Aureus: Comparison with pulsed-field gel electrophoresis and spa-typing. PLoS One, 4(4), e5082.

    PubMed  PubMed Central  Google Scholar 

  • Sebaihia, M., Bocsanczy, A. M., Biehl, B. S., Quail, M. A., Perna, N. T., Glasner, J. D., DeClerck, G. A., Cartinhour, S., Schneider, D. J., Bentley, S. D., Parkhill, J., & Beer, S. V. (2010). Complete genome sequence of the plant pathogen Erwinia amylovora strain ATCC 49946. Journal of Bacteriology, 192, 2020–2021.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stepanovic, S., Vukovic, D., Dakic, I., Savic, B., & Svabic-Vlahovic, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40, 175–179.

    CAS  PubMed  Google Scholar 

  • Stockwell, V. O., Johnson, K. B., & Loper, J. E. (2001). Enhancement of biocontrol of fire blight with an iron chelate. Phytopathology, 91, S86.

    Google Scholar 

  • Stonier, T. (1960). Agrobacterium tumefaciens Conn. II. Production of an antibiotic substance. Journal of Bacteriology, 79, 889–898.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Suslow, T. V., Schroth, M. N., & Isaka, M. (1982). Application of a rapid method for gram differenciation of plant pathogenic and saprophytic bacteria without staining. Phytopathology, 72, 917–918.

    Google Scholar 

  • Tailor, A. J., & Joshi, H. B. (2012). Characterization and optimization of siderophore production from Pseudomonas fluorescens strain isolated from sugarcane rhizosphere. Journal of Environmental Research and Development, 6, 688e694.

    Google Scholar 

  • Temple, T. N., Stockwell, V. O., Loper, J. E., & Johnson, K. B. (2004). Bioavailability of iron to Pseudomonas fluorescens A506 on flowers of pear and apple. Phytopathology, 94, 1286–1294.

    CAS  PubMed  Google Scholar 

  • Ülke, G., & Ҫınar, Ö. (1999). Biological control studies on fire blight caused by Erwinia amylovora (Burr.) Winslow et al. Acta Horticulturae, 489, 611–614.

    Google Scholar 

  • van der Zwet, T., & Beer, S. (1995). Fire blight: Its nature, prevention and control. A practical guide to integrated disease management. USDA Agricultural Information Bulletin, No. 631.

  • Vanneste, J. L., Paulin, J. P., & Expert, D. (1990). Bacteriophage mu as a genetic tool to study Erwinia amylovora pathogenicity and hypersensitive reaction on tobacco. Journal of Bacteriology, 172(2), 932–941.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wilson, M., & Lindow, S. E. (1993). Interactions between the biological control agent Pseudomonas fluorescens strain A506 and Erwinia amylovora in pear flowers. Phytopathology, 83, 117–123.

    Google Scholar 

  • Yaich, M., Fatmi, M., Mougsiba, M., Valentini, F., Scuderi, G., D’Onghia, A. M., & Cirvilleri, G. (2011). Fire blight (Erwinia amylovora [Burrill] Winslow) in Morocco: importance, geographical distribution and characterization. Phytopathologia Mediterranea, 50, 212–227.

    CAS  Google Scholar 

  • Zhang, X. Q., Bishop, P. L., & Kupferle, M. J. (1998). Measurement of polysaccharides and proteins in biofilm extracellular polymers. Water Science and Technology, 37, 345–348.

    CAS  Google Scholar 

  • Zhao, Y., Blumer, S. E., & Sundin, G. W. (2005). Identification of Erwinia amylovora genes induced during infection of immature pear tissue. Journal of Bacteriology, 187, 8088–8103.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lamia Tafifet.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

ESM 1

(DOCX 136 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tafifet, L., Raio, A., Holeva, M.C. et al. Molecular characterization of Algerian Erwinia amylovora strains by VNTR analysis and biocontrol efficacy of Bacillus spp. and Pseudomonas brassicacearum antagonists. Eur J Plant Pathol 156, 867–883 (2020). https://doi.org/10.1007/s10658-020-01938-6

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-020-01938-6

Keywords

Navigation