Vol. 64 No. 1 (2025)
Articles

Orange oil postharvest dips for control of grey mould (Botrytis cinerea) of plums and strawberries, and green mould (Penicillium digitatum) of citrus

PDF
  • Ncumisa NJOMBOLWANA-SWARTZ,
  • Julia MEITZ-HOPKINS,
  • Sara MONTEIRO,
  • Cheryl LENNOX
Ncumisa NJOMBOLWANA-SWARTZ
Department of Plant Pathology, Stellenbosch University, Stellenbosch, South Africa
Bio
Julia MEITZ-HOPKINS
Department of Plant Pathology, Stellenbosch University, Stellenbosch, South Africa
Bio
Sara MONTEIRO
ORO AGRI EUROPE S.A.Estrada Municipal 533, Zona de Biscaia, Estr. Do Lau, 2950-401, Palmela, Portugal
Cheryl LENNOX
Department of Plant Pathology, Stellenbosch University, Stellenbosch, South Africa
DOI: https://doi.org/10.36253/phyto-15613
Categories

Published 2025-05-14

Keywords

  • Fungicide sensitivity,
  • natural antimicrobial products,
  • plant extracts,
  • soft chemicals

How to Cite

[1]
N. NJOMBOLWANA-SWARTZ, J. MEITZ-HOPKINS, S. MONTEIRO, and C. LENNOX, “Orange oil postharvest dips for control of grey mould (Botrytis cinerea) of plums and strawberries, and green mould (Penicillium digitatum) of citrus”, Phytopathol. Mediterr., vol. 64, no. 1, pp. 57–70, May 2025.

Copyright (c) 2025 Ncumisa NJOMBOLWANA-SWARTZ, Julia MEITZ-HOPKINS, Sara MONTEIRO, Cheryl LENNOX

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Crossref
Scopus
Google Scholar
Europe PMC

Abstract

Orange oil has antibacterial properties for uses in food and pharmaceutical industries. This study evaluated the efficacy of orange oil dip applications and treatment periods for protective and curative effects against Botrytis cinerea, (which causes grey mould on plums and strawberries), and Penicillium digitatum, responsible for green mould of citrus. Pure orange oil and two orange oil-based formulations (OR007B and OR79) were tested on inoculated fruit, at oil concentrations from 0.05% to 1.00%, and were compared to the fungicides fludioxonil at 300 mg. L-1 for B. cinerea, or imazalil at 500 µg mL-1 for P. digitatum, the respective South African registered doses for these fungicides. Orange oil treatments failed to control green mould on lemons and oranges, with disease incidence exceeding 90% even after 120 sec of exposure. Two plum cultivars had different susceptibilities to grey mould, and orange oil reduced the disease incidence (24 to 14%) as the oil concentration increased in the curative treatments of cv. African Delight, outperforming 1% fludioxonil (24%). The OR007B and OR79 formulations both gave low incidence of grey mould, with 0.5% of orange oil in these formulations resulting in up to 12% incidence (from OR007B) and 17% (from OR79). Cv. Laetitia, in contrast, had >60% incidence of grey mould across all treatments, including fludioxonil. Protective treatments showed similar trends in both cultivars. On strawberries stored at 4°C for 14 d, grey mould incidence was reduced from 82% (control treatment) to 55% (for orange oil), 21% (for OR007B), and 44% (for OR79), with the orange oil treatments having efficacy comparable to fludioxonil. These results demonstrate the potential of orange oil treatments as alternatives for grey mould management in plums and strawberries.

PDF

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

  1. Andrade M.A., Barbosa C.H., Shah M.A., Ahmad N., Vilarinho F., … Ramos F., 2022. Citrus by-products: valuable source of bioactive compounds for food applications. Antioxidants 12: 38. DOI: https://doi.org/10.3390/antiox12010038
  2. Botrel D.A., Fernandes R.V. de B., Borges S.V., 2015. Microencapsulation of Essential Oils Using Spray Drying Technology Chapter 12, In: Microencapsulation and Microspheres for Food Applications, pp. 235–251, Elsevier Academic Press, Amsterdam, The Netherlands, from https://doi.org/10.1016/B978-0-12-800350-3.00013-3 DOI: https://doi.org/10.1016/B978-0-12-800350-3.00013-3
  3. Caccioni D.R.L., Guizzardi M., Biondi, D.M., Renda A., Ruberto G., 1998. Relationship between volatile components of Citrus fruit essential oils and antimicrobial action on Penicillium digitatum and Penicillium italicum. International Journal of Food Microbiology 43: 1–2. DOI: https://doi.org/10.1016/S0168-1605(98)00099-3
  4. Cherono K. & Workneh T.S., 2018. A review of the role of transportation on the quality changes of fresh tomatoes and their management in South Africa and other emerging markets. International Food Research 25: 2211–2228.
  5. Commission delegated regulation (EU) 2023/1656, 2023. amending Regulation (EU) No. 649/2012 of the European Parliament and of the Council as regards the listing of pesticides and industrial chemicals. Official Journal of the European Union 32023R1656.
  6. Costa J.H., Bazioli J.M., de Moraes Pontes J.G., Fill T.P., 2019. Penicillium digitatum infection mechanisms in Citrus: What do we know so far? Fungal Biology 123: 584–593. DOI: https://doi.org/10.1016/j.funbio.2019.05.004
  7. Department of Agriculture and Forestry (DAFF), 2010. Pesticide Management Policy (Act 36 of 1947). Pages 37–58.
  8. DALRRD (Department of Agriculture Land Reform and Rural Development), 2021. Plums and prunes maximum residue limits (MRL) list. Food Safety and Quality Assurance. Available at https://dalrrd.gov.za/foodSafety
  9. DALRRD (Department of Agriculture, Land Reform and Rural Development), 2023. Regulations relating to agricultural remedies. Government Gazette No. 3812.
  10. Droby S., Eick A., Macarisin D., Cohen L., Rafael G. … Shapira R., 2008. Role of Citrus volatiles in host recognition, germination, and growth of Penicillium digitatum and Penicillium italicum. Postharvest Biology and Technology 49: 386–396. DOI: https://doi.org/10.1016/j.postharvbio.2008.01.016
  11. Du Plooy W., Regnier T., Combrinck S., 2009. Essential oil amended coatings as alternatives to synthetic fungicides in Citrus postharvest management. Postharvest Biology and Technology 53: 117–122. DOI: https://doi.org/10.1016/j.postharvbio.2009.04.005
  12. Erasmus A., Lennox C.L., Jordaan H., Smilanick J.L., Lesar K., Fourie P.H., 2011. Imazalil residue loading and green mould control in Citrus packhouses. Postharvest Biology and Technology 62: 193–203. DOI: https://doi.org/10.1016/j.postharvbio.2011.05.006
  13. European Chemicals Agency, 2024. Classification, labelling and packaging. An agency of the European Union. Substance information: Imazalil sulphate. Available at https://echa.europa.eu/substance-information/-/substanceinfo/100.055.755
  14. Fan F., Hamada M.S., Li N., Li G.Q., Luo C.X., 2017. Multiple fungicide resistance in Botrytis cinerea from greenhouse strawberries in Hubei Province, China. Plant Disease 101: 601–606. DOI: https://doi.org/10.1094/PDIS-09-16-1227-RE
  15. Federal Register, 2014. Sweet orange peel tincture, exemption from the requirement of a tolerance. Environmental Protection Agency 40 CFR Part 80. Available at https://www.federalregister.gov/documents/2014/08/15/2014-19450/sweet-orange-peel-tincture-exemption-from-the-requirement-of-a-tolerance
  16. Feliziani E., Romanazzi G., 2013. Preharvest application of synthetic fungicides and alternative treatments to control postharvest decay of fruit. Steward Postharvest Review 3: 1–6. DOI: https://doi.org/10.2212/spr.2013.3.4
  17. Food and Drug Administration, 2006. How U.S. FDA’s GRAS notification program works US Food and Drug Administration. Available at https://www.fda.gov/food/generally-recognized-safe-gras (02 September 2018).
  18. Förster H., Driever G.F., Thompson D.C., Adaskaveg J.E., 2007. Postharvest decay management for stone fruit crops in California using the “reduced risk” fungicides fludioxonil and fenhexamid. Plant Disease 91: 209–215. DOI: https://doi.org/10.1094/PDIS-91-2-0209
  19. Fourie J.F., Holz G., 1985. Postharvest fungal decay of stone fruit in the South-Western Cape. Phytophylactica 17: 175–177.
  20. Gradziel T.M., Bostock R.M., Adaskaveg J.E., 2003. Resistance to brown rot disease in peach is determined by multiple structural and biochemical components. Acta Horticulturae 622: 347–352. DOI: https://doi.org/10.17660/ActaHortic.2003.622.34
  21. Guo Q., Liu K., Deng W., Zhong B., Yang W., Chun J., 2018. Chemical composition and antimicrobial activity of Gannan navel orange (Citrus sinensis Osbeck cv. Newhall) peel essential oils. Food Science and Nutrition 6: 1431–1437. DOI: https://doi.org/10.1002/fsn3.688
  22. Haffner K. 2002. Postharvest quality and processing of strawberries. Acta Horticulturae 567: 715–722. DOI: https://doi.org/10.17660/ActaHortic.2002.567.157
  23. Hamdan M., Jaradat N., Al‑Maharik N., Ismail S., Qadi M., 2024.Chemical composition, cytotoxic effects and antimicrobial activity of combined essential oils from Citrus meyeri, Citrus paradise, and Citrus sinensis leaves. Industrial Crops and Products 210: 118096. https://doi.org/10.1016/j.indcrop.2024.118096 DOI: https://doi.org/10.1016/j.indcrop.2024.118096
  24. Hanafy S.M., El-Shafea Y.M.A., Saleh W.D., Fathy H.M. 2021. Chemical profiling, in vitro antimicrobial and antioxidant activities of pomegranate, orange and banana peel-extracts against pathogenic microorganisms. Journal of Genetic Engineering and Biotechnology 19: 80. https://doi.org/10.1186/s43141-021-00151-0 DOI: https://doi.org/10.1186/s43141-021-00151-0
  25. Hezakiel H.E., Thampi M., Rebello S. & Sheikhmoideen J.M. 2023. Biopesticides: a green approach towards agricultural pests. Applied biochemistry and biotechnology. Pharmaceutics 196: 5533–5562. DOI: https://doi.org/10.1007/s12010-023-04765-7
  26. Jantrawut P., Boonsermsukcharoen K., Thipnan K., Chaiwarit T., Hwang K.M., Park E.S. 2018. Enhancement of antibacterial activity of orange oil in pectin thin film by microemulsion. Nanomaterial 8: 1–12. DOI: https://doi.org/10.3390/nano8070545
  27. Jenneker N., Silue Y., Meitz-Hopkins J.C., Lennox C.L., Opara U.L., Fawole O.A. 2024. Gum Arabic-incorporated thymol/salicylic acid composite coatings control grey mould and brown rot in ‘Angeleno’ plums. European Journal of Plant Pathology 170: 943–954. https://doi.org/1007/s10658-024-02888-z DOI: https://doi.org/10.1007/s10658-024-02888-z
  28. John I., Muthukumar K., Arunagiri A., 2017. A review on the potential of Citrus waste for D-Limonene, pectin, and bioethanol production. International Journal of Green Energy 14: 599–612. DOI: https://doi.org/10.1080/15435075.2017.1307753
  29. López-Reyes J.G., Spadaro D., Gullino M.L., Garibaldi A., 2010. Efficacy of plant essential oils on postharvest control of rot caused by fungi on four cultivars of apples in vivo. Flavour and Fragrance Journal 25: 171-177. DOI: https://doi.org/10.1002/ffj.1989
  30. López-Reyes J.G., Spadaro D., Prelle A., Garibaldi A., Gullino M.L., 2013. Efficacy of plant essential oils on postharvest control of rots caused by fungi on different stone fruits in vivo. Journal of Food Protection 76: 631–639. DOI: https://doi.org/10.4315/0362-028X.JFP-12-342
  31. Lucintel, 2024. Pesticide Market: Trends, Opportunities and Competitive Analysis. 8951 Cypress Waters Blvd, Suite 160 Dallas, TX 75019, USA.
  32. Macarisin D., Cohen L., Eick A., Rafael G., Belausov E., … Droby, S.. 2007. Penicillium digitatum suppresses production of hydrogen peroxide in host tissue during infection of Citrus fruit. Phytopathology 97: 1491–1500. DOI: https://doi.org/10.1094/PHYTO-97-11-1491
  33. Maes C., Bouquillon S., Fauconnier M.L., 2019. Encapsulation of essential oils for the development of biosourced pesticides with controlled release: A review. Molecules 24: 1–15. DOI: https://doi.org/10.3390/molecules24142539
  34. Mudzunga M.J., 2022. Phase-out of active ingredients and formulations that meet the criteria of carcinogenicity, mutagenicity, and reproductive toxicity categories 1A or 1B of the globally harmonized system of classification and labelling of chemicals. Agriculture, Land Reform and Rural Development of South Africa.
  35. Nelson R.M., 2010. Quality challenges facing the South African avocado industry – An overview of the 2009 South African avocado season. SAAGA 33: 7–13.
  36. Njombolwana N.S., Erasmus A., van Zyl J.G., du Plooy W., Cronje P.J.R., Fourie P.H., 2013. Effects of Citrus wax coating and brush type on imazalil residue loading, green mould control and fruit quality retention of sweet oranges. Postharvest Biology and Technology 86: 362–371. DOI: https://doi.org/10.1016/j.postharvbio.2013.07.017
  37. Njombolwana N., Meitz-Hopkins J.C., Monteiro S., Lennox C. 2022. Postharvest decay control of plums using orange oil. Proceedings V IS on Pomegranate and Minor Mediterranean Fruits. Acta Horticulturae 1349: 189–194. DOI: https://doi.org/10.17660/ActaHortic.2022.1349.26
  38. Ouyang Q., Liu Y., Chen Y., Tao N., 2022. Antifungal action of α-terpineol on imazalil-resistant Penicillium digitatum Pdw03. Food Science 43: 8–13.
  39. Palou L., Ali A., Fallik E., Romanazzi G., 2016. GRAS, plant- and animal-derived compounds as alternatives to conventional fungicides for the control of postharvest diseases of fresh horticultural produce. Postharvest Biology and Technology 122: 41–52. DOI: https://doi.org/10.1016/j.postharvbio.2016.04.017
  40. Parvez S. & Wani I.A., 2018. Postharvest Biology and Technology of Strawberry. In: Postharvest Biology and Technology of Temperate Fruits (Mir, S.A., Shah, M.A. and Mir, M.M., ed) Springer, Cham., Switzerland. pp. 331-348, from https://www.springerprofessional.de/en/postharvest-biology-and-technology-of-temperate-fruits/15801108 DOI: https://doi.org/10.1007/978-3-319-76843-4_14
  41. Pejin B., Vujisic L., Sabovljevic M., Tesevic V., Vajs V., 2011. Preliminary data on essential oil composition of the moss Rhodobryum ontariense (Kindb.) Cryptogamie. Bryologie 32: 113–117. DOI: https://doi.org/10.7872/cryb.v32.iss1.2011.113
  42. Plaza P., Torre, R. Usall, J. Lamarca N., Ninas I., 2004. Evaluation of the potential of commercial post-harvest application of essential oils to control Citrus decay. Journal of Horticultural Science and Biotechnology 79: 935–940. DOI: https://doi.org/10.1080/14620316.2004.11511869
  43. Pothakamury U.R., Barbosa-Cánovas G. V., 1995. Fundamental aspects of controlled release in foods. Trends In Food Science and Technology 6: 397–406. DOI: https://doi.org/10.1016/S0924-2244(00)89218-3
  44. Radi M., Akhavan-Darabi S., Akhavan H.R., Amiri S., 2018. The use of orange peel essential oil microemulsion and nanoemulsion in pectin-based coating to extend the shelf life of fresh-cut orange. Journal of Food Processing and Preservation 42(2): e13441. https://doi.org/10.1111/jfpp.13441 DOI: https://doi.org/10.1111/jfpp.13441
  45. Rahman M.M., Wills, R.B., Bowyer M.C., Golding J.B., Kirkman T., Pristijono P., 2020. Efficacy of orange essential oil and citral after exposure to UV-C irradiation to inhibit Penicillium digitatum in navel oranges. Horticulturae 6(4): 102. https://doi.org/10.3390/horticulturae6040102 DOI: https://doi.org/10.3390/horticulturae6040102
  46. Ramírez-Gómez X.S., Jiménez-García S.N., Campos V.B., Lourdes M. Campos G., 2020. Plant Metabolites in Plant Defence Against Pathogens. In: Plant Disease-Current Threats and Management Trends. (S. Topolovec-Pintaric, ed.) pp. 1-20. InTechOpen Ltd., London, UK, from: https://doi.org/10.5772/intechopen.87958 DOI: https://doi.org/10.5772/intechopen.87958
  47. Rammanee K., Hongpattarakere T., 2011. Effects of tropical Citrus essential oils on growth, aflatoxin production, and ultrastructure alterations of Aspergillus flavus and Aspergillus parasiticus. Food and Bioprocess Technology 4: 1050–1059. DOI: https://doi.org/10.1007/s11947-010-0507-1
  48. Regnier T., Combrinck S., Veldman W., du Plooy W., 2014. Application of essential oils as multi-target fungicides for the control of Geotrichum citri-aurantii and other postharvest pathogens of Citrus. Industrial Crops and Products 61: 151–159. DOI: https://doi.org/10.1016/j.indcrop.2014.05.052
  49. Rodríguez A., Shimada T., Cervera M., Redondo A., Alquézar B., Rodrigo M.J., …. López M.M., Peña L., 2015. Resistance to pathogens in terpene down-regulated orange fruits inversely correlates with the accumulation of D-limonene in peel oil glands. Plant Signalling and Behaviour
  50. : e1028704. https://doi.org/10.1080/15592324.2015.1028704. DOI: https://doi.org/10.1080/15592324.2015.1028704
  51. Sharifi-Rad J., Sureda A., Tenore G.C., Daglia M., Sharifi-Rad M., Valussi M.,… Iriti M., 2017. Biological activities of essential oils: from plant chemoecology to traditional healing systems. Molecules 22: 70. https://doi.org/10.3390/molecules22010070 DOI: https://doi.org/10.3390/molecules22010070
  52. Sharma N., Tripathi A., 2006. Fungitoxicity of the essential oil of Citrus sinensis on postharvest pathogens. World Journal of Microbiology and Biotechnology 22: 587–593. DOI: https://doi.org/10.1007/s11274-005-9075-3
  53. Shi Y., Huang S., He Y., Wu J., Yang Y., 2018. Navel orange peel essential oil to control food spoilage molds in potato slices. Journal of Food Protection 81(9): 1496–1502. DOI: https://doi.org/10.4315/0362-028X.JFP-18-006
  54. Sişman T., Türkez H., 2010. Toxicologic evaluation of imazalil with particular reference to genotoxic and teratogenic potentials. Toxicology and Industrial Health 26: 641–648. DOI: https://doi.org/10.1177/0748233710375951
  55. Smilanick J.L., Michael I.F., Mansour M.F., Mackey B.E., Margosan D.A., … Weist C.F., 1997. Improved control of green mould of Citrus with imazalil in warm water compared with its use in wax. Plant Disease 81: 1299–1304. DOI: https://doi.org/10.1094/PDIS.1997.81.11.1299
  56. Smilanick J.L., Mansour M.F., Margosan D.A., Gabler F.M., Goodwine W.R., 2005. Influence of pH and NaHCO3 on effectiveness of imazalil to Inhibit germination of Penicillium digitatum and to control postharvest green mould on Citrus fruit. Plant Disease 89: 640–648. DOI: https://doi.org/10.1094/PD-89-0640
  57. Stander C., Van Dyk F.E., 2017. Maintaining cold chain integrity: Temperature breaks within fruit reefer containers in the Cape Town Container Terminal. Southern African Business Review 21:362–384.
  58. Talibi I., Boubaker H., Boudyach E.H., Aoumar A.A. Ben, 2014. Alternative methods for the control of postharvest Citrus diseases. Applied Microbiology 117: 1–17. DOI: https://doi.org/10.1111/jam.12495
  59. Tao H., Bao Z., Jin C., Miao W., Fu Z., Jin Y., 2020. Toxic effects and mechanisms of three commonly used fungicides on the human colon adenocarcinoma cell line Caco-2. Environmental Pollution 263: 114660. DOI: https://doi.org/10.1016/j.envpol.2020.114660
  60. Tao N.G., Liu Y.J., Zhang M.L., 2009. Chemical composition and antimicrobial activities of essential oil from the peel of bingtang sweet orange (Citrus sinensis Osbeck). International Journal of Food Science and Technology 44: 1281–1285. DOI: https://doi.org/10.1111/j.1365-2621.2009.01947.x
  61. Tripathi P., Dubey N.K., 2004. Exploitation of natural products as an alternative strategy to control postharvest fungal rotting of fruit and vegetables. Postharvest Biology and Technology 32: 235–245. DOI: https://doi.org/10.1016/j.postharvbio.2003.11.005
  62. Tsao R., Zhou T., 2000. Antifungal activity of monoterpenoids against postharvest pathogens Botrytis cinerea and Monilinia fructicola. Journal of Essential Oil Research 12: 113–121. DOI: https://doi.org/10.1080/10412905.2000.9712057
  63. Vitoratos A., Bilalis D., Karkanis A., Efthimiadou A., 2013. Antifungal Activity of Plant Essential Oils Against Botrytis cinerea, Penicillium italicum and Penicillium digitatum. Notulae Botanicae 41: 86–92. DOI: https://doi.org/10.15835/nbha4118931
  64. Viuda-Martos M., Ruiz-Navajas Y., Fernández-López J., Pérez-Álvarez J., 2008. Antifungal activity of lemon (Citrus lemon L.), mandarin (Citrus reticulata L.), grapefruit (Citrus paradisi L.) and orange (Citrus sinensis L.) essential oils. Food Control 19: 1130–1138. DOI: https://doi.org/10.1016/j.foodcont.2007.12.003
  65. Wuryatmo E., Able A.J., Ford C.M., Scott E.S., 2014. Effect of volatile citral on the development of blue mould, green mould, and sour rot on navel orange. Australasian Plant Pathology 43: 403-411. DOI: https://doi.org/10.1007/s13313-014-0281-z
  66. Yuan X., Meng, K. Shi S., Wu Y., Chen X., … Tao N., 2023. Trans-2-hexenal inhibits the growth of imazalil-resistant Penicillium digitatum Pdw03 and delays green mould in postharvest Citrus. Postharvest Biology and Technology 199: 112304. https://doi.org/10.1016/j.postharvbio.2023.112304 DOI: https://doi.org/10.1016/j.postharvbio.2023.112304
  67. Zareiyan F., Khajehsharifi H., 2021. Analyzing bioactive compounds in essential oil of Citrus maxima and Citrus sinensis peel. Journal of Essential Oil Bearing Plants 24(4): 677–682. DOI: https://doi.org/10.1080/0972060X.2021.1958702
  68. Ziedan E. S. H., Saad M. M., El-Kafrawy A. A., Sahab A. F., Mossa A. T. H., 2022. Evaluation of essential oils nanoemulsions formulations on Botrytis cinerea growth, pathology, and grey mould incidence on cucumber fruits. Bulletin of the National Research Centre 46(1): 88. DOI: https://doi.org/10.1186/s42269-022-00765-5