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Effects of plant essential oils on growth and virulence factors of Erwinia amylovora

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Abstract

Erwinia amylovora causes fire blight in plants of economic importance in Rosaceae family. In this study, 11 essential oils were screened for their antibacterial activities and capabilities to influence the growth and virulence factors by the E. amylovora, such as amylovoran production, biofilm formation, and motility at non-lethal concentrations. Essential oils from Foeniculum vulgare and Pimpinella anisum showed strong antibacterial activity, those of Artemisia aucheri and Heracleum persicum had a moderate antibacterial activity. Oils of seven other plant species did not show substantial growth inhibition but could reduce the production of virulence factors in E. amylovora at non-lethal concentrations. Determining bacteriostatic and bactericidal concentrations enabled us to gather precise data about the antibacterial characteristics. The results suggested that at non-lethal concentrations, some essential oils reduced the effect of virulence factors of E. amylovora. An inverse correlation was found between amylovoran and biofilm production when the bacterium was treated with oils of H. persicum, P. anisum, C. arabica, J. horizentalis, C. aurantifolia and V. agnus-castus. The oils with low antibacterial activity had an insignificant effect on motility at non-lethal concentrations. Generally, Apium graveolens (celery seed) and Curcuma longa (turmeric) essential oils showed the optimum reduction in the effects of virulence factors of E. amylovora. These oils led to 41.71% and 30.17% reduction in the disease progression of E. amylovora on immature pear fruit, respectively and reduced disease progression in the shoot of pear seedlings with 26.9% and 16.7%. This study indicated that essential oils individually may be applied as environmentally safe compounds for controlling the fire blight disease.

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References

  • Ab Rahman SFS, Sijam K, Omar D (2014) Chemical composition of Piper sarmentosum extracts and antibacterial activity against the plant pathogenic bacteria Pseudomonas fuscovaginae and Xanthomonas oryzae pv. oryzae. J Plant Dis Protect 121:237–242. https://doi.org/10.1007/BF03356518

    Article  Google Scholar 

  • Adeolu M, Alnajar S, Naushad S, Gupta RS (2016) Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 66:5575–5599

    Article  CAS  PubMed  Google Scholar 

  • Al-Bayati FA (2008) Synergistic antibacterial activity between Thymus vulgaris and Pimpinella anisum essential oils and methanol extracts. J Ethnopharmacol 116:403–406. https://doi.org/10.1016/j.jep.2007.12.003

    Article  CAS  PubMed  Google Scholar 

  • American Public Health Association (2005) Standard methods for the examination of water and wastewater. American Public Health Association, Washington DC

  • Asghari G, Jalali M, Sadoughi E (2012) Antimicrobial activity and chemical composition of essential oil from the seeds of Artemisia aucheri Boiss. Jundishapur J Nat Pharm Prod 7:11–15

    Article  PubMed  PubMed Central  Google Scholar 

  • Ataee M, Akhondzadeh Basti A, Zahraei Salehi T, Hosseini H, Gandomi Nasrabadi H, Noori N, Khanjari A, Taheri Mirghaed A, Mohammad khan F, Faghih Fard P (2013) Effect of Zataria multiflora Boiss. essential oil on growth curve and shigatoxin 2 production of enter hemorrhagic Escherichia coli O157:H7. J Med Plant 48:62–71

  • Baananou S, Bouftira I, Mahmoud A, Boukef K, Marongiu B, Boughattas NA (2012) Antiulcerogenic and antibacterial activities of Apium graveolens essential oil and extract. Nat Prod Res 27:1075–1083. https://doi.org/10.1080/14786419.2012.717284

    Article  CAS  PubMed  Google Scholar 

  • Bajpai VK, Sharma A, Baek KH (2013) Antibacterial mode of action of Cudrania tricuspidata fruit essential oil, affecting membrane permeability and surface characteristics of food-borne pathogens. Food Control 32:582–590. https://doi.org/10.1016/j.foodcont.2013.01.032

    Article  CAS  Google Scholar 

  • Bereswill S, Geider K (1997) Characterization of the rcsB gene from Erwinia amylovora and its influence on exopolysaccharide synthesis and virulence of the fire blight pathogen. J Bacteriol 179:1354–1361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carezzano ME, Sotelo JP, Primo E, Reinoso EB, Paletti Rovey MF, Demo MS, Giordano MF, Oliva M (2017) Inhibitory effect of Thymus vulgaris and Origanum vulgare essential oils on virulence factors of phytopathogenic Pseudomonas syringae strains. Plant Biol 19:599–607. https://doi.org/10.1111/plb.12572

    Article  CAS  PubMed  Google Scholar 

  • Chen XH, Scholz R, Borriss M, Junge H, Mögel G, Kunz S, Borriss R (2009) Difficidin and bacilysin produced by plant-associated Bacillus amyloliquefaciens are efficient in controlling fire blight disease. J Biotechnol 140:38–44. https://doi.org/10.1016/j.jbiotec.2008.10.015

    Article  CAS  PubMed  Google Scholar 

  • Clements A, Tull D, Jenney AW, Farn JL, Kim SH, Bishop RE, McPhee JB, Hancock RE, Hartland EL, Pearse MJ, Wijburg OL, Jackson DC, McConville MJ, Strugnell RA (2007) Secondary acylation of Klebsiella pneumoniae lipopolysaccharide contributes to sensitivity to antibacterial peptides. J Biol Chem 282:15569–15577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cowan MM (1999) Plant products as antimicrobial agents. Clin Microbiol Rev 12:564–582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dadalioğlu I, Akdemir Evrendilek G (2004) Chemical compositions and antibacterial effects of essential oils of Turkish oregano (Origanum minutiflorum), bay laurel (Laurus nobilis), Spanish lavender (Lavandula stoechas L.), and fennel (Foeniculum vulgare) on common foodborne. J Agric Food Chem 52:8255–8260. https://doi.org/10.1021/jf049033e

    Article  CAS  PubMed  Google Scholar 

  • Damjanovi’c-Vratnica B, Dakov T, Sukovi’c D, Damjanovi’c J (2011) Antimicrobial effect of essential oil isolated from Eucalyptus globulus Labill. From Montenegro. Czech J Food Sci 29:277–284

    Article  Google Scholar 

  • Dewdney MM, Biggs AR, Turechek WW (2007) A Statistical comparison of the blossom blight forecasts of MARYBLYT and Cougarblight with receiver operating characteristic curve analysis. Phytopathology 97:1164–1176

    Article  CAS  PubMed  Google Scholar 

  • Dorman HJD, Deans SG (2000) Antimicrobial agents from plants: Antibacterial activity of plant volatile oils. J Appl Microbiol 88:308–316

    Article  CAS  PubMed  Google Scholar 

  • Düker A, Kubiak R (2011) Stem injection of prohexadione carboxylic acid to protect blossoms of apple trees from fire blight infection (Erwinia amylovora). J Plant Dis Protect 118:156–160. https://doi.org/10.1007/BF03356398

    Article  Google Scholar 

  • Gusberti M, Klemm U, Meier MS, Maurhofer M, Hunger-Glaser I (2015) Fire blight control: the struggle goes on. A comparison of different fire blight control methods in Switzerland with respect to biosafety, efficacy and durability. Int J Environ Res Public Health 12:11422–11447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Habibipour R, Moradi Haghgou M (2015) Study on Hydro-Alcoholic Extract Effect of Pomegranate Peel on Pseudomonas aeruginosa Biofilm Formation. Avicenna J Clin Med Medicine 22:195–202

    Google Scholar 

  • Hasanzadeh N (2005) Technological implication of natural products in plant diseases management with special emphasis on fire blight. J Agric Sci 11:53–68

    Google Scholar 

  • Hollinger FB (ed.) (1993) AIDS clinical trials group virology manual for HIV laboratories. NIH (NIAID Division of AIDS), Rockville MD, pp. MIC-1–MIC-5

  • Iacobellis NS, Lo Cantore P, Capasso F, Senatore F (2005) Antibacterial activity of Cuminum cyminum L. and Carum carvi L. essential oils. J Agric Food Chem 53:57–61. https://doi.org/10.1021/jf0487351

    Article  CAS  PubMed  Google Scholar 

  • Joe MM, Benson A, Saravanan VS, Sa T (2015) In vitro antibacterial activity of nanoemulsion formulation on biofilm, AHL production, hydrolytic enzyme activity, and pathogenicity of Pectobacterium carotovorum sub sp. carotovorum. Physiol Mol Plant Pathol 91:46–55. https://doi.org/10.1016/j.pmpp.2015.05.009

    Article  CAS  Google Scholar 

  • Joshi RJ, Burdman S, Lipsky A, Yedidia I (2015) Effects of plant antimicrobial phenolic compounds on virulence of the genus Pectobacterium. Res Microbiol 166:535–545. https://doi.org/10.1016/j.resmic.2015.04.004

    Article  CAS  PubMed  Google Scholar 

  • Karami-Osboo R, Khodaverdi M, Ali-Akbari F (2010) Antibacterial effect of effective compounds of Satureja hortensis and Thymus vulgaris essential oils against Erwinia amylovora. J Agr Sci Tech 12:35–45

    CAS  Google Scholar 

  • Kim BS, Park SJ, Kim MK, Kim YH, Lee SB, Lee KH, Choi NY, Lee YR, Lee YE, You YO (2015) Inhibitory effects of chrysanthemum boreale essential oil on biofilm formation and virulence factor expression of Streptococcus mutans. Evid Based Complement Alternat Med 2015:1–11

    Google Scholar 

  • Koczan J (2011) The role of biofilm formation in systemic movement of Erwinia amylovora in apple. Michigan State University, Dissertation

    Google Scholar 

  • Kokoskova B, Pavela R (2007) Effectiveness of plant essential oils on the growth of Erwinia amylovora, the causal agent of fire blight disease. Pest Technology 1:76–80

    Google Scholar 

  • Kokoskova B, Pouvova D, Pavela R (2011) Effectiveness of plant essential oils against Erwinia amylovora, Pseudomonas syringae pv. syringae and associated saprophytic bacteria on/in host plants. J Plant Pathol 93:133–139

  • Jk K, Felso P, Makszin L, Pápai Z, Horváth ÁH, Palkovics T, Böszörményi A, Emody L, Schneider G (2016) Antimicrobial and virulence-modulating effects of clove essential oil on the foodborne pathogen Campylobacter jejuni. Appl Environ Microbiol 82:6158–6166

  • Lee K, Lee JH, Kim SI, Cho M, Lee J (2014) Anti-biofilm, anti-hemolysis, and anti-virulence activities of black pepper, cananga, myrrh oils, and nerolidol against Staphylococcus aureus. Appl Microbiol Biotechno 98:9447–9457. https://doi.org/10.1007/s00253-014-5903-4

    Article  CAS  Google Scholar 

  • Lewis K, Ausubel FM (2006) Prospects for plant derived antibacterial. Nat Biotechnol 24:1504–1507

    Article  CAS  PubMed  Google Scholar 

  • Lin LI, Stephenson WR (1998) Validating an assay of viral contamination. In: Peck R, Haugh LD, Goodman A (eds) statistical case studies: A collaboration between academe and industry. SIAM, Philadelphia, PA. https://doi.org/10.1137/1.9780898719741.ch7

    Chapter  Google Scholar 

  • Linares JF, Gustafsson I, Baquero F, Martinez JL (2006) Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci U S A of America 103:19484–19489

    Article  CAS  Google Scholar 

  • Lo Cantore P, Iacobellis NS, De Marco A, Capasso F, Senatore F (2004) Antibacterial activity of Coriandrum sativum L. and Foeniculum vulgare Miller var. vulgare (Miller) essential oils. J Agric Food Chem 52:7862–7866. https://doi.org/10.1021/jf0493122

    Article  CAS  PubMed  Google Scholar 

  • Lv F, Liang H, Yuan Q, Li C (2011) In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Res Int 44:3057–3064. https://doi.org/10.1016/j.foodres.2011.07.030

    Article  CAS  Google Scholar 

  • Mirzaei-Najafgholi H, Tarighi S, Golmohammadi M, Taheri P (2017) The effect of citrus essential oils and their constituents on growth of Xanthomonas citri subsp. citri. Molecules 22:1–14

    Article  CAS  Google Scholar 

  • Mitrev S, Kostadinovska E (2016) Isolation and molecular determination of the fire blight pathogen, Erwinia amylovora isolated from apple trees in the republic of Macedonia. J Plant Pathol 98:577–580

    Google Scholar 

  • Mohammadi M (2010) Enhanced colonization and pathogenicity of Erwinia amylovora strains transformed with the near-ubiquitous pEA29 plasmid on pear and apple. Plant Pathol 59:252–261

    Article  CAS  Google Scholar 

  • Nazzaro F, Fratianni F, De Martino L, Coppola R, De Feo V (2013) Effect of essential oils on pathogenic bacteria. Pharmaceuticals 6:1451–1474

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nyenje ME, Gree E, Ndip RN (2012) Biofilm Formation and adherence characteristics of Listeria ivanovii strains isolated from ready-to-eat foods in Alice, South Africa. Scientific World Journal 2012(ID 873909):1–7

    Article  Google Scholar 

  • Obey KJ, Wright VA, Orjala J, Kauhanen J, Tikkanen-Kaukanen C (2016) Antimicrobial activity of Croton macrostachyus stem bark extracts against several human pathogenic bacteria. J Pathog 2016(ID 1453428):1–5

    Article  CAS  Google Scholar 

  • Olanya OM, Larkin RP (2007) Efficacy of essential oils and biopesticides on Phytophthora infestans suppression in laboratory and growth chamber studies. Biocontrol Sci Techn 16:901–917

    Article  Google Scholar 

  • Ozrenk K, Balta F, Celik F (2011) Levels of fire blight (Erwinia amylovora) susceptibility of native apple, pear and quince germplasm from Lake Van Basin, Turkey. Eur J Plant Pathol 132:229–236

    Article  Google Scholar 

  • Piqué N, Miñana-Galbis D, Merino S, Tomás JM (2015) Virulence factors of Erwinia amylovora: a review. Int J Mol Sci 16:12836–12854

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Qiu J, Zhang X, Luo M, Li H, Dong J, Wang J, Leng B, Wang X, Feng H, Ren W, Deng X (2011) Subinhibitory concentrations of Perilla oil affect the expression of secreted virulence factor genes in Staphylococcus aureus. PLoS One 6:1–8

    Google Scholar 

  • Rhouma A, Daoud HB, Ghanmi S, Salah HB, Romdhane M, Demak M (2009) Antimicrobial activities of leaf extracts of Pistacia and Schinus species against some plant pathogenic fungi and bacteria. J Plant Pathol 91:339–345

    Google Scholar 

  • Ruz L, Moragrega C, Montesinos E (2008) Evaluation of four whole-plant inoculation methods to analyze the pathogenicity of Erwinia amylovora under quarantine conditions. Int Microbiol 11:111–119

    PubMed  Google Scholar 

  • Sharifi-Rad J, Miria A, Hoseini-Alfatemic SM, Sharifi-Rad M, Setzere WN, Hadjiakhoondif A (2014) Chemical composition and biological activity of Pulicaria vulgaris essential oil from Iran. Nat Prod Commun 9:1633–1636

    PubMed  Google Scholar 

  • Sikkema J, De Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sundin GW, Wang N (2018) Antibiotic resistance in plant-pathogenic bacteria. Annu Rev Phytopathol 56:161–180

    Article  CAS  PubMed  Google Scholar 

  • Taswell C (1984) Limiting dilution assays for the determination of immunocompetent cell frequencies.III. Validity tests for the single-hit Poisson model. J Immunol Methods 72:29–40

    Article  CAS  PubMed  Google Scholar 

  • Vanneste JL (2000) Fire blight, the disease and its causative agent Erwinia amylovora. In: Vanneste JL (ed) What is fire blight? Who is Erwinia amylovora? How to control it? CABI Publishing, Wallingford, pp 1–6

    Google Scholar 

  • Vanneste JL, Eden-Green S (2000) Fire blight, the disease and its causative agent Erwinia amylovora. In: Vanneste JL (ed) Migration of Erwinia amylovora in host plant tissues. CABI Publishing, New York, pp 73–83

    Google Scholar 

  • Vasinauskiene M, Radu Iene J, Zitikaite I, Surviliene E (2006) Antibacterial activities of essential oils from aromatic and medical plants against growth of phytopathogenic bacteria. Agron Res 4:437–440

    Google Scholar 

  • Vieira M, Bessa LJ, Martins MR, Arantes S, Teixeira APS, Mendes Â, Costa PM, Belo ADF (2017) Chemical composition, antibacterial, antibiofilm and synergistic properties of essential oils from Eucalyptus globulus Labill. and seven Mediterranean aromatic plants. Chem Biodivers 14:1–12. https://doi.org/10.1002/cbdv.201700006

    Article  CAS  Google Scholar 

  • Vrancken K, Holtappels M, Schoofs H, Deckers T, Valcke R (2013) Pathogenicity and infection strategies of the fire blight pathogen Erwinia amylovora in Rosaceae: State of the art. Microbiology 159:823–832

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Korban SS, Pusey PL, Zhao Y (2012) AmyR is a novel negative regulator of amylovoran production in Erwinia amylovora. PLoS One 7:1–11

    Google Scholar 

  • Wang D, Korban SS, Zhao Y (2010) Molecular signature of differential virulence in natural isolates of Erwinia amylovora. Phytopathology 100:8–192

    Google Scholar 

  • Zhao Y, Blumer SE, Sundin GW (2005) Identification of Erwinia amylovora genes induced during infection of immature pear tissue. J Bacteriol 187:8088–8103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Wang D, Nakka S, Sundin GW, Korban SS (2009) Systems level analysis of two-component signal transduction systems in Erwinia amylovora: Role in virulence, regulation of amylovoran biosynthesis and swarming motility. BMC Genomics 10:1–16

    Article  CAS  Google Scholar 

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Acknowledgements

The research was financially supported by Ferdowsi University of Mashhad (Grant number: 3/39797).

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Akhlaghi, M., Tarighi, S. & Taheri, P. Effects of plant essential oils on growth and virulence factors of Erwinia amylovora. J Plant Pathol 102, 409–419 (2020). https://doi.org/10.1007/s42161-019-00446-9

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