Examining the response of Botrytis cinerea to aqueous ozone: inactivation kinetics, structure, physiology, and growth in different strawberries cultivars

References

• Aslam, R., Alam, M. S., & Saeed, P. A. (2020). Sanitization potential of ozone and its role in postharvest quality management of fruits and vegetables. Food Engineering Reviews, 12(1), 48–11. https://doi.org/10.1007/s12393-019-09204-0
   Web of Science ®Google Scholar
• Bardas, G. A., Veloukas, T., Koutita, O., & Karaoglanidis, G. S. (2010). Multiple resistance of Botrytis cinerea from kiwifruit to SDHIs, QoIs and fungicides of other chemical groups. Pesticide Management Science, 66(9), 967–973. https://doi.org/10.1002/ps.1968
   PubMed Web of Science ®Google Scholar
• Bestfleisch, M., Luderer-Pfimpfl, M., Höfer, M., Schulte, E., Wünsche, J. N., Hanke, M. V., & Flachowsky, H. (2015). Evaluation of strawberry (Fragaria L.) genetic resources for resistance to Botrytis cinerea. Plant Pathology, 64(2), 396–405. https://doi.org/10.1111/ppa.12278
   Web of Science ®Google Scholar
• Bi, K., Liang, Y., Mengiste, T., & Sharon, A. (2023). Killing softly: A roadmap of Botrytis cinerea pathogenicity. Trends in Plant Science, 28(2), 211–222. https://doi.org/10.1016/j.tplants.2022.08.024
   PubMed Web of Science ®Google Scholar
• Brul, S., Nussbaum, J., & Dielbandhoesing, S. K. (1997). Fluorescence probes for wall porosity and membrane integrity in filamentous fungi. Journal of Microbiological Methods, 28(3), 169–178. https://doi.org/10.1016/S0167-7012(97)00975-5
   Web of Science ®Google Scholar
• Butt, T. M., Hoch, H. C., Staples, R. C., & Leger, R. J. (1989). Use of fluorochromes in the study of fungal cytology and differentiation. Experimental Mycology, 13(4), 303–320. https://doi.org/10.1016/0147-5975(89)90026-1
   Google Scholar
• Contigiani, E. V., Jaramillo- Sánchez, G., Castro, M. A., Gómez, P. L., & Alzamora, S. M. (2018). Postharvest quality of strawberry fruit (Fragaria x Ananassa Duch cv. Albion) as affected by ozone washing: Fungal spoilage, mechanical properties, and structure. Food and Bioprocess Technology, 11(9), 1639–1650. https://doi.org/10.1007/s11947-018-2127-0
   Web of Science ®Google Scholar
• Contigiani, E. V., Kronberg, M. F., Jaramillo-Sánchez, G., Gómez, P. L., Garcia-Loredo, A. B., Munarriz, E., & Alzamora, S. M. (2020). Ozone washing decreases strawberry susceptibility to Botrytis cinerea while maintaining antioxidant, optical and sensory quality. Heliyon, 6(11), e05416. https://doi.org/10.1016/j.heliyon.2020.e05416
   PubMed Web of Science ®Google Scholar
• Cosseboom, S. D., Ivors, K. L., Schnabel, G., Bryson, P. K., & Holmes, G. J. (2019). Within-season shift in fungicide resistance profiles of botrytis cinerea in California Strawberry fields. Plant Disease, 103(1), 59–64. https://doi.org/10.1094/PDIS-03-18-0406-RE
   PubMed Web of Science ®Google Scholar
• Dean, R., Van Kan, J. A. L., Pretorius, Z. A., Hammond-Kosack, K. E., DiPietro, A., Spanu, P. D., Rudd, J. J., Dickman, M., Kahmann, R., Ellis, J., & Foster, G. D. (2012). The top 10 fungal pathogens in molecular plant pathology. Molecular Plant Pathology, 13(4), 414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
   PubMed Web of Science ®Google Scholar
• Dijksterhuis, J. (2017). The fungal spores and food spoilage. Current Opinion in Food Science, 17, 68–74. https://doi.org/10.1016/j.cofs.2017.10.006
   Web of Science ®Google Scholar
• Epelle, E. I., Macfarlane, A., Cusack, M., Burns, A., Okolie, J. A., Mackay, W., Rateb, M., & Yaseen, M. (2023). Ozone application in different industries: A review of recent developments. Chemical Engineering Journal, 5(454), 140188. https://doi.org/10.1016/j.cej.2022.140188
   Google Scholar
• Fröhling, A., & Schlüter, O. (2015). Flow cytometric evaluation of physico-chemical impact on gram-positive and gram-negative bacteria. Frontiers in Microbiology, 6, 939. https://doi.org/10.3389/fmicb.2015.00939
   PubMed Web of Science ®Google Scholar
• Garcia-Loredo, A. B., Guerrero, S. N., & Alzamora, S. M. (2015). Inactivation kinetics and growth dynamics during cold storage of Escherichia coli ATCC 11229, listeria innocua ATCC 33090 and Saccharomyces cerevisiae KE162 in peach juice using aqueous ozone. Innovative Food Science and Emerging Technologies, 29, 271–279. https://doi.org/10.1016/j.ifset.2015.02.007
   Web of Science ®Google Scholar
• Glaze, W. H. (1986). Reaction products of ozone: A review. Environmental Health Perspectives, 69, 151–157. https://doi.org/10.1289/ehp.8669151
   PubMed Web of Science ®Google Scholar
• Hewitt, C. J., Bellara, S. R., Andreani, A., Nebe von Caron, G., & Mcfarlane, C. M. (2001). An evaluation of the anti-bacterial action of ceramic powder slurries using multiparameter flow cytometry. Biotechnology Letters, 23(9), 667–675. https://doi.org/10.1023/A:1010379714673
   Web of Science ®Google Scholar
• Hunt, N. K., & MariñMariñAs, B. J. (1999). Inactivation of Escherichia coli with ozone: Chemical and inactivation kinetics. Water Research, 33(11), 2633–2691. https://doi.org/10.1016/S0043-1354(99)00115-3
   Web of Science ®Google Scholar
• Kang, M. H., Pengkit, A., Choi, K., Jeon, S. S., Choi, H. W., Shin, D. B., Choi, E. H., Uhm, H. S., Park, G., & Wang, Z. (2015). Differential inactivation of fungal spores in water and on seeds by ozone and arc discharge plasma. PLOS ONE, 10(9), e0139263. https://doi.org/10.1371/journal.pone.0139263
   PubMed Web of Science ®Google Scholar
• Kangasjärvi, J., Talvinen, J., Utriainen, M., & Karjalainen, R. (1994). Plant defence systems induced by ozone. Plant, Cell & Environment, 17(7), 783–794. https://doi.org/10.1111/j.1365-3040.1994.tb00173.x
   Web of Science ®Google Scholar
• Li, H., Larsen, D. L., Cao, R., van de Peppel, A. C., Tikunov, Y. M., Marcelis, L. F. M., Woltering, E. J., van Kan, J. A. L., & Schouten, R. E. (2022). The association between the susceptibility to Botrytis cinerea and the levels of volatile and non-volatile metabolites in red ripe strawberry genotypes. Food Chemistry, 393, 133252. https://doi.org/10.1016/j.foodchem.2022.133252
   PubMed Web of Science ®Google Scholar
• Minas, I. S., Karaoglanidis, G. S., Manganaris, G. A., & Vasilakakis, M. (2010). Effect of ozone application during cold storage of kiwifruit on the development of stem-end rot caused by botrytis cinerea. Postharvest Biology and Technology, 58(3), 203–210. https://doi.org/10.1016/j.postharvbio.2010.07.002
   Web of Science ®Google Scholar
• Muthusamy, M., & Lee, S. I. (2024). Abiotic stress-induced secondary metabolite production in Brassica: Opportunities and challenges. Frontiers in Plant Science, 14, 1323085. https://doi.org/10.3389/fpls.2023.1323085
   PubMed Web of Science ®Google Scholar
• Nadas, A., Olmo, M., & García, J. M. (2003). Growth of Botrytis cinerea and strawberry quality in ozone‐enriched atmospheres. Journal of Food Science, 68(5), 1798–1802. https://doi.org/10.1111/j.1365-2621.2003.tb12332.x
   Web of Science ®Google Scholar
• Orozco-Mosqueda, M. C., Kumar, A., Fadiji, A. E., Babalola, O. O., Puopolo, G., & Santoyo, G. (2023). Agroecological management of the grey mould fungus Botrytis cinerea by plant growth-promoting bacteria. Plants, 12(3), 637. https://doi.org/10.3390/plants12030637
   Google Scholar
• Pagès, M., Kleiber, D., Pierron, R. J., & Violleau, F. (2015). Ozone effects on Botrytis cinerea conidia using a bubble column: Germination inactivation and membrane phospholipids oxidation. Ozone: Science & Engineering, 38(1), 62–69. https://doi.org/10.1080/01919512.2015.1074856
   Web of Science ®Google Scholar
• Pandiselvam, R., Subhashini, S., Banuu Priya, E. P., Kothakota, A., Ramesh, S. V., & Shahir, S. (2019). Ozone based food preservation: A promising green technology for enhanced food safety. Ozone: Science & Engineering, 41(1), 17–34. https://doi.org/10.1080/01919512.2018.1490636
   Web of Science ®Google Scholar
• Peleg, M. (1999). On calculating sterility in thermal and non-thermal preservation methods. Food Research International, 32(4), 271–278. https://doi.org/10.1016/S0963-9969(99)00081-2
   Web of Science ®Google Scholar
• Peleg, M., & Cole, M. B. (1998). Reinterpretation of microbial survival curves. Critical Reviews in Food Science and Nutrition, 38(5), 353–380. https://doi.org/10.1080/10408699891274246
   PubMed Web of Science ®Google Scholar
• Petrasch, S., Knapp, S. J., van Kan, J. A. L., & Blanco-Ulate, B. (2019). Grey mould of strawberry, a devastating disease caused by the ubiquitous necrotrophic fungal pathogen Botrytis cinerea. Molecular Plant Pathology, 20(6), 877–892. https://doi.org/10.1111/mpp.12794
   PubMed Web of Science ®Google Scholar
• Ramamurthy, T., Ghosh, A., Pazhani, G. P., & Shinoda, S. (2014). Current perspectives on viable but non-culturable (VBNC) pathogenic bacteria. Frontiers in Public Health, 2, 103. https://doi.org/10.3389/fpubh.2014.00103
   PubMedGoogle Scholar
• Rangel, K., Cabral, F. O., Lechuga, G. C., Carvalho, J. P. R. S., Villas- BôBôAs, M. H. S., Midlej, V., & De Simone, S. G. (2022). Detrimental effect of ozone on pathogenic bacteria. Microorganisms [Internet], 10(1), 40. https://doi.org/10.3390/microorganisms10010040
   Web of Science ®Google Scholar
• Romero-Bernal, A. R., Contigiani, E. V., González, H. H. L., Alzamora, S. M., Gómez, P. L., & Raffellini, S. (2019). Botrytis cinerea response to pulsed light: Cultivability, physiological state, ultrastructure and growth ability on strawberry fruit. International Journal of Food Microbiology, 309, 1–8. https://doi.org/10.1016/j.ijfoodmicro.2019.108311
   Web of Science ®Google Scholar
• Šamec, D., Karalija, E., Šola, I., Vujčić Bok, V., & Salopek-Sondi, B. (2021). The role of polyphenols in abiotic stress response: The influence of molecular structure. Plants, 10(1), 118. https://doi.org/10.3390/plants10010118
   Google Scholar
• Šamec, S., Maretic’, M., Lugaric’, I., Mešic’, A., Salopek-Sondi, B., & Duralija, B. (2016). Assessment of the differences in the physical, chemical and phytochemical properties of four strawberry cultivars using principal component analysis. Food Chemistry, 194, 828–834. https://doi.org/10.1016/j.foodchem.2015.08.095
   PubMed Web of Science ®Google Scholar
• Sandermann, H. J., Ernst, D., Heller, W., & Langebartels, C. (1998). Ozone: An abiotic elicitor of plant defense reactions. Trends in Plant Science Reviews, 3(2), 47–50. https://doi.org/10.1016/S1360-1385(97)01162-X
   Web of Science ®Google Scholar
• Savi, G. D., & Scussel, V. M. (2014). Effects of ozone gas exposure on toxigenic fungi species from fusarium, Aspergillus, and Penicillium genera. Ozone: Science & Engineering, 36(2), 144–152. https://doi.org/10.1080/01919512.2013.846824
   Web of Science ®Google Scholar
• Tuffi, R., Lovino, R., Canese, S., Cafiero, L. M., & Vitali, F. (2012). Effects of exposure to gaseous ozone and negative air ions on control of epiphytic flora and the development of Botrytis cinerea and Penicillium expansum during cold storage of strawberries and tomatoes. Italian Journal of Food Science, 4(2), 102.
   Google Scholar
• Tzortzakis, N. (2023). Preservation of fresh strawberries in an ozone-enriched atmosphere. Acta Horticulturae, 1363(1363), 212–220. https://doi.org/10.17660/ActaHortic.2023.1363.32
   Google Scholar
• Veloso, J., & van Kan, J. A. L. (2018). Many shades of grey in Botrytis–host plant interactions. Trends in Plant Sciences, 23(7), 613–622. https://doi.org/10.1016/j.tplants.2018.03.016
   PubMed Web of Science ®Google Scholar
• Wen, G., Liang, Z., Xu, X., Cao, R., Wan, Q., Ji, G., Lin, W., Wang, J., Yang, J., & Huang, T. (2020). Inactivation of fungal spores in water using ozone: Kinetics, influencing factors and mechanisms. Water Research, 185, 116218. https://doi.org/10.1016/j.watres.2020.116218
   PubMed Web of Science ®Google Scholar
• Xue, W., Macleod, J., & Blaxland, J. (2023). The use of ozone technology to control microorganism growth, enhance food safety and extend shelf life: A promising food decontamination technology. Foods, 12(4), 814. https://doi.org/10.3390/foods12040814
   PubMed Web of Science ®Google Scholar
• Zhao, Y., Vlasselaer, L., Ribeiro, B., Terzoudis, K., Van den Ende, W., Hertog, M., Nicolaï, B., & De Coninck, B. (2022). Constitutive defense mechanisms have a major role in the resistance of woodland strawberry leaves against botrytis cinerea. Frontiers in plant science, 13, 912667. https://doi.org/10.3389/fpls.2022.912667
   PubMed Web of Science ®Google Scholar
• Zhou, D., Wang, Z., Peng, S., Chen, J., & Tu, K. (2019). Effects of cold plasma, UV-C or aqueous ozone treatment on Botrytis cinerea and their potential application in preserving blueberry. Journal of Applied Microbiology, 127(1), 175–185. https://doi.org/10.1111/jam.14280
   PubMed Web of Science ®Google Scholar