Advertisement

Phytoparasitica

, Volume 47, Issue 5, pp 733–741 | Cite as

Synthesis and in planta antibacterial activity of head-to-head bis-benzimidazole and bis-benzoxazole derivatives

  • Amal Smaili
  • Said Jebbari
  • Lalla Aicha Rifai
  • Lydia Faize
  • Tayeb Koussa
  • Houssine Ait Sir
  • Kacem Makroum
  • Malika Belfaiza
  • Abdellatif El Kihel
  • Mustapha Ahbala
  • Jean Stéphane Venisse
  • Mohamed FaizeEmail author
Article
  • 12 Downloads

Abstract

A series of head-to-head bis-benzimidazole and bis-benzoxazole derivatives was synthetized. Their antibacterial activity was examined in planta against Pseudomonas syringae pv. tabaci, the causal agent of wild fire in tobacco and in vitro against Pseudomonas syringae pv. tabaci and Pseudomonas syringae pv. tabaci. All synthetized compounds did not inhibit bacterial growth in vitro. However, they protected Nicotiana benthamiana against P. syringae pv. tabaci in the greenhouse. Only one foliar application at 50 μg ml−1 reduced diameter of leaf lesion by 25 to 52% as well as bacterial population in planta by 0.4 to 0.9 logarithmic units. This protection was associated with the inhibition of the accumulation of H2O2in planta and enhancement of the activity of catalase, ascorbate peroxidase and guaiacol peroxidase. These results suggest that the bis-benzoimidazole and bis-benzoxazole derivatives act as antioxidants and may be used to protect plants against bacterial diseases.

Keywords

Antioxidant Bis-benzimidazole Bis-benzoxazole Protection Nicotiana benthamiana Pseudomonas syringae pv. tabaci 

Notes

Acknowledgements

This work was supported by the University Chouaib Doukkali El Jadida. The authors are grateful to Professor S. El Idrissi for reviewing the English of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

12600_2019_764_MOESM1_ESM.docx (132 kb)
ESM 1 (DOCX 131 kb)

References

  1. Alexieva, V., Sergiev, I., Mapelli, S., & Karanov, E. (2001). The effect of drought and ultraviolet radiation growth and stress markers in pea and wheat. Plant Cell Environment, 24, 1337–1344.CrossRefGoogle Scholar
  2. Anterola, A. M., & Lewis, N. G. (2002). Trends in lignin modification: A comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry, 61, 221–234.CrossRefGoogle Scholar
  3. Barker, H. A., Smyth, R. D., Weissbach, H., Toohey, J. I., Ladd, J. N., & Volcani, B. E. (1960). Isolation and properties of crystalline cobamide coenzymes containing Benzimidazole or 5,6- Dimethylbenzimidazole. Journal of Biological Chemistry, 235, 480–488.PubMedGoogle Scholar
  4. Colombi, E., Straub, C., Kunzel, S., Templeton, D., McCann, H. C., & Rainey, P. B. (2017). Evolution of copper resistance in the kiwifruit pathogen Pseudomonas syringae pv. actinidiae through acquisition of integrative conjugative elements and plasmids. Environmental Microbiology, 19, 819–832.CrossRefGoogle Scholar
  5. Dale, A. G., Hinds, J., Mann, J., Taylor, P. W., & Neidle, S. (2012). Symetric bis-benzimidazoles are potent anti-staphylococcal agents with dual inhibitory mechanisms against DNA gyrase. Biochemistry, 51, 5860–5871.CrossRefGoogle Scholar
  6. Das, K., & Royshoudhri, A. (2014). Reactive oxygen species (ROS) and responses of antioxidants as ROS scavengers during environmental stress in plants. Frontiers in Environmental Sciences, 2, 53.  https://doi.org/10.3389/fenvs.2014.00053.CrossRefGoogle Scholar
  7. Esserti, S., Smaili, A., Makroum, K., Belfaiza, M., Rifai, L. A., Koussa, T., Kasmi, I., & Faize, M. (2018). Priming of Nicotiana Benthamiana antioxidant defenses using brown seaweed extracts. Journal of Phytopathology, 166, 86–94.CrossRefGoogle Scholar
  8. Faize, L., & Faize, M. (2018). Functional analogues of salicylic acid and their use in crop protection. Agronomy, 8, 5  https://doi.org/10.3390/agronomy8010005.CrossRefGoogle Scholar
  9. Faize, M., Faize, L., & Ishii, H. (2009). Gene expression during Acibenzolar-S-methyl-induced priming for potentiated responses to Venturia nashicola in Japanese pear. Journal of Phytopathology, 157, 137–144.CrossRefGoogle Scholar
  10. Faize, M., Faize, L., Petri, C., Barba-Espin, G., Diaz-Vivancos, P., Clemente Moreno, M. J., Koussa, T., Rifai, L. A., Burgos, L., & Hernandez, J. A. (2013). Cu/Zn superoxide dismutase and ascorbate peroxidase enhance in vitro shoot multiplication in transgenic plum. Journal of Plant Physiology, 170, 625–632.CrossRefGoogle Scholar
  11. Guo, Y. S., Su, X. K., Cai, L. T., & Wang, H. C. (2017). Phenotypic characterization of Pseudomonas syringae pv. tabaci, the causal agent of tobacco wildfire. Journal of Plant Pathology, 99, 499–504.Google Scholar
  12. Hu, L., Kully, M. L., Boykin, W., & Abood, N. (2009). Optimization of the central linker of dicationic bis-benzimidazole anti-MRSA and anti-VRE agents. Bioorganic and Medicinal Chemistry Letters, 19, 3374–3377.CrossRefGoogle Scholar
  13. Laber, B., Usunow, G., Wiecko, E., Franke, W., Frank, H., & Köhn, A. (1999). Inhibition of narcissus pseudonarcissus phytoene desaturase by herbicidal 3-trifluoromethyl-1,1-biphenyl derivatives. Pesticide Biochemistry and Physiology, 63, 173–184.CrossRefGoogle Scholar
  14. Lamichhane, J. R., Messean, A., & Morris, C. (2015). Insights into epidemiology and control of diseases of annual plants caused by the Pseudomonas syringae species complex. Journal of General Plant Pathology, 81, 331–350.CrossRefGoogle Scholar
  15. Lindeberg, M., Myers, C. R., Collmer, A., & Schneider, D. J. (2008). Roadmap to new virulence determinants in Pseudomonas syringae: Insights from comparative genomics and genome organization. Molecular Plant Microbe-Interaction, 21, 685–700.CrossRefGoogle Scholar
  16. Lipsitch, M., Singer, R. S., & Levin, B. R. (2002). Antibiotics in agriculture: When it is time to close the barn door? Proceeding of the National Academic Sciences USA, 99, 5572–5574.CrossRefGoogle Scholar
  17. Liu, Y., & He, C. (2016). Regulation of reactive oxygen species (ROS) in stress responses: Learning from AtRBOH. Plant Cell Reports, 35, 995–1007.CrossRefGoogle Scholar
  18. Mckee, M. L., & Kerwin, S. M. (2008). Synthesis and evaluation of 2-(2′-hydroxyphenyl)benzoxazole analogues of UK-1 as anticancer agents. Bioorganic and Medicinal Chemistry, 6, 1775–1783.CrossRefGoogle Scholar
  19. Moreira, J. B., Mann, J., Neidle, S., McHugh, T. D., & Taylor, P. W. (2013). Antibacterial activity of head-to-head bis-benzimidazoles. International Journal of Antimicrobial Agents, 42, 361–366.CrossRefGoogle Scholar
  20. Oehlers, L., Mazzitelli, C. L., Brodbelt, J. S., Rodriguez, M., & Kerwin, S. (2004). Evaluation of complexes of DNA duplexes and novel benzoxazoles or benzimidazoles by electrospray ionization mass spectrometry. Journal of the American Society of Mass Spectrometry, 15, 1593–1603.CrossRefGoogle Scholar
  21. Oh, H. S., Park, D. H., & Collmer, A. (2010). Components of the Pseudomonas syringae type III secretion system can suppress and may elicit plant innate immunity. Molecular Plant-Microbe Interaction, 23, 727–739.CrossRefGoogle Scholar
  22. Padmavathi, V., Venkatesh, B. C., Murali Krishna, A., & Padmaja, A. (2012). The reactivity of gem cyanoester keteno dithiolates toward the development of potent antioxidant heterocycles. Chemical and Pharmaceutical Bulletin, 60, 449–458.CrossRefGoogle Scholar
  23. Pernezny, K., Kudela, V., Kokoskova, B., & Hladka, I. (1995). Bacterial diseases of tomato in the Czech and Slovak republics and lack of streptomycin resistance among copper-tolerant bacterial strains. Crop Protection, 14, 267–270.CrossRefGoogle Scholar
  24. Rajasekhar, S., Barnali, M., Balamurali, M. M., & Kaushik, C. (2017). Synthesis and medicinal applications of benzimidazoles: An overview. Current Organic Synthesis, 14, 1–21.CrossRefGoogle Scholar
  25. Sangeetha, R. (2010). Activity of superoxide dismutase and catalase in fenugreek (Trigonella foenum-graecum) in response to carbendazim. Indian Journal of Pharmaceutical Sciences, 72, 116–118.CrossRefGoogle Scholar
  26. Saxena, R. K., Puri, S., & Prakash, R. (2003). Synthesis and evaluation of 2-mercaptoacetylaminobenzoxazole-2-yl thiadiazoles as potent anti-helminthic agents. Indian Journal of Heterocycle Chemistrty, 13, 127–134.Google Scholar
  27. Smaili, A., Mazoir, N., Rifai, L. A., Koussa, T., Makroum, K., Benharref, A., Faize, L., Alburquerque, N., Burgos, L., Belfaiza, M., & Faize, M. (2017). Antimicrobial activity of two semisynthetic triterpene derivatives from Euphorbia officinarum latex against fungal and bacterial phytopathogens. Natural Product Communications, 12, 331–336.CrossRefGoogle Scholar
  28. Smita Nayyar, H. (2005). Carbendazim alleviates effects of water stress on chickpea seedlings. Biologia Plantarum, 49, 289–291.CrossRefGoogle Scholar
  29. Sorrenti, V., Salerno, L., Di Giacomo, C., Acquaviva, R., Siracusa, M. A., & Vanella, A. (2006). Imidazole derivatives as antioxidants and selective inhibitors of nNOS. Nitric Oxide, 14, 45–50.CrossRefGoogle Scholar
  30. Tavman, A., Ikiz, S., Bagcigil, A. F., Ozgur, N. Y., & Ak, S. (2009). Preparation, characterization and antibacterial effect of 2-methoxy-6-(5-H/Me/Cl/NO2-1H-benzimidazol-2-yl)phenols and some transition metal complexes. Journal of Serbian Chemistry Society, 74, 537–548.CrossRefGoogle Scholar
  31. Tumosiene, I., Peleckis, A., Jonuskiene, I., Vaickelioniene, R., Kantminiene, K., Siugzdaite, J., Beresnevicius, Z. J., & Mickevicius, V. (2018). Synthesis of novel 1,2- and 2-substituted benzimidazoles with high antibacterial and antioxidant activity. Monatshefte fur Chemistry, 149, 577–594.CrossRefGoogle Scholar
  32. Unlu, S., Baytas, S. N., & Kupeli, E. (2003). Synthesis of [7-acyl-5-chloro-2-oxo-3H-benzoxazole-3-yl] alkanoic acid derivatives for their anti-inflamatory activity. Archives of Pharmaceutical and Medicinal Chemistry, 336, 310–321.CrossRefGoogle Scholar
  33. Young, J. M. (2010). Taxonomy of Pseudomonas syringae. Journal of Plant Pathology, 92, S1.5–S1.14.Google Scholar
  34. Zhang, L. Z., Wei, N., Wu, Q. X., & Ping, & M. L. (2007). Anti-oxidant response of Cucumis sativus L. to fungicide carbendazim. Pesticide Biochemistry and Physiology, 89, 54–59.Google Scholar
  35. Zhang, Y., Dia, D. J., Wang, H. D., & Zhang, C. Q. (2016). Management of benzimidazole fungicide resistance in eggplant brown rot (Phomopsis vexans) with pyraclostrobin. Phytoparasitica, 44, 313–324.CrossRefGoogle Scholar
  36. Zhou, Y., Xue, N., & Wang, G. (2010). Synthesis and herbicidal activity of pyrazolyl benzoxazole derivatives. Journal of Heterocycle Chemistry, 48, 15–21.Google Scholar
  37. Zine, H., Rifai, L. A., Faize, M., Smaili, A., Makroum, K., Belfaiza, M., Kabil, E. M., & Koussa, T. (2016). Duality of acibenzolar-S-methyl in the inhibition of pathogen growth and induction of resistance during the interaction tomato/Verticillium dahliae. European Journal of Plant Pathology, 145, 61–69.CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Amal Smaili
    • 1
  • Said Jebbari
    • 2
  • Lalla Aicha Rifai
    • 1
  • Lydia Faize
    • 3
  • Tayeb Koussa
    • 1
  • Houssine Ait Sir
    • 2
  • Kacem Makroum
    • 1
  • Malika Belfaiza
    • 1
  • Abdellatif El Kihel
    • 2
  • Mustapha Ahbala
    • 2
  • Jean Stéphane Venisse
    • 4
  • Mohamed Faize
    • 1
    Email author
  1. 1.Laboratory of Plant Biotechnology, Ecology and Ecosystem Valorization, Faculty of SciencesUniversity Chouaib DoukkaliEl JadidaMorocco
  2. 2.Laboratory of Bioorganic Chemistry, Department of Chemistry, Faculty of SciencesUniversity Chouaib DoukkaliEl JadidaMorocco
  3. 3.Group of Fruit Tree Biotechnology, Department of Plant BreedingMurciaSpain
  4. 4.PIAF-UMR547University Blaise PascalAubierreFrance

Personalised recommendations