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Microparticles containing gallic and ellagic acids for the biological control of bacterial diseases of kiwifruit plants

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Abstract

Over the last decades, kiwifruit cultivation has gained increasing importance all over the world, but some bacterial diseases seriously threaten its cultivation. The most dangerous one is the bacterial canker caused by Pseudomonas syringae pv. actinidiae Takikawa et al., but also floral bud necrosis by Pseudomonas syringae pv. syringae van Hall and bacterial blight by Pseudomonas viridiflava (Burkholder) Dowson affect kiwifruit plants. Their control relies mainly on antibiotics, where allowed, and copper, although this adversely affects the environment, so that alternative control measures are needed. Here we investigate gallic acid and ellagic acid, substances easily obtainable from some plant tissues, for their antimicrobial activity aiming to use them as support in the biocontrol of kiwifruit bacterial diseases. These active principles demonstrated their effectiveness as pure substances in both in vitro and in vivo tests. Moreover, their encapsulation in methacrylate polymeric microparticles showed to improve their usefulness and to prolong remarkably their activity up to 14 days after the treatment, when applied in greenhouse or in field on artificially and naturally infected plants, respectively. The encouraging results obtained by this type of microformulation point the way to future alternative biological control strategies against kiwifruit bacterial diseases.

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References

  • Adachi, S., Imaoka, H., Ashida, H., Maeda, H., & Matsuno, R. (2004). Preparation of microcapsules of W/O/W emulsions containing a polysaccharide in the outer aqueous phase by spray-drying. European Journal of Lipid Science and Technology, 106(4), 225–231. doi:10.1002/ejlt.200300900.

    Article  CAS  Google Scholar 

  • Balestra, G. M., Mazzaglia, A., Quattrucci, A., Renzi, M., & Rossetti, A. (2009a). Occurrence of Pseudomonas syringae pv. actinidiae in Jin Tao kiwi plants in Italy. Phytopathologia Mediterranea, 48(2), 299–301.

    Google Scholar 

  • Balestra, G. M., Mazzaglia, A., Quattrucci, A., Renzi, M., & Rossetti, A. (2009b). Current status of bacterial canker spread on kiwifruit in Italy. Australasian Plant Disease Notes, 4(1), 34–36. doi:10.1071/DN09014.

    Google Scholar 

  • Balestra, G. M., Renzi, M., & Mazzaglia, A. (2010). First report of bacterial canker of Actinidia deliciosa caused by Pseudomonas syringae pv. actinidiae in Portugal. New Disease Reports, 22, 10. doi:10.5197/j.2044-0588.2010.022.010.

    Article  Google Scholar 

  • Balestra, G. M., Renzi, M., & Mazzaglia, A. (2011). First report of Pseudomonas syringae pv. actinidiae on kiwifruit plants in Spain. New Disease Reports. doi:10.5197/j.2044-0588.2011.024.010.

    Google Scholar 

  • Balestra, G. M., & Varvaro, L. (1997). Pseudomonas syringae pv. syringae causal agent of disease on floral buds of Actinidia deliciosa (A. Chev) Liang et Ferguson in Italy. Journal of Phytopathology, 145(8–9), 375–378.

    Article  Google Scholar 

  • Balestra, G. M., & Varvaro, L. (1999). Bacterial diseases on kiwifruit orchards in Italy. Acta Horticulturae 498(498), 355–358.

    Article  Google Scholar 

  • Bastas, K. K., & Karakaya, A. (2012). First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Turkey. Plant Disease, 96(3), 452. doi:10.1094/PDIS-08-11-0675.

    Article  Google Scholar 

  • Braga, L. C., Shupp, J. W., Cummings, C., Jett, M., Takahashi, J. A., Carmo, L. S., et al. (2005). Pomegranate extract inhibits Staphylococcus aureus growth and subsequent enterotoxin production. Journal of Ethnopharmacology, 96(1–2), 335–339. doi:10.1016/j.jep.2004.08.034.

    Article  CAS  PubMed  Google Scholar 

  • Brook, P. J. (1990). Diseases of kiwifruit. In W. Warrington & G. C. Weston (Eds.), Kiwifruit: science and management (pp. 422–424). Auckland: Ray Richards Publisher.

    Google Scholar 

  • Brown, R. P. (2004). Polymers in agriculture and horticulture. RAPRA Review Reports (Vol. 15(2)). Shropshire, UK: Rapra Technology Limited.

  • Burt, S. (2004). Essential oils: their antibacterial properties and potential applications in foods–a review. International Journal of Food Microbiology, 94(3), 223–253. doi:10.1016/j.ijfoodmicro.2004.03.022.

    Article  CAS  PubMed  Google Scholar 

  • Cortesi, R., Esposito, E., Luca, G., & Nastruzzi, C. (2002). Production of lipospheres as carriers for bioactive compounds. Biomaterials, 23(11), 2283–2294. doi:10.1016/S0142-9612(01)00362-3.

    Article  CAS  PubMed  Google Scholar 

  • Cortesi, R., Quattrucci, A., Esposito, E., Mazzaglia, A., & Balestra, G. M. (2016). Natural antimicrobials in spray-dried microparticles based on cellulose derivatives as potential eco-compatible agrochemicals. Journal of Plant Diseases and Protection. doi:10.1007/s41348-016-055-7.

    Google Scholar 

  • Delaquis, P. J., Stanich, K., Girard, B., & Mazza, G. (2002). Antimicrobial activity of individual and mixed fractions of dill, cilantro, coriander and eucalyptus essential oils. International Journal of Food Microbiology, 74(1–2), 101–109. doi:10.1016/S0168-1605(01)00734-6.

    Article  CAS  PubMed  Google Scholar 

  • Donegan, K., Matyac, C., Seidler, R., & Porteous, A. (1991). Evaluation of methods for sampling, recovery, and enumeration of bacteria applied to the phylloplane. Applied and Environmental Microbiology, 57(1), 51–56.

    CAS  PubMed  PubMed Central  Google Scholar 

  • EPPO. (2011). First report of Pseudomonas syringae pv. actinidiae in Switzerland. Reporting Service No. 8.

  • EPPO. (2013). First report of Pseudomonas syringae pv. actinidiae in Germany. Reporting Service No. 9.

  • EPPO. (2014). First report of Pseudomonas syringae pv. actinidiae in Slovenia. Reporting Service No. 2.

  • Esposito, E., Cervellati, F., Menegatti, E., Nastruzzi, C., & Cortesi, R. (2002). Spray dried Eudragit microparticles as encapsulation devices for vitamin C. International Journal of Pharmaceutics, 242(1–2), 329–334. doi:10.1016/S0378-5173(02)00176-X.

    Article  CAS  PubMed  Google Scholar 

  • Esposito, E., Roncarati, R., Cortesi, R., Cervellati, F., & Nastruzzi, C. (2000). Production of Eudragit microparticles by spray-drying technique: Influence of experimental parameters on morphological and dimensional characteristics. Pharmaceutical Development and Technology, 5(2), 267–278. doi:10.1081/PDT-100100541.

    Article  CAS  PubMed  Google Scholar 

  • Everett, K. R., Taylor, R. K., Romberg, M. K., Rees-George, J., Fullerton, R. A., Vanneste, J. L., et al. (2011). First report of Pseudomonas syringae pv. actinidiae causing kiwifruit bacterial canker in New Zealand. Australasian Plant Disease Notes, 6(1), 67–71. doi:10.1007/s13314-011-0023-9.

    Article  Google Scholar 

  • Fortunati, E., Rescignano, N., Botticella, E., La Fiandra, D., Renzi, M., Mazzaglia, A., et al. (2016). Effect of poly(DL-lactide-co-glycolide) nanoparticles or cellulose nanocrystals-based formulations on Pseudomonas syringae pv. tomato (Pst) and tomato plant development. Journal of Plant Diseases an Protection, 123, 301–310.

    Article  Google Scholar 

  • Glazer, I., Masaphy, S., Marciano, P., Bar-Ilan, I., Holland, D., Kerem, Z., et al. (2012). Partial identification of antifungal compounds from Punica granatum peel extracts. Journal of Agricultural and Food Chemistry, 60(19), 4841–4848. doi:10.1021/jf300330y.

    Article  CAS  PubMed  Google Scholar 

  • Glenn, G. M., Klamczynski, A. P., Woods, D. F., Chiou, B., Orts, W. J., & Imam, S. H. (2010). Encapsulation of plant oils in porous starch microspheres. Journal of Agricultural and Food Chemistry, 58(7), 4180–4184. doi:10.1021/jf9037826.

    Article  CAS  PubMed  Google Scholar 

  • Hammer, K. A., Carson, C. F., & Riley, T. V. (1999). Antimicrobial activity of essential oils and other plant extracts. Journal of Applied Microbiology, 86(6), 985–990. doi:10.1046/j.1365-2672.1999.00780.x.

    Article  CAS  PubMed  Google Scholar 

  • Hirano, S. S., & Upper, C. D. (1983). Ecology and epidemiology of foliar bacterial plant pathogens. Annual review of Phytopathology, 21(1), 243–270. doi:10.1146/annurev.py.21.090183.001331.

    Article  Google Scholar 

  • Hirano, S. S., & Upper, C. D. (2000). Bacteria in the Leaf Ecosystem with Emphasis on Pseudomonas syringae -a Pathogen, Ice Nucleus, and Epiphyte. Microbiology and Molecular Biology Reviews, 64(3), 624–653. doi:10.1128/MMBR.64.3.624-653.2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holeva, M. C. C., Glynos, P. E. E., & Karafla, C. D. D. (2015). First report of bacterial canker of kiwifruit caused by Pseudomonas syringae pv. actinidiae in Greece. Plant Disease, 99(5), 723. doi:10.1094/PDIS-07-14-0738-PDN.

    Article  Google Scholar 

  • Jurenka, J. S. (2008). Therapeutic applications of pomegranate (Punica granatum L.): a review. Alternative medicine review: a journal of clinical therapeutic, 13(2), 128–144.

    Google Scholar 

  • Karamaæ, M., Kosiñska, A., & Pegg, R. B. (2006). Content of gallic acid in selected plant extracts. Journal of Food and Nutrition Sciences, 15(1), 55–58.

    Google Scholar 

  • Klement, Z., Rudolph, K., & Sands, D. C. (1990). Methods in phytobacteriology. Budapest: Akademiai Kiado.

  • Koh, Y. J., Chung, H. J., Cha, B. J., & Lee, D. H. (1994). Outbreak and spread of bacterial canker in kiwifruit. Korean Journal of Plant Pathology, 10, 68–72.

    Google Scholar 

  • Lehmann, K., Rothgang, G., Boessler, H., Dreher, D., & Petereit, H. U. (1989). Practical course in Lacquer coating. Weiterstadt: Rohm Pharma GMBH.

    Google Scholar 

  • Martini, S., D’Addario, C., Colacevich, A., Focardi, S., Borghini, F., Santucci, A., et al. (2009). Antimicrobial activity against Helicobacter pylori strains and antioxidant properties of blackberry leaves (Rubus ulmifolius) and isolated compounds. International Journal of Antimicrobial Agents, 34(1), 50–59. doi:10.1016/j.ijantimicag.2009.01.010.

    Article  CAS  PubMed  Google Scholar 

  • Mohamed Sham Shihabudeen, H., Hansi Priscilla, D., & Thirumurugan, K. (2010). Antimicrobial activity and phytochemical analysis of selected Indian folk medicinal plants. International Journal of Pharma Sciences and Research (IJPSR), 1(10), 430–434.

    Google Scholar 

  • Muganu, M., & Paolocci, M. (2013). Adaptation of local grapevine germplasm: exploitation of natural defence mechanisms to biotic stresses. In D. Poljuha & B. Sladonja (Ed.), The Mediterranean Genetic Code—Grapevine and Olive. InTech. doi:10.5772/51976

  • Nagajyoti, P. C., Lee, K. D., & Sreekanth, T. V. M. (2010). Heavy metals, occurrence and toxicity for plants: A review. Environmental Chemistry Letters. doi:10.1007/s10311-010-0297-8.

    Google Scholar 

  • Naz, S., Siddiqi, R., Ahmad, S., Rasool, S. A., & Sayeed, S. A. (2007). Antibacterial activity directed isolation of compounds from Punica granatum. Journal of Food Science, 72(9), M341–M345. doi:10.1111/j.1750-3841.2007.00533.x.

    Article  CAS  PubMed  Google Scholar 

  • Negi, P. S., & Jayaprakasha, G. K. (2003). Antioxidant and antibacterial activities of Punica granatum peel extracts. Journal of Food Science, 68(4), 1473–1477.

    Article  CAS  Google Scholar 

  • Orak, H. H., Demirci, A. Ş., & Gümüş, T. (2011). Antibacterial and antifungal activity of pomegranate (Punica granatum L.cv.) peel. Electronic Journal of Environmental, Agricultural and Food Chemistry, 10(3), 1958–1969.

    Google Scholar 

  • Pagliarulo, C., De Vito, V., Picariello, G., Colicchio, R., Pastore, G., Salvatore, P., et al. (2016). Inhibitory effect of pomegranate (Punica granatum L.) polyphenol extracts on the bacterial growth and survival of clinical isolates of pathogenic Staphylococcus aureus and Escherichia coli. Food Chemistry, 190, 824–831. doi:10.1016/j.foodchem.2015.06.028.

    Article  CAS  PubMed  Google Scholar 

  • Paolocci, M., Muganu, M., Alonso-Villaverde, V., & Gindro, K. (2015). Leaf morphological characteristics and stilbene production differently affect downy mildew resistance of Vitis vinifera varieties grown in Italy. VITIS—Journal of Grapevine Research, 53(3), 155.

    Google Scholar 

  • Patent EU 1484956 A2. (2004). A product for use in agriculture or horticulture.

  • Patent US 20130065755 A1. (2013). Controlled release of seed and soil treatments triggered by pH change of growing media.

  • Pätsikkä, E., Kairavuo, M., Sersen, F., Aro, E.-M., & Tyystjärvi, E. (2002). Excess copper predisposes photosystem II to photoinhibition in vivo by outcompeting iron and causing decrease in leaf chlorophyll. Plant Physiology, 129(July), 1359–1367. doi:10.1104/pp.004788.

    Article  PubMed  PubMed Central  Google Scholar 

  • Phaechamud, T., Mahadlek, J., & Charoenteeraboon, J. (2014). Antimicrobial activity of in situ forming gel comprising cork tree seed extract. Acta Horticulturae, 1023(53–58), 2014. doi:10.17660/ActaHortic.2014.1023.6.

    Google Scholar 

  • Prashanth, D., Asha, M. K., & Amit, A. (2001). Antibacterial activity of Punica granatum. Fitoterapia, 72(2), 171–173. doi:10.1016/S0367-326X(00)00270-7.

    Article  CAS  PubMed  Google Scholar 

  • ProMed. (2011). Bacterial canker, kiwifruit–Chile: first report: (O’Higgins, Maule). Posting no. 20110325.0940.

  • Quattrucci, A., Ovidi, E., Tiezzi, A., Vinciguerra, V., & Balestra, G. M. (2013). Biological control of tomato bacterial speck using Punica granatum fruit peel extract. Crop Protection, 46, 18–22. doi:10.1016/j.cropro.2012.12.008.

    Article  Google Scholar 

  • Renzi, M., Copini, P., Taddei, A. R., Rossetti, A., Gallipoli, L., Mazzaglia, A., et al. (2012). Bacterial canker on kiwifruit in Italy: anatomical changes in the wood and in the primary infection sites. Phytopathology, 102(9), 827–840. doi:10.1094/PHYTO-02-12-0019-R.

    Article  PubMed  Google Scholar 

  • Romeo, F. V., Ballistreri, G., Fabroni, S., Pangallo, S., Nicosia, Li Destri, et al. (2015). Chemical characterization of different sumac and pomegranate extracts effective against Botrytis cinerea rots. Molecules, 20(7), 11941–11958. doi:10.3390/molecules200711941.

    Article  CAS  PubMed  Google Scholar 

  • Rossetti, A., & Balestra, G. M. (2008). Pseudomonas syringae pv. syringae on kiwifruit plants: epidemiological traits and its control. In M. Fatmi, A. Collmer, N. S. Iacobellis, J. W. Mansfield, J. Murillo, N. W. Schaad, & M. Ullrich (Eds.), Pseudomonas syringae Pathovars and Related Pathogens (pp. 65–68). Dordrecht: Springer. doi:10.1007/978-1-4020-6901-7.

    Google Scholar 

  • Satish, S., Raveesha, K. A., & Janardhana, G. R. (1999). Antibacterial activity of plant extracts on phytopathogenic Xanthomonas campestris pathovars. Letters in Applied Microbiology, 28(2), 145–147.

    Article  Google Scholar 

  • Scalbert, A. (1991). Antimicrobial properties of tannins. Phytochemistry. doi:10.1016/0031-9422(91)83426-L.

    Google Scholar 

  • Serizawa, S., Ichikawa, T., Takikawa, Y., Tsuyumu, S., & Goto, M. (1989). Occurrence of bacterial canker of kiwifruit in Japan: Description of symptoms, isolation of the pathogen and screening of bactericides. Japanese Journal of Phytopathology, 55(4), 427–436. doi:10.3186/jjphytopath.55.427.

    Article  Google Scholar 

  • Sharma, R. R., & Pongener, A. (2010). Natural products for postharvest decay control in horticultural produce: A review. Stewart Postharvest Review. doi:10.2212/spr.2010.4.1.

    Google Scholar 

  • Steel, R. G. D., Torrie, J. H., Dickey, D., & Hiram, J. (1997). Principles and Procedures of Statistics: a Biometrical Approach. New York: McGraw-Hill.

    Google Scholar 

  • Takei, T., Yoshida, M., Hatate, Y., Shiomori, K., & Kiyoyama, S. (2008). Preparation of polylactide/poly (ε-caprolactone) microspheres enclosing acetamiprid and evaluation of release behavior. Polymer Bulletin. 61(3), 391–397.

    Article  CAS  Google Scholar 

  • Takikawa, Y., Serizawa, S., Ichikawa, T., Tsuyumu, S., & Goto, M. (1989). Pseudomonas syringae pv. actinidiae pv. nov.: the causal bacterium of canker of kiwifruit in Japan. Annals of the Phytopathological Society of Japan, 55(4), 437–444. doi:10.3186/jjphytopath.55.437.

    Article  Google Scholar 

  • Tanyolaç, D., Ekmekçi, Y., & Ünalan, Ş. (2007). Changes in photochemical and antioxidant enzyme activities in maize (Zea mays L.) leaves exposed to excess copper. Chemosphere, 67(1), 89–98. doi:10.1016/j.chemosphere.2006.09.052.

    Article  PubMed  Google Scholar 

  • Tsuchiya, H., Sato, M., Miyazaki, T., Fujiwara, S., Tanigaki, S., Ohyama, M., et al. (1996). Comparative study on the antibacterial activity of phytochemical flavanones against methicillin-resistant Staphylococcus aureus. Journal of Ethnopharmacology, 50(1), 27–34. doi:10.1016/0378-8741(96)85514-0.

    Article  CAS  PubMed  Google Scholar 

  • Vanneste, J. L., Poliakoff, F., Audusseau, C., Cornish, D. A., Paillard, S., Rivoal, C., et al. (2011). First report of Pseudomonas syringae pv. actinidiae, the causal agent of bacterial canker of kiwifruit in France. Plant Disease, 95(10), 1311. doi:10.1094/PDIS-03-11-0195.

    Article  Google Scholar 

  • Varvaro, L., & Balestra G. M. (1998). Seasonal fluctuations in kiwifruit phyllosphere and ice nucleation activity of Pseudomonas viridiflava. Journal of Plant Pathology. 80(1), 151–156.

    Google Scholar 

  • Vattem, D. A., & Shetty, K. (2005). Biological functionality of ellagic acid: A review. Journal of Food Biochemistry. doi:10.1111/j.1745-4514.2005.00031.x.

    Google Scholar 

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Acknowledgements

Authors thank Ministry of Agriculture, Food and Forestry of Italy MIPAAF for financial support (BBB PAN-2009). Authors are grateful to Dr. Andrea Costenaro for technical issues.

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Authors and Affiliations

  1. Department of Agricultural and Forestry Science (DAFNE), University of Tuscia, Viterbo, Italy

    Antonio Rossetti, Angelo Mazzaglia, Massimo Muganu, Marco Paolocci & Giorgio Mariano Balestra

  2. Department of Life Sciences and Biotechnology (SVeB), University of Ferrara, Ferrara, Italy

    Maddalena Sguizzato, Elisabetta Esposito & Rita Cortesi

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  1. Antonio Rossetti
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  2. Angelo Mazzaglia
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  3. Massimo Muganu
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  8. Giorgio Mariano Balestra
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Correspondence to Giorgio Mariano Balestra.

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Rossetti, A., Mazzaglia, A., Muganu, M. et al. Microparticles containing gallic and ellagic acids for the biological control of bacterial diseases of kiwifruit plants. J Plant Dis Prot 124, 563–575 (2017). https://doi.org/10.1007/s41348-017-0096-6

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