Abstract
Anthracnose and crown-rot postharvest diseases of banana fruit are responsible for major postharvest losses of the fruit. For natural control of these diseases, in vitro antifungal activity of cassia and holy basil essential oils was evaluated by disc volatilization method. Cassia essential oil at 6 μL per plate exhibited 100% growth inhibition of both the causative fungal pathogens, namely Colletotrichum musae and Lasiodiplodia theobromae. Holy basil essential oil was capable of completely inhibiting the growth of L. theobromae at 6 μL per plate, whereas it could inhibit C. musae up to 96% at 10 μL per plate. Molecular docking and conceptual DFT studies have been performed to ascertain the components of essential oils responsible for antifungal activity based on their binding affinities to chitin synthase protein and chemical behaviour. Components, such as eugenol, cinnamyl acetate, caryophyllene, humulene and trans-calamenene, may most likely be responsible for high activity of the tested essential oils as per the in silico results.
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Abdollahi A, Hassani A, Ghosta Y, Meshkatalsadat MH, Shabani R (2011) Screening of antifungal properties of essential oils extracted from sweet basil, fennel, summer savory and thyme against postharvest phytopathogenic fungi. J Food Saf 31:350–356. https://doi.org/10.1111/j.1745-4565.2011.00306.x
Adams RP (2007) Identification of essential oil components by gas chromatography/mass spectrometry, vol 456. Allured Publishing Corporation, Carol Stream
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Alvindia DG (2012) Revisiting hot water treatments in controlling crown rot of banana cv. Buñgulan. Crop Prot 33:59–64. https://doi.org/10.1016/j.cropro.2011.09.023
Amber K, Aijaz A, Immaculata X, Luqman KA, Nikhat M (2010) Anticandidal effect of Ocimum sanctum essential oil and its synergy with fluconazole and ketoconazole. Phytomedicine 17:921–925. https://doi.org/10.1016/j.phymed.2010.02.012
Baker D, Sali A (2001) Protein structure prediction and structural genomics. Science 294:93–96. https://doi.org/10.1126/science.1065659
Bakr RO, Zaghloul SS, Hassan RA, Sonousi A, Wasfi R, Fayed MA (2020) Antimicrobial activity of Vitex agnus-castus essential oil and molecular docking study of Its major constituents. J Essent Oil-Bear Plants 23:184–193. https://doi.org/10.1080/0972060X.2020.1727368
Becke AD (1993) Becke’s three parameter hybrid method using the LYP correlation functional. J Chem Phys 98:5648–5652
Boulogne I, Petit P, Ozier-Lafontaine H, Desfontaines L, Loranger-Merciris G (2012) Insecticidal and antifungal chemicals produced by plants: a review. Environ Chem Lett 10:325–347. https://doi.org/10.1007/s10311-012-0359-1
Colovos C, Yeates TO (1993) Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci 2:1511–1519. https://doi.org/10.1002/pro.5560020916
D’agostino M, Tesse N, Frippiat JP, Machouart M, Debourgogne A (2019) Essential oils and their natural active compounds presenting antifungal properties. Molecules 24:3713. https://doi.org/10.3390/molecules24203713
Da Silva JKR, Silva JRA, Nascimento SB, Da Luz SF, Meireles EN, Alves CN, Ramos AR, Maia JGS (2014) Antifungal activity and computational study of constituents from Piper divaricatum essential oil against Fusarium infection in black pepper. Molecules 19:7926–17942. https://doi.org/10.3390/molecules191117926
Dallakyan S, Olson AJ (2015) Small-molecule library screening by docking with PyRx. Chem Biol. https://doi.org/10.1007/978-1-4939-2269-7_19
David F, Sandra P, Wylie PL (2002) Improving the analysis of fatty acid methyl esters using retention time locked methods and retention time databases. Agilent Technologies-Application
Dhifi W, Bellili S, Jazi S, Bahloul N, Mnif W (2016) Essential oils’ chemical characterization and investigation of some biological activities: a critical review. Medicines 3:25. https://doi.org/10.3390/medicines3040025
Domingo L, Ríos-Gutiérrez M, Pérez P (2016) Applications of the conceptual density functional theory indices to organic chemistry reactivity. Molecules 21:748. https://doi.org/10.3390/molecules21060748
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
Eisenberg D, Lüthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Method Enzymol 277:396–404
Feng W, Zheng X (2006) Control of Alternaria alternata by cassia oil in combination with potassium chloride or sodium chloride. J Appl Microbiol 101:1317–1322. https://doi.org/10.1111/j.1365-2672.2006.03024.x
Frisch M, Trucks G, Schlegel H, Scuseria G, Robb M, Cheeseman J, Fox D (2016) Gaussian 16 (Version Revision B. 01) [Linux]
Fukui K (1982) The role of frontier orbitals in chemical reactions (nobel lecture). Angew Chem Int Ed Engl 21:801–809
Giordani R, Regli P, Kaloustian J, Portugal H (2006) Potentiation of antifungal activity of amphotericin B by essential oil from Cinnamomum cassia. Phytother Res 20:58–61. https://doi.org/10.1002/ptr.1803
Gucwa K, Milewski S, Dymerski T, Szweda P (2018) Investigation of the antifungal activity and mode of action of Thymus vulgaris, Citrus limonum, Pelargonium graveolens, Cinnamomum cassia, Ocimum basilicum, and Eugenia caryophyllus essential oils. Molecules 23:1116. https://doi.org/10.3390/molecules23051116
Hipólito TM, Bastos GT, Barbosa TW, de Souza TB, Coelho LF, Dias AL, Rodríguez IC, Dos Santos MH, Dias DF, Franco LL, Carvalho DT (2018) Synthesis, activity, and docking studies of eugenol-based glucosides as new agents against Candida sp. Chem Biol Drug Des 92(2):1514–1524. https://doi.org/10.1111/cbdd.13318
Hohenberg P, Kohn W (1964) Density functional theory (DFT). Phys Rev 136:B864
Hyldgaard M, Mygind T, Meyer RL (2012) Essential oils in food preservation: mode of action, synergies, and interactions with food matrix components. Front Microbiol 3:12. https://doi.org/10.3389/fmicb.2012.00012
Jiang Z, Jiang H, Xie P (2013) Antifungal activities against Sclerotinia sclerotiorum by Cinnamomum cassia oil and its main components. J Essent Oil Res 25:444–451. https://doi.org/10.1080/10412905.2013.782475
Kalia A (2020) Microbiology of fresh bananas and processed banana products. Handbook of banana production, postharvest science, processing technology, and nutrition. Wiley, New York, pp 245–267. https://doi.org/10.1002/9781119528265.ch13
Khaled KF (2011) Modeling corrosion inhibition of iron in acid medium by genetic function approximation method: a QSAR model. Corros Sci 53:3457–3465. https://doi.org/10.1016/j.corsci.2011.01.035
Kloucek P, Smid J, Frankova A, Kokoska L, Valterova I, Pavela R (2012) Fast screening method for assessment of antimicrobial activity of essential oils in vapor phase. Food Res Int 47:161–165. https://doi.org/10.1016/j.foodres.2011.04.044
Kocevski D, Du M, Kan J, Jing C, Lačanin I, Pavlović H (2013) Antifungal effect of Allium tuberosum, Cinnamomum cassia, and Pogostemon cablin essential oils and their components against population of Aspergillus species. J Food Sci 78:M731–M737. https://doi.org/10.1111/1750-3841.12118
Kumar A, Kudachikar VB (2018) Antifungal properties of essential oils against anthracnose disease: a critical appraisal. J Plant Dis Protect 125:133–144. https://doi.org/10.1007/s41348-017-0128-2
Kumar A, Shukla R, Singh P, Dubey NK (2010) Chemical composition, antifungal and antiaflatoxigenic activities of Ocimum sanctum L. essential oil and its safety assessment as plant based antimicrobial. Food Chem Toxicol 48:539–543. https://doi.org/10.1016/j.fct.2009.11.028
Laird K, Phillips C (2012) Vapour phase: a potential future use for essential oils as antimicrobials? Lett Appl Microbiol 54:169–174. https://doi.org/10.1111/j.1472-765X.2011.03190.x
Lenardon MD, Munro CA, Gow NA (2010) Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol 13:416–423. https://doi.org/10.1016/j.mib.2010.05.002
Lin BH, Yen ST, Huang CL, Smith TA (2009) US demand for organic and conventional fresh fruits: the roles of income and price. Sustainability 1:464–478. https://doi.org/10.3390/su1030464
Ma YN, Chen CJ, Li Q, Wang W, Xu FR, Cheng YX, Dong X (2019) Fungicidal activity of essential oils from Cinnamomum cassia against the pathogenic fungi of Panax notoginseng diseases. Chem Biodivers 16:e1900416. https://doi.org/10.1002/cbdv.201900416
Maduwanthi SDT, Marapana RAUJ (2019) Induced ripening agents and their effect on fruit quality of banana. Int J Food Sci. https://doi.org/10.1155/2019/2520179
Maqbool M, Ali A, Ramachandran S, Smith DR, Alderson PG (2010) Control of postharvest anthracnose of banana using a new edible composite coating. Crop Prot 29:1136–1141. https://doi.org/10.1016/j.cropro.2010.06.005
Mert BD, Mert ME, Kardaş G, Yazıcı B (2012) Experimental and theoretical studies on electrochemical synthesis of poly (3-amino-1, 2, 4-triazole). Appl Surf Sci 258:9668–9674. https://doi.org/10.1016/j.apsusc.2012.04.180
Mizuhara N, Kuroda M, Ogita A, Tanaka T, Usuki Y, Fujita KI (2011) Antifungal thiopeptide cyclothiazomycin B1 exhibits growth inhibition accompanying morphological changes via binding to fungal cell wall chitin. Bioorg Med Chem 19:5300–5310. https://doi.org/10.1016/j.bmc.2011.08.010
Murmu SB, Mishra HN (2018) Post-harvest shelf-life of banana and guava: mechanisms of common degradation problems and emerging counteracting strategies. Innov Food Sci Emerg Technol. https://doi.org/10.1016/j.ifset.2018.07.011
Nazzaro F, Fratianni F, Coppola R, Feo VD (2017) Essential oils and antifungal activity. Pharmaceuticals 10:86. https://doi.org/10.3390/ph10040086
O’Boyle NM, Banck M, James CA, Morley C, Vandermeersch T, Hutchison GR (2011) Open babel: an open chemical toolbox. J Cheminform 3:33. https://doi.org/10.1186/1758-2946-3-33
Pandey AK, Kumar P, Singh P, Tripathi NN, Bajpai VK (2017) Essential oils: sources of antimicrobials and food preservatives. Front Microbiol 7:2161. https://doi.org/10.3389/fmicb.2016.02161
Perumal AB, Sellamuthu PS, Nambiar RB, Sadiku ER (2016) Antifungal activity of five different essential oils in vapour phase for the control of Colletotrichum gloeosporioides and Lasiodiplodia theobromae in vitro and on mango. Int J Food Sci Tech 51:411–418. https://doi.org/10.1111/ijfs.12991
Powers CN, Osier JL, McFeeters RL, Brazell CB, Olsen EL, Moriarity DM, Satyal P, Setzer WN (2018) Antifungal and cytotoxic activities of sixty commercially-available essential oils. Molecules 23:1549. https://doi.org/10.3390/molecules23071549
Powers CN, Satyal P, Mayo JA, McFeeters H, McFeeters RL (2019) Bigger data approach to analysis of essential oils and their antifungal activity against Aspergillus niger, Candida albicans, and Cryptococcus neoformans. Molecules 24:2868. https://doi.org/10.3390/molecules24162868
Ranjitham Thangamani P, Kuppusamy P, Peeran MF, Gandhi K, Raguchander T (2011) Morphological and physiological characterization of Colletotrichum musae the causal organism of banana anthracnose. World J Agr Sci 7:743–754
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 60:1641–1650. https://doi.org/10.1080/10408398.2019.1586641
Sangeetha G, Anandan A, Rani SU (2012) Morphological and molecular characterisation of Lasiodiplodia theobromae from various banana cultivars causing crown rot disease in fruits. Arch Phytopathol Plant Prot 45:475–486. https://doi.org/10.1080/03235408.2011.587986
Šarac Z, Matejić JS, Stojanović-Radić ZZ, Veselinović JB, Džamić AM, Bojović S, Marin PD (2014) Biological activity of Pinus nigra terpenes—evaluation of FtsZ inhibition by selected compounds as contribution to their antimicrobial activity. Comput Biol Med 54:72–78. https://doi.org/10.1016/j.compbiomed.2014.08.022
Sellamuthu PS, Sivakumar D, Soundy P, Korsten L (2013) Essential oil vapours suppress the development of anthracnose and enhance defence related and antioxidant enzyme activities in avocado fruit. Postharvest Biol Technol 81:66–72. https://doi.org/10.1016/j.postharvbio.2013.02.007
Sutton BC, Waterston JM (1970) Colletotrichum musae.[Descriptions of Fungi and Bacteria]. IMI descriptions of fungi and bacteria. CAB International, Wallingford
Tariq S, Wani S, Rasool W, Shafi K, Bhat MA, Prabhakar A, Shalla AH, Rather MA (2019) A comprehensive review of the antibacterial, antifungal and antiviral potential of essential oils and their chemical constituents against drug-resistant microbial pathogens. Microb Pathog 134:103580. https://doi.org/10.1016/j.micpath.2019.103580
Tripathi P, Dubey NK, Shukla AK (2008) Use of some essential oils as post-harvest botanical fungicides in the management of grey mould of grapes caused by Botrytis cinerea. World J Microbiol Biotechnol 24:39–46. https://doi.org/10.1007/s11274-007-9435-2
Trott O, Olson AJ (2010) AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31:455–461. https://doi.org/10.1002/jcc.21334
Vieira TF, Sousa SF (2019) Comparing AutoDock and Vina in Ligand/Decoy Discrimination for Virtual Screening. Appl Sci 9:4538. https://doi.org/10.3390/app9214538
Vilaplana R, Hurtado G, Valencia-Chamorro S (2018) Hot water dips elicit disease resistance against anthracnose caused by Colletotrichum musae in organic bananas (Musa acuminata). LWT 95:247–254. https://doi.org/10.1016/j.lwt.2018.04.085
Wang H, Gu D, Wang M, Guo H, Wu H, Tian G, Li Q, Yang Y, Tian J (2017) A strategy based on gas chromatography–mass spectrometry and virtual molecular docking for analysis and prediction of bioactive composition in natural product essential oil. J Chromatogr A 1501:128–133. https://doi.org/10.1016/j.chroma.2017.04.031
Wang H, Yang Z, Ying G, Yang M, Nian Y, Wei F, Kong W (2018) Antifungal evaluation of plant essential oils and their major components against toxigenic fungi. Ind Crop Prod 120:180–186. https://doi.org/10.1016/j.indcrop.2018.04.053
Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35(suppl_2):W407-W410. https://doi.org/10.1093/nar/gkm290
Wightwick A, Walters R, Allinson G, Reichman S, Menzies N (2010) Environmental risks of fungicides used in horticultural production systems. Fungicides. https://doi.org/10.5772/13032
Xu D, Zhang Y (2013) Toward optimal fragment generations for ab initio protein structure assembly. Proteins: structure. Funct Bioinform 81:229–239. https://doi.org/10.1002/prot.24179
Xu SX, Li YC, Liu X, Mao LJ, Zhang H, Zheng XD (2012) In vitro and in vivo antifungal activity of a water-dilutable cassia oil microemulsion against Geotrichum citri-aurantii. J Sci Food Agic 92:2668–2671. https://doi.org/10.1002/jsfa.5686
Zhan CG, Nichols JA, Dixon DA (2003) Ionization potential, electron affinity, electronegativity, hardness, and electron excitation energy: molecular properties from density functional theory orbital energies. J Phys Chem A 107:4184–4195. https://doi.org/10.1021/jp0225774
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Kulkarni, S.A., Sellamuthu, P.S., Anitha, D.P.M. et al. In vitro and in silico evaluation of antifungal activity of cassia (Cinnamomum cassia) and holy basil (Ocimum tenuiflorum) essential oils for the control of anthracnose and crown-rot postharvest diseases of banana fruits. Chem. Pap. 75, 2043–2057 (2021). https://doi.org/10.1007/s11696-020-01434-5
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DOI: https://doi.org/10.1007/s11696-020-01434-5