Abstract
This research investigated the inhibitory effects of essential oils (EOs) extracted from four Citrus sinensis cultivars (Thomson navel, Jaffa sweet, Sanguine blood, and Valencia) against Alternaria spp., a pathogen affecting oranges. Among the cultivars studied, the EO from the Sanguine blood cultivar exhibited the highest antifungal activity when added into the culture medium and it was selected for further investigations. Sanguine blood EO reduced melanin in the fungal hyphae and completely inhibited vegetative growth of Alternaria species at 550–750 μg mL−1 concentrations and inhibited spore germination at 800–1000 μg mL−1 concentrations, which were similar to the fungicide Mancozeb. Separation of cytoplasm from cell wall, hyphal emptying, destruction of cell wall, plasma membrane, organelles such as nucleus and mitochondria, hyphal lysis and cell death were observed in all three fungal species tested. Activities of cell wall degrading enzymes produced by the pathogens were significantly reduced in the fungi treated with the EO. Reduction of the disease index was observed in all four cultivars, similar to the effect of fungicide. Gas chromatography-mass spectrometry analysis revealed presence of D-limonene, β-myrcene, and β-linalool as the main components of the EO obtained from the Sanguine blood cultivar. In conclusion, the EOs as natural plant protectants could control Alternaria spp. on orange under both in vitro and in vivo conditions.
Similar content being viewed by others
Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
References
Abdel-Razik A (1970) The parasitism of white Sclerotium cepivorum Berk., the incitant of white rot of onion. Ph. D. thesis, Faculty of Agriculture, Assiut University, Assiut, Egypt
Abo-Elyousr KA, Al-Qurashi AD, Almasoudi NM (2021) Evaluation of the synergy between Schwanniomyces vanrijiae and propolis in the control of Penicillium digitatum on lemons. Egypt J Biol Pest Control 31(1):1–10. https://doi.org/10.1186/s41938-021-00415-4
Aguilar-Veloz LM, Calderón-Santoyo M, Vazquez Gonzalez Y, Ragazzo-Sánchez JA (2020) Application of essential oils and polyphenols as natural antimicrobial agents in postharvest treatments: advances and challenges. Food Sci Nutr 8(6):2555–2568. https://doi.org/10.1002/fsn3.1437
Akhtari A, Davari M, Habibi-Yangjeh A, Ebadollahi A, Feizpour S (2022) Antifungal activities of pure and ZnO-encapsulated essential oil of Zataria multiflora on Alternaria solani as the pathogenic agent of tomato early blight disease. Front Plant Sci 13:932475. https://doi.org/10.3389/fpls.2022.932475
Ali M, Haroon U, Khizar M, Chaudhary HJ, Munis MFH (2020) Facile single step preparations of phyto-nanoparticles of iron in Calotropis procera leaf extract to evaluate their antifungal potential against Alternaria alternata. Curr Plant Biol 23:100157. https://doi.org/10.1016/j.cpb.2020.100157
Almasaudi NM, Al-Qurashi AD, Elsayed MI, Abo-Elyousr KA (2022) Essential oils of oregano and cinnamon as an alternative method for control of gray mold disease of table grapes caused by Botrytis cinerea. J Plant Pathol 104(1):317–328. https://doi.org/10.1007/s42161-021-01008-8
Alves E, Lucas GC, Pozza EA, de Carvalho Alves M (2013) Scanning Electron Microscopy for Fungal Sample Examination. In: Gupta V, Tuohy M, Ayyachamy M, Turner K, O’Donovan A (eds) Laboratory Protocols in Fungal Biology. Fungal Biology. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-2356-0_8
Amini L, Soudi MR, Saboora A, Mobasheri H (2018) Effect of essential oil from Zataria multiflora on local strains of Xanthomonas campestris: an efficient antimicrobial agent for decontamination of seeds of Brassica oleracea var. capitata. Sci Hortic 236:256–264. https://doi.org/10.1016/j.scienta.2018.03.046
Ammad F, Moumen O, Gasem A, Othmane S, Hisashi K-N, Zebib B, Merah O (2018) The potency of lemon (Citrus limon L.) essential oil to control some fungal diseases of grapevine wood. C R Biol 341(2):97–101. https://doi.org/10.1016/j.crvi.2018.01.003
Arlotta C, Ciacciulli A, Strano MC, Cafaro V, Salonia F, Caruso P, Licciardello C, Russo G, Smith MW, Cuenca J (2020) Disease resistant citrus breeding using newly developed high resolution melting and CAPS protocols for Alternaria brown spot marker assisted selection. Agronomy 10(9):1368. https://doi.org/10.3390/agronomy10091368
Bassimba D, Mira JL, Vicent A (2014) Inoculum sources, infection periods, and effects of environmental factors on Alternaria brown spot of mandarin in Mediterranean climate conditions. Plant Dis 98(3):409–417. https://doi.org/10.1094/PDIS-09-13-0956-RE
Bnina EB, Hajlaoui H, Chaieb I, Said MB, Jannet HB, Daami-Remadi M (2019) Chemical composition, antimicrobial and insecticidal activities of the tunisian Citrus aurantium essential oils. Czech J Food Sci 37(2):81–92. https://doi.org/10.17221/202/2017-CJFS
Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods—a review. Int J Food Microbiol 94(3):223–253. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
Celia C, Trapasso E, Locatelli M, Navarra M, Ventura CA, Wolfram J, Carafa M, Morittu VM, Britti D, Di Marzio L (2013) Anticancer activity of liposomal bergamot essential oil (BEO) on human neuroblastoma cells. Colloids Surf B 112:548–553. https://doi.org/10.1016/j.colsurfb.2013.09.017
Chang H-T, Cheng Y-H, C-l W, Chang S-T, Chang -T-T, Y-c S (2008) Antifungal activity of essential oil and its constituents from Calocedrus macrolepis var. formosana Florin leaf against plant pathogenic fungi. Bioresour Technol 99(14):6266–6270. https://doi.org/10.1016/j.biortech.2007.12.005
Chavan M, Wakte P, Shinde D (2010) Analgesic and anti-inflammatory activity of Caryophyllene oxide from Annona squamosa L. bark. Phytomedicine 17(2):149–151. https://doi.org/10.1016/j.phymed.2009.05.016
Chen C, Cai N, Chen J, Wan C (2019) Clove essential oil as an alternative approach to control postharvest blue mold caused by Penicillium italicum in citrus fruit. Biomolecules 9(5):197. https://doi.org/10.3390/biom9050197
Cordero RJ, Casadevall A (2017) Functions of fungal melanin beyond virulence. Fungal Biol Rev 31(2):99–112. https://doi.org/10.1016/j.fbr.2016.12.003
da Cruz Almeida ET, de Souza GT, de Sousa Guedes JP, Barbosa IM, de Sousa CP, Castellano LRC, Magnani M, de Souza EL (2019) Mentha piperita L. essential oil inactivates spoilage yeasts in fruit juices through the perturbation of different physiological functions in yeast cells. Food Microbiol 82:20–29. https://doi.org/10.1016/j.fm.2019.01.023
da Cruz Cabral L, Pinto VF, Patriarca A (2013) Application of plant derived compounds to control fungal spoilage and mycotoxin production in foods. Int J Food Microbiol 166(1):1–14. https://doi.org/10.1016/j.ijfoodmicro.2013.05.026
Da Silva JK, Da Trindade R, Moreira EC, Maia JGS, Dosoky NS, Miller RS, Cseke LJ, Setzer WN (2017) Chemical diversity, biological activity, and genetic aspects of three Ocotea species from the Amazon. Int J Mol Sci 18(5):1081. https://doi.org/10.3390/ijms18051081
Dang HX, Pryor B, Peever T, Lawrence CB (2015) The Alternaria genomes database: a comprehensive resource for a fungal genus comprised of saprophytes, plant pathogens, and allergenic species. BMC Genomics 16(1):1–9. https://doi.org/10.1186/s12864-015-1430-7
de Azevedo FA, Devite FT, Bastianel M, Schinor EH, Da Conceição PM, 2023. Citrus essential oils as an alternative method of control of the fungus Alternaria alternata (Fr.: fr.) Keissler. https://doi.org/10.20944/preprints202304.0940.v1
De-Miguel MD, Caballero P, Fernández-Zamudio MA (2019) Varietal change dominates adoption of technology in Spanish citrus production. Agronomy 9(10):631. https://doi.org/10.3390/agronomy9100631
Devite FT, Azevedo F, Bastianel M, Schinor EH, Conceição P (2023) Mandarin essential oils as an alternative method of controlling the fungus Alternaria alternata (Fr.: fr.) Keissler. Hortic 9(6):613. https://doi.org/10.3390/horticulturae9060613
Ding S, Ge W, Buswell JA (2001) Endoglucanase I from the edible straw mushroom, Volvariella volvacea. Purification, characterization, cloning and expression. Eur J Biochem 268(22):5687–5695. https://doi.org/10.1046/j.0014-2956.2001.02503.x
Dwivedy AK, Kumar M, Upadhyay N, Prakash B, Dubey NK (2016) Plant essential oils against food borne fungi and mycotoxins. Curr Opin Food Sci 11:16–21. https://doi.org/10.1016/j.cofs.2016.08.010
El Asbahani A, Miladi K, Badri W, Sala M, Addi EA, Casabianca H, El Mousadik A, Hartmann D, Jilale A, Renaud F (2015) Essential oils: from extraction to encapsulation. Int J Pharm 483(1-2):220–243. https://doi.org/10.1016/j.ijpharm.2014.12.069
Elena K (2006) Alternaria brown spot of Minneola in Greece; evaluation of citrus species susceptibility. EurJ Plant Pathol 115:259–262. https://doi.org/10.1007/s10658-006-9005-8
Elsayed MI, Al-Qurashi AD, Almasaudi NM, Abo-Elyousr KA (2022) Efficacy of essential oils against gray mold and effect on fruit quality during cold storage in table grapes. S Afr J Bot 146:481–490. https://doi.org/10.1016/j.sajb.2021.11.046
Fan Y, Zhang R, Liu X, Ma Y, Wang Y, Liu F, He W, Wu A, Wang C (2022) Transcriptomics analysis and candidate genes associated with Xinjiang jujube fruits in response to Alternaria alternata infection. Physiol Mol Plant Pathol 122:101915. https://doi.org/10.1016/j.pmpp.2022.101915
Fancello F, Petretto GL, Marceddu S, Venditti T, Pintore G, Zara G, Mannazzu I, Budroni M, Zara S (2020) Antimicrobial activity of gaseous Citrus limon var pompia leaf essential oil against Listeria monocytogenes on ricotta salata cheese. Food Microbiol 87:103386. https://doi.org/10.1016/j.fm.2019.103386
Felipini RB, Brito RAS, Azevedo FA, Massola Júnior NS (2023) Alternaria alternata f. sp. citri tangerine pathotype induces reactive oxygen species accumulation in susceptible citrus leaves. Physiol Mol Plant Pathol 126:102040. https://doi.org/10.1016/j.pmpp.2023.102040
Feng W, Zheng X (2006) Control of Alternaria alternata by cassia oil in combination with potassium chloride or sodium chloride. J Appl Microbiol 101(6):1317–1322. https://doi.org/10.1111/j.1365-2672.2006.03024.x
Fisher K, Phillips C (2008) Potential antimicrobial uses of essential oils in food: is citrus the answer? Trends Food Sci Technol 19(3):156–164. https://doi.org/10.1016/j.tifs.2007.11.006
Garganese F, Ippolito A, Di Rienzo V, Lotti C, Montemurro C, Sanzani SM (2018) A new high resolution melting assay for genotyping Alternaria species causing citrus brown spot. J Sci Food Agric 98(12):4578–4583. https://doi.org/10.1002/jsfa.8986
Garganese F, Sanzani SM, Di Rella D, Schena L, Ippolito A (2019) Pre-and postharvest application of alternative means to control Alternaria Brown spot of citrus. Crop Prot 121:73–79. https://doi.org/10.1016/j.cropro.2019.03.014
Garganese F, Schena L, Siciliano I, Prigigallo MI, Spadaro D, De Grassi A, Ippolito A, Sanzani SM (2016) Characterization of citrus-associated Alternaria species in Mediterranean areas. PloS One 11(9):e0163255. https://doi.org/10.1371/journal.pone.0163255
Ghanei Ghooshkhaneh N, Golzarian MR, Mamarabadi M (2022) Withdrawn: spectral pattern study of citrus black rot caused by Alternaria alternata and selecting optimal wavelengths for decay detection. Food Sci Nutr 10. https://doi.org/10.1002/fsn3.2739
Golmohammadi M, Rahimian H, 2004. First report of brown spot caused by Alternaria alternata on tangrine in Iran. In Proceedings of 16th Iranian plant protection congress (Vol. 28, p. 461). https://doi.org/10.22059/ijpps.2017.233507.1006787
González-Lamothe R, Mitchell G, Gattuso M, Diarra MS, Malouin F, Bouarab K (2009) Plant antimicrobial agents and their effects on plant and human pathogens. Int J Mol Sci 10(8):3400–3419. https://doi.org/10.3390/ijms10083400
Grati Affes T, Chenenaoui S, Zemni H, Hammami M, Bachkouel S, Aidi Wannes W, Nasraoui B, Saidani Tounsi M, Lasram S (2023) Biological control of Citrus brown spot pathogen,“Alternaria alternata” by different essential oils. Int J Environ Health Res 33(8):823–836. https://doi.org/10.1080/09603123.2022.2055748
Grewling Ł, Magyar D, Chłopek K, Grinn-Gofroń A, Gwiazdowska J, Siddiquee A, Ianovici N, Kasprzyk I, Wójcik M, Lafférsová J (2022) Bioaerosols on the atmospheric super highway: an example of long distance transport of Alternaria spores from the Pannonian Plain to Poland. Sci Total Environ 819:153148. https://doi.org/10.1016/j.scitotenv.2022.153148
Güney IG, Tekin F, Günen TU, Özer G, Derviş S (2023) Alternaria alternata causing inner black rot of lemon (Citrus limon) fruits in Turkey: genetic diversity and characterization. Physiol Mol Plant Pathol 125:101998. https://doi.org/10.1016/j.pmpp.2023.101998
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 Sci Nutr 6(6):1431–1437. https://doi.org/10.1002/fsn3.688
Gwinn KD (2018) Bioactive natural products in plant disease control. Stud Nat Prod Chem 56:229–246. https://doi.org/10.1016/B978-0-444-64058-1.00007-8
Hajlaoui H, Arraouadi S, Aouadi K, Snoussi M, Noumi E, Kadri A (2021) GC-MS Profile, α-glucosidase Inhibition potential, antibacterial and antioxidant evaluation of peels Citrus aurantium (L) essential oil. J Pharm Res Int 33(60B):1580–1591
Han J, Fan Y, Sun T, An J, Ding Y, Zhang W, Liu F, Wang C (2023) Sodium nitroprusside (SNP) treatment increases the postharvest resistance of apple fruit to Alternaria alternata by enhancing antioxidant enzyme activity. Physiol Mol Plant Pathol 129:102199. https://doi.org/10.1016/j.pmpp.2023.102199
Hankin L, Zucker M, Sands D (1971) Improved solid medium for the detection and enumeration of pectolytic bacteria. Appl Microbiol 22(2):205–209. https://doi.org/10.1128/am.22.2.205-209.1971
Hu F, Tu X-F, Thakur K, Hu F, Li X-L, Zhang Y-S, Zhang J-G, Wei Z-J (2019) Comparison of antifungal activity of essential oils from different plants against three fungi. Food Chem Toxicol 134:110821. https://doi.org/10.1016/j.fct.2019.110821
Huang J, Liu S, Liu R, Yi Y, Li C, Xiao Z, Tu J, Xiao J (2023) Mechanisms of Litsea cubeba essential oil in the control of Colletotrichum scovillei in pepper (Capsicum annuum L.): cell membrane/wall perspective. Physiol Mol Plant Pathol 127:102103. https://doi.org/10.1016/j.pmpp.2023.102103
Hyldgaard M, Mygind T, Meyer RL (2012) Essential oils in food preservation: mode of action, synergies, and interactions with food matrix components. Food Chem Toxicol 3:12. https://doi.org/10.3389/fmicb.2012.00012
Jahani M, Pira M, Aminifard MH (2020) Antifungal effects of essential oils against Aspergillus niger in vitro and in vivo on pomegranate (Punica granatum) fruits. Sci Hortic 264:109188. https://doi.org/10.1016/j.scienta.2020.109188
Jing L, Lei Z, Li L, Xie R, Xi W, Guan Y, Sumner LW, Zhou Z (2014) Antifungal activity of citrus essential oils. J Agric Food Chem 62(14):3011–3033. https://doi.org/10.1021/jf5006148
Kagale S, Marimuthu T, Kagale J, Thayumanavan B, Samiyappan R (2011) Induction of systemic resistance in rice by leaf extracts of Zizyphus jujuba and Ipomoea carnea against Rhizoctonia solani. Plant Signaling Behav 6(7):919–923. https://doi.org/10.4161/psb.6.7.15304
Kenfaoui J, Lahlali R, Laasli S-E, Goura K, Fardi M, Tahiri A, El Ghadraoui L, Amiri S (2023) The potency and effectiveness of six essential oils in controlling grapevine trunk diseases in Morocco. J Nat Pestic Res 6:100053. https://doi.org/10.1016/j.napere.2023.100053
Kheder AA, Akagi Y, Akamatsu H, Yanaga K, Maekawa N, Otani H, Tsuge T, Kodama M (2012) Functional analysis of the melanin biosynthesis genes ALM1 and BRM2-1 in the tomato pathotype of Alternaria alternata. J Gen Plant Pathol 78:30–38. https://doi.org/10.1007/s10327-011-0356-4
Kikot GE, Moschini R, Consolo VF, Rojo R, Salerno G, Hours RA, Gasoni L, Arambarri AM, Alconada T (2011) Occurrence of different species of Fusarium from wheat in relation to disease levels predicted by a weather-based model in Argentina pampas region. Mycopathologia 171:139–149. https://doi.org/10.1007/s11046-010-9335-0
Kumar A, Kudachikar V (2018) Antifungal properties of essential oils against anthracnose disease: a critical appraisal. J Plant Dis Prot 125:133–144. https://doi.org/10.1007/s41348-017-0128-2
Lamine M, Rahali FZ, Hammami M, Mliki A (2019) Correlative metabolite profiling approach to understand antioxidant and antimicrobial activities from citrus essential oils. Int J Food Sci Technol 54(8):2615–2623. https://doi.org/10.1111/ijfs.14173
Lazar Baker E, Hetherington S, Ku V, Newman S (2011) Evaluation of commercial essential oil samples on the growth of postharvest pathogen Monilinia fructicola (G. Winter) Honey. Lett Appl Microbiol 52(3):227–232. https://doi.org/10.1111/j.1472-765X.2010.02996.x
Lee HB, Patriarca A, Magan N (2015) Alternaria in food: ecophysiology, mycotoxin production and toxicology. Mycobiology 43(2):93–106. https://doi.org/10.5941/MYCO.2015.43.2.93
Lima C, Rentschler LLA, Bueno JT, Boaventura AC (2016) Plant extracts and essential oils on the control of Alternaria alternata, Alternaria dauci and on the germination and emergence of carrot seeds (Daucus carota L.). Cienc Rural 46:764–770. https://doi.org/10.1590/0103-8478cr20141660
Liu C, Cheng Y, Zhang H, Deng X, Chen F, Xu J (2012) Volatile constituents of wild citrus Mangshanyegan (Citrus nobilis Lauriro) peel oil. J Agric Food Chem 60(10):2617–2628. https://doi.org/10.1021/jf2039197
Ma H, Zhang B, Gai Y, Sun X, Chung K-R, Li H (2019) Cell-wall-degrading enzymes required for virulence in the host selective toxin-producing necrotroph Alternaria alternata of citrus. Front Microbiol 10:2514. https://doi.org/10.3389/fmicb.2019.02514
Macmillan JD, Vaughn RH (1964) Purification and properties of a polygalacturonic acid-trans-eliminase produced by Clostridium multifermentans. Biochemistry 3(4):564–572. https://doi.org/10.1021/bi00892a016
Maghsoodi F, Taheri P (2021) Efficacy of Althaea officinalis leaf extract in controlling Alternaria spp. pathogenic on Citrus. EurJ Plant Pathol 161(4):799–813. https://doi.org/10.1007/s10658-021-02361-1
Magyar D, Vass M, Li D-W (2016) Dispersal strategies of microfungi. In: Biology of microfungi, pp 315–371. https://doi.org/10.1007/978-3-319-29137-6_14
Martelli IB, de Andrade Pacheco C, Bastianel M, Schinor EH, da Conceição PM, de Azevedo FA (2016) Diagrammatic scale for assessing foliar symptoms of alternaria brown spot in citrus. Agron Soc Biotechnol 2(2):57–57. https://doi.org/10.33158/ASB.2016v2i2p57
Mbili NC, Opara UL, Lennox CL, Vries FA (2017) Citrus and lemongrass essential oils inhibit Botrytis cinerea on ‘Golden Delicious’,‘Pink Lady’and ‘Granny Smith’apples. J Plant Dis Prot 124:499–511. https://doi.org/10.1007/s41348-017-0121-9
Meena M, Gupta SK, Swapnil P, Zehra A, Dubey MK, Upadhyay RS (2017) Alternaria toxins: potential virulence factors and genes related to pathogenesis. Front Microbiol 8:1451. https://doi.org/10.3389/fmicb.2017.01451
Meena M, Zehra A, Dubey MK, Aamir M, Gupta VK, Upadhyay RS (2016) Comparative evaluation of biochemical changes in tomato (Lycopersicon esculentum Mill.) infected by Alternaria alternata and its toxic metabolites (TeA, AOH, and AME). Front Plant Sci 7:1408. https://doi.org/10.3389/fpls.2016.01408
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(4):591. https://doi.org/10.3390/molecules22040591
Mitropoulou G, Fitsiou E, Spyridopoulou K, Tiptiri-Kourpeti A, Bardouki H, Vamvakias M, Panas P, Chlichlia K, Pappa A, Kourkoutas Y (2017) Citrus medica essential oil exhibits significant antimicrobial and antiproliferative activity. LWT 84:344–352. https://doi.org/10.1016/j.lwt.2017.05.036
Moghaddam M, Miran SNK, Pirbalouti AG, Mehdizadeh L, Ghaderi Y (2015) Variation in essential oil composition and antioxidant activity of cumin (Cuminum cyminum L.) fruits during stages of maturity. Ind Crops Prod 70:163–169. https://doi.org/10.1016/j.indcrop.2015.03.031
Morales H, Marín S, Ramos AJ, Sanchis V (2010) Influence of post-harvest technologies applied during cold storage of apples in Penicillium expansum growth and patulin accumulation: a review. Food Control 21(7):953–962. https://doi.org/10.1016/j.foodcont.2009.12.016
Mostafa YS, Hashem M, Alshehri AM, Alamri S, Eid EM, Ziedan E-SH, Alrumman SA (2021) Effective management of cucumber powdery mildew with essential oils. Agriculture 11(11):1177. https://doi.org/10.3390/agriculture11111177
Mugao LG, Muturi PW, Gichimu BM, Njoroge EK (2020) In vitro control of Phytophthora infestans and Alternaria solani using crude extracts and essential oils from selected plants. Int J Agron 2020:1–10. https://doi.org/10.1155/2020/8845692
Nandhavathy G, Dharini V, Babu PA, Nambiar RB, Selvam SP, Sadiku ER, Kumar MM (2021) Determination of antifungal activities of essential oils incorporated-pomegranate peel fibers reinforced-polyvinyl alcohol biocomposite film against mango postharvest pathogens. Mater Today Proc 38:923–927. https://doi.org/10.1016/j.matpr.2020.05.384
Nassimi Z, Taheri P, Tarighi S (2019) Farnesol altered morphogenesis and induced oxidative burst–related responses in Rhizoctonia solani AG1-IA. Mycologia 111(3):359–370. https://doi.org/10.1080/00275514.2019.1600315
Nicosia MGLD, Pangallo S, Raphael G, Romeo FV, Strano MC, Rapisarda P, Droby S, Schena L (2016) Control of postharvest fungal rots on citrus fruit and sweet cherries using a pomegranate peel extract. Postharvest Biol Technol 114:54–61. https://doi.org/10.1016/j.postharvbio.2015.11.012
Noda J, Brito N, González C (2010) The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol 10(1):1–15. https://doi.org/10.1016/j.plantsci.2016.06.009
Pavela R, Benelli G (2016) Essential oils as ecofriendly biopesticides? Challenges and constraints. Trends Plant Sci 21(12):1000–1007. https://doi.org/10.1016/j.tplants.2016.10.005
Perczak A, Gwiazdowska D, Marchwińska K, Juś K, Gwiazdowski R, Waśkiewicz A (2019) Antifungal activity of selected essential oils against Fusarium culmorum and F. graminearum and their secondary metabolites in wheat seeds. Arch Microbiol 201:1085–1097. https://doi.org/10.1007/s00203-019-01673-5
Perina FJ, Belan LL, Moreira SI, Nery EM, Alves E, Pozza EA (2019a) Diagrammatic scale for assessment of Alternaria brown spot severity on tangerine leaves. J Plant Pathol 101:981–990. https://doi.org/10.1007/s42161-019-00306-6
Perina FJ, de Andrade CCL, Moreira SI, Nery EM, Ogoshi C, Alves E (2019b) Cinnamomun zeylanicum oil and trans-cinnamaldehyde against Alternaria brown spot in tangerine: direct effects and induced resistance. Phytoparasitica 47:575–589. https://doi.org/10.1007/s12600-019-00754-x
Philippe V, Neveen A, Marwa A, Basel A-YA (2021) Occurrence of pesticide residues in fruits and vegetables for the Eastern Mediterranean Region and potential impact on public health. Food Control 119:107457. https://doi.org/10.1016/j.foodcont.2020.107457
Phillips CA, Laird K, Allen S (2012) The use of Citri-V™®—An antimicrobial citrus essential oil vapour for the control of Penicillium chrysogenum, Aspergillus niger and Alternaria alternata in vitro and on food. Food Res Int 47(2):310–314. https://doi.org/10.1016/j.foodres.2011.07.035
Plodpai P, Chuenchitt S, Petcharat V, Chakthong S, Voravuthikunchai SP (2013) Anti-Rhizoctonia solani activity by Desmos chinensis extracts and its mechanism of action. Crop Prot 43:65–71. https://doi.org/10.1016/j.cropro.2012.09.004
Plotto A, Roberts D, Roberts R (2002) Evaluation of plant essential oils as natural postharvest disease control of tomato (Lycopersicon esculentum). XXVI Int Hortic Congr: Issues and Advances in Postharvest Horticulture 628:737–745. https://doi.org/10.17660/ActaHortic.2003.628.93
Porcino MM, Oliveira V, da Silva HF, de Souza M, Do Nascimento LC (2023) Essential oils in the management of Alternaria alternata f. sp. citri in ‘Dancy’tangerine fruits. Rev Caatinga 36:291–299. https://doi.org/10.1590/1983-21252023v36n206rc
Raveau R, Fontaine J, Lounès-Hadj SA (2020) Essential oils as potential alternative biocontrol products against plant pathogens and weeds: a review. Foods 9(3):365. https://doi.org/10.3390/foods9030365
Restuccia C, Oliveri Conti G, Zuccarello P, Parafati L, Cristaldi A, Ferrante M (2019) Efficacy of different citrus essential oils to inhibit the growth and B1 aflatoxin biosynthesis of Aspergillus flavus. Environ Sci Pollut Res 26:31263–31272. https://doi.org/10.1007/s11356-019-06169-9
Reyes-Jurado F, Navarro-Cruz AR, Ochoa-Velasco CE, Palou E, López-Malo A, Ávila-Sosa R (2020) Essential oils in vapor phase as alternative antimicrobials: a review. Crit Rev Food Sci Nutr 60(10):1641–1650. https://doi.org/10.1080/10408398.2019.1586641
Riyahi M, Taheri P, Mamarabadi M (2018) Identification of Alternaria spp. in orange trees of Golestan and Mazandaran provinces and investigating their virulence on orange cultivars. Iran J Plant Prot Sci 48(2):183–196. https://doi.org/10.22059/ijpps.2017.233507.1006787
Rotem J (1994) The genus Alternaria: biology, epidemiology, and pathogenicity. American Phytopathological Society
Salvatore MM, Nicoletti R, Andolfi A (2022) Essential oils in citrus fruit ripening and postharvest quality. Hortic 8(5):396. https://doi.org/10.3390/horticulturae8050396
Seif AA, Hillocks RJ (1993) Phaeoramularia fruit and leaf spot of citrus with special reference to Kenya. Int J Pest Management 39:44–50. https://doi.org/10.1080/09670879309371757
Sephton-Clark PC, Voelz K (2018) Spore germination of pathogenic filamentous fungi. Adv Appl Microbiol 102:117–157. https://doi.org/10.1016/bs.aambs.2017.10.002
Sharifi A, Mohammadzadeh A, Zahraei Salehi T, Mahmoodi P (2018) Antibacterial, antibiofilm and antiquorum sensing effects of Thymus daenensis and Satureja hortensis essential oils against Staphylococcus aureus isolates. J Appl Microbiol 124(2):379–388. https://doi.org/10.1111/jam.13639
Sharma A, Rajendran S, Srivastava A, Sharma S, Kundu B (2017) Antifungal activities of selected essential oils against Fusarium oxysporum f. sp. lycopersici 1322, with emphasis on Syzygium aromaticum essential oil. J Biosci Bioeng 123(3):308–313. https://doi.org/10.1016/j.jbiosc.2016.09.011
Sharma N, Tripathi A (2008) Effects of Citrus sinensis (L.) Osbeck epicarp essential oil on growth and morphogenesis of Aspergillus niger (L.) Van Tieghem. Microbiol Res 163(3):337–344. https://doi.org/10.1016/j.micres.2006.06.009
Shehata SA, Abdeldaym EA, Ali MR, Mohamed RM, Bob RI, Abdelgawad KF (2020) Effect of some citrus essential oils on post-harvest shelf life and physicochemical quality of strawberries during cold storage. Agron 10(10):1466. https://doi.org/10.3390/agronomy10101466
Sil A, Pramanik K, Samantaray P, Firoz M, Yadav V (2020) Essential oils: a boon towards eco-friendly management of phytopathogenic fungi. J Entomol Zool Stud 8:1884–1891
Simmons EG (2007) Alternaria: an identification manual. [CBS Biodiversity Series no. 6.]. CBS-KNAW Fungal Biodiversity Centre, Utrecht
Singh P, Shukla R, Prakash B, Kumar A, Singh S, Mishra PK, Dubey NK (2010) Chemical profile, antifungal, antiaflatoxigenic and antioxidant activity of Citrus maxima Burm. and Citrus sinensis (L.) Osbeck essential oils and their cyclic monoterpene, DL-limonene. Food Chem Toxicol 48(6):1734–1740. https://doi.org/10.1016/j.fct.2010.04.001
Sun J, Zhang X, Zheng J, Liu G, Chen L (2023) Importance of Cell Wall Permeability and Cell Wall Degrading Enzymes during Infection of Botrytis cinerea in Hazelnut. Forests 14(3):565. https://doi.org/10.3390/f14030565
Sunitha V, Nirmala Devi D, Srinivas C (2013) Extracellular enzymatic activity of endophytic fungal strains isolated from medicinal plants. World J Agric Sci 9(1):1–9. https://doi.org/10.5829/idosi.wjas.2013.9.1.72148
Taheri P, Soweizy M, Tarighi S (2023) Application of essential oils to control some important fungi and bacteria pathogenic on cereals. J Nat Pest Res 6:100052. https://doi.org/10.1016/j.napere.2023.100052
Taheri P, Tarighi S (2010) Riboflavin induces resistance in rice against Rhizoctonia solani via jasmonate-mediated priming of phenylpropanoid pathway. J Plant Physiol 167(3):201–208. https://doi.org/10.1016/j.jplph.2009.08.003
Tanabe K, Park P, Takashi T, et al (1995) Characterization of the Mutants of Alternaria alternata Japanese Pear Pathotype Deficient in Melanin Production and Their Pathogenicity. JJP 61:27–33. https://doi.org/10.3186/jjphytopath.61.27
Tao N, OuYang Q, Jia L (2014) Citral inhibits mycelial growth of Penicillium italicum by a membrane damage mechanism. Food Control 41:116–121. https://doi.org/10.1016/j.foodcont.2014.01.010
Tomazoni EZ, Pauletti GF, da Silva Ribeiro RT, Moura S, Schwambach J (2017) In vitro and in vivo activity of essential oils extracted from Eucalyptus staigeriana, Eucalyptus globulus and Cinnamomum camphora against Alternaria solani Sorauer causing early blight in tomato. Sci Hortic 223:72–77. https://doi.org/10.1016/j.scienta.2017.04.033
Trabelsi D, Hamdane AM, Said MB, Abdrrabba M (2016) Chemical composition and antifungal activity of essential oils from flowers, leaves and peels of Tunisian Citrus aurantium against Penicillium digitatum and Penicillium italicum. J Essent Oil Bear Plants 19(7):1660–1674. https://doi.org/10.1080/0972060X.2016.1141069
Tranchida PQ, Bonaccorsi I, Dugo P, Mondello L, Dugo G (2012) Analysis of Citrus essential oils: state of the art and future perspectives. A review. Flavour Fragrance J 27(2):98–123. https://doi.org/10.1002/ffj.2089
Van Hung P, Chi PTL, Phi NTL (2013) Comparison of antifungal activities of Vietnamese citrus essential oils. Nat Prod Res 27(4-5):506–508. https://doi.org/10.1080/14786419.2012.706293
Vega B, Dewdney MM (2014) QoI-resistance stability in relation to pathogenic and saprophytic fitness components of Alternaria alternata from citrus. Plant Dis 98(10):1371–1378. https://doi.org/10.1094/PDIS-01-14-0078-RE
Vicent A, Armengol J, Sales R, García-Jiménez J, Alfaro-Lassala F (2000) First report of Alternaria brown spot of citrus in Spain. Plant Dis 84(9):1044–1044. https://doi.org/10.1094/PDIS.2000.84.9.1044B
Villa F, Cappitelli F, Cortesi P, Kunova A (2017) Fungal biofilms: targets for the development of novel strategies in plant disease management. Front Microbiol 8:654. https://doi.org/10.3389/fmicb.2017.00654
Villaverde JJ, Sevilla Morán B, Sandín España P, López-Goti C, Alonso Prados JL (2014) Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Manage Sci 70(1):2–5. https://doi.org/10.1002/ps.3663
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(12):1130–1138. https://doi.org/10.1016/j.foodcont.2007.12.003
Wang H, Fu L, Li C, Zhang X, Narcisse KE, Qi H, Han C, Wang X, Ma H, Zhu C, Zheng F (2023) Tannic acid exerts antifungal activity in vitro and in vivo against Alternaria alternata causing postharvest rot on apple fruit. Physiol Mol Plant Pathol 125:102012. https://doi.org/10.1016/j.pmpp.2023.102012
Wei X, Zheng K, Chen M, Liu G, Li J, Lei Y, Qin Y, Qu Y (2011) Transcription analysis of lignocellulolytic enzymes of Penicillium decumbens 114–2 and its catabolite-repression-resistant mutant. C R Biol 334(11):806–811. https://doi.org/10.1016/j.crvi.2011.06.002
Weisany W, Samadi S, Tahir NA, Amini J, Hossaini S (2022) Nano-encapsulated with mesoporous silica enhanced the antifungal activity of essential oil against Botrytis cinerea (Helotiales; Sclerotiniaceae) and Colletotrichum nymphaeae (Glomerellales; Glomerellaceae). Physiol Mol Plant Pathol 122:101902. https://doi.org/10.1016/j.pmpp.2022.101902
Wood TM, Bhat KM (1988) Methods for measuring cellulase activities. In: Methods in enzymology, vol 160. Elsevier, pp 87–112. https://doi.org/10.1016/0076-6879(88)60109-1
Wu Y, Yin Y, Chen X, Zhou Y, Jiang S, Zhang M, Cai G, Gao Q (2023) Effect of novel botanical synergist on the effectiveness and residue behavior of prothioconazole in wheat field. Sci Rep 13:20353. https://doi.org/10.1038/s41598-023-47797-z
Yu S, Zhen C, Zhao P, j L, Qin Z, Gao H (2023) Antifungal mechanisms of γ-aminobutyric acid against the postharvest pathogen Alternaria alternata. LWT 173:114314. https://doi.org/10.1016/j.lwt.2022.114314
Zhou T, Wang X, Ye B, Shi L, Bai X, Lai T (2018a) Effects of essential oil decanal on growth and transcriptome of the postharvest fungal pathogen Penicillium expansum. Postharvest Biol Technol 145:203–212. https://doi.org/10.1016/j.postharvbio.2018.07.015
Zhou Y, Huang L-J, Zhao Y-J, Tang N-Y, Qu R-J, Tang X-Q, Wang K-C (2018b) Changes of ion absorption, distribution and essential oil components of flowering Schizonepeta tenuifolia under salt stress. Zhongguo Zhong Yao Za Zhi= Zhongguo Zhongyao Zazhi= China J Chin Mater Med 43(22):4410–4418. https://doi.org/10.19540/j.cnki.cjcmm.20180820.013
Zorzi Tomazoni E, Ribeiro RT, Pauletti GF, Soares GL, Schwambach J (2019) Inhibition of Alternaria stem canker on tomato by essential oils from Baccharis species. J Environ Sci Health Part B 54(9):781–790. https://doi.org/10.1080/03601234.2019.1633212
Funding
We thank Ferdowsi University of Mashhad, Iran, for the financial support of this research with project number 3/45005 approved on 1st October 2017.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Samandari-Najafabadi, N., Taheri, P. & Tarighi, S. Antifungal and antivirulence effects of Citrus sinensis essential oil on Alternaria pathogens in orange. J Plant Pathol (2024). https://doi.org/10.1007/s42161-024-01638-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s42161-024-01638-8