Antifungal Activity of Essential Oil and Hydrosol Extract of Ballota nigra L. and their Protective Effects Against the Black Rot of Tomatoes

Author(s): Nabila A. Sebaa*, Amina T. Zatla, Mohammed E.A. Dib, Boufeldja Tabti, Jean Costa, Alain Muselli.

Journal Name: Current Nutrition & Food Science

Volume 15 , Issue 7 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Background: Bellota species are used to treat various diseases in traditional folk medicine.

Objectives: This study aimed to chemically characterize the essential oils and the hydrosol extract and regional specificity of the major components of Ballota nigra essential oil and to evaluate their in vitro and in vivo antifungal activities.

Methods: Essential oils were obtained by a Clevenger-type apparatus and analyzed by using Gas Chromatography (GC) and Gas Chromatography Mass Spectroscopy (GC/MS). The antifungal activities were tested to three phytopathogenic stains (Penicillium expansum, Aspergillus niger and Alternaria alternata).

Results: Altogether, 38 compounds were identified in the essential oils, representing 92.1-96.8% of the total oil composition. Their main constituents were E-β-caryophyllene (4.8-24.6%), E-β-farnesene (3.3-22.9%), β-bisabolene (7.6-30.2%), α-humulene (2.1-13.3%) and geranyl linalool (1.1-8.2%). The statistical methods deployed confirmed that there is a relation between the essential oil compositions and the harvest locations. Hydrosol extract was constituted by seven components, represented principally by methyl eugenol (75.2%) and caryophyllene oxide (12.5%). The results of in vitro antifungal activity with essential oil and hydrosol extract have shown very interesting antifungal activities on Penicillium expansum and Alternaria alternata strains with percentage reductions up to 80%. Additionally, in in vivo assays, Ballota nigra essential oil and hydrosol extract significantly reduce decay in artificially inoculated tomato by Alternaria alternata.

Conclusion: The essential oil and hydrosol extract can be used as a potential source of sustainable eco-friendly botanical fungicides to protect stored tomatoes from pathogens, saprophytic fungi causing bio-deterioration to a variety of food commodities.

Keywords: Ballota nigra, essential oil, hydrosol extract, in vivo antifungal infections, protective effect, black rot of tomatoes.

Schnaubelt K. Essential oil therapy according to traditional Chinese medical concepts. Int J Aromather 2005; 15: 98-105.
Konyalıoglu S, Karamenderes C. Screening of total flavonoid, phenol contents and antioxidant capacities of Achillea L. species growing in Turkey. Acta Pharm Turc 2004; 46: 163-70.
Kordali S, Cakir A, Akcin TA, et al. Antifungal and herbicidal properties of essential oils and n-hexane extracts of Achillea gypsicola Hub-Mor. and Achillea biebersteinii Afan. (Asteraceae). Ind Crop Prod 2009; 29: 562-70.
Tian J, Ban X, Zeng H, He J, Huang B, Wang Y. Chemical composition and antifungal activity of essential oil from Cicuta virosa L. var. latisecta Celak. Int J Food Microbiol 2011; 145: 464-70.
Feng W, Chen J, Zheng X, Liu L. Thyme oil to control Alternaria alternata in-vitro and in-vivo as fumigant and contact treatments. Food Control 2011; 22: 78-81.
Soylu EM, Kurt Ş, Soylu S. In-vitro and in-vivo antifungal activities of the essential oils of various plants against tomato grey mould disease agent Botrytis cinerea. Int J Food Microbiol 2010; 143: 183-9.
Tzortzakis NG. Ethanol, vinegar and Origanum vulgare oil vapour suppress the development of anthracnose rot in tomato fruit. Int J Food Microbiol 2010; 142: 14-8.
Weisheimer V, Miron D, Silva CB, Guterres SS, Schapoval EES. Microparticles containing lemongrass volatile oil: Preparation, characterization and thermal stability. Pharmazie 2010; 65: 885-90.
Zore GB, Thakre AD, Rathod V, Karuppayil SM. Evaluation of anti-Candida potential of geranium oil constituents against clinical isolates of Candida albicans differentially sensitive to fluconazole: inhibition of growth, dimorphism and sensitization. Mycoses 2011a 54(4): 99-109.
Zore GB, Thakre AD, Rathod V, Karuppayil SM. Terpenoids inhibit Candida albicans growth by affecting membrane integrity and arrest of cell cycle. Phytomedicine 2011b 18: 1181-90.
Kazemizadeh Z, Amini T, Nazari F, Habibi Z. Volatile constituents of Ballota nigra subsp. anatolica from Iran. Chem Nat Compd 2009; 45(5): 737-8.
Tipirdamaz R, Guvenc V. Seed fatty acids composition of Ballota cristata. Chem Nat Compd 2004; 40(3): 291-2.
Bader A, Caponi C, Cioni PL, Flamini G, Morelli I. Composition of the essential oil of Ballota undulata, B. nigra ssp. foetida and B. saxatilis. Flavour Fragr J 2003; 18(6): 502-4.
Semnani KM, Saeedi M, Akbarzadeh M. The essential oil composition of Ballota nigra. Chem Nat Compd 2007; 43(6): 722-3.
Vukovic N, Sukdolak S, Solujic S, Niciforovic N. Antimicrobial activity of the essential oil obtained from roots and chemical composition of the volatile constituents from the roots, stems, and leaves of Ballota nigra from Serbia. J Med Food 2009; 12(2): 435-41.
Fraternale D, Ricci D. Essential oil composition and antifungal activity of aerial parts of Ballota nigra ssp. foetida collected at flowering and fruiting times. Nat Prod Commun 2014; 9(7): 1015-8.
Jennings W, Shibamoto T. Qualitative analysis of flavour and fragrance volatiles by glass-capillary gas chromatography. In: Jovanovich HB, Ed. 1st ed. Academic Press: New York 1980.
König WA, Hochmuth DH, Joulain D. Terpenoids and Related Constituents of Essential oils first ed Library of Mass Finder 21, Institute of Organic Chemistry, Hamburg . 2001.
National Institute of Standards and Technology. NIST Chemistry WebBook, Reference Database, Gaisthersburg, MD 2008. Available at:
Mc Lafferty FW, Stauffer DB. The Wiley/NBS Registry of Mass Spectra Data. 1st ed. Wiley-Interscience New York 1988.
Mc Lafferty FW, Stauffer DB. Wiley Registry of Mass Spectral Data 6th ed Mass Spectrometry Library Search System Bench- Top/PBM version 310d Palisade: Newfield. 1994.
National Institute of Standards and Technology. PC Version 17 of the NIST/EPA/NIH Mass Spectral Library. Perkin-Elmer Corp Norwalk, CT, USA: 1999.
Barnett HL, Hunter BB. Illustrated genera of imperfect fungi. 4th ed. The American Phytopatological Society St. Paul Minnesota 2006.
Samson RA, Hoekstra ES, Frisvad JC. Introduction to Food and Airborne Fungi 7th ed Centraal bureau voor Schimmel cultures: Utrecht . 2001.
Belabbes R, Dib MEA, Djabou N, et al. Chemical variability, antioxidant and antifungal activities of essential oils and hydrosol extract of Calendula arvensis L. from Western Algeria. Chem Biodiversity 2017; 14e1600482
Pandey DK, Tripathi NN, Tripathi RD. Fungitoxic and phytotoxic properties of essential oil of Hyptissu aveolens. J Plant Dis Prot 1982; 89: 344-9.
Li Y. Department of Plant Pathology and Ecology, The Connecticut Agricultural Experiment Station 2013. Available at
Collignon B. Hydrogeologies appliquees des aquifères karstiques des monts de Tlemcen PhD dissertation Avignon University 1986.
Kaya A, Kürkçüoğlu M, Dinç M, Doğu S. Compositions of the essential oils of Ballota nigra subsp. uncinata and subsp. anatolica from Turkey. Indian J Pharm Educ 2017; 51(3): 185-9.
Sacchetti G, Maietti S, Muzzoli M, et al. Comparative evaluation of 11 essential oils of different origin as functional antioxidants, antiradicals and antimicrobials in foods. Food Chem 2005; 91(4): 621-32.
Pirbalouti AG, Hashemi M, Ghahfarokhi FT. Essential oil and chemical compositions of wild and cultivated Thymus daenensis Celak and Thymus vulgaris L. Ind Crop Prod 2013; 48: 43-8.
Sabulal B, Dan M, Kurup AJR, et al. Caryophyllene-rich rhizome oil of Zingiber nimmonii from South India: chemical characterization and antimicrobial activity. Phytochemistry 2006; 67(22): 2469-73.
Fernandes ES, Passos GF, Medeiros R, et al. Anti-inflammatory effects of compounds alpha-humulene and (−)- trans-caryophyllene isolated from the essential oil of Cordia verbenacea. Eur J Clin Pharmacol 2007; 569(3): 228-36.
Dahham SS, Tabana YM, Iqbal MA, et al. The Anticancer, antioxidant and antimicrobial properties of the sesquiterpene β-caryophyllene from the essential oil of Aquilaria crassna. Molecules 2015; 20(7): 11808-29.
Lahlou M. Essential oils and fragrance compounds: bioactivity and mechanisms of action. Flavour Fragr J 2004; 19(2): 159-65.
Shaalan EAS, Canyon DV, Bowden B, et al. Efficacy of botanical extracts from Callitris glaucophylla, against Aedes aegypti and Culex annulirostris mosquitoes. Trop Biomed 2006; 23: 180-5.
Yang D, Michel L, Pierre Chaumont J, Millet-Clerc J. Use of caryophyllene oxide as an antifungal agent in an in vitro experimental model of onychomycosis. Mycopathologia 1999; 148: 79-82.
D’auria FD, Tecca M, Strippoli V, Salvatore G, Battinelli L, Mazzanti G. Antifungal activity of Lavandula angustifolia essential oil against Candida albicans yeast and mycelial form. Med Mycol 2005; 43(5): 391-6.
Campaniello D, Corbo MR, Sinigaglia M. Activité antifongique d'Eugénol contre les espèces de Penicillium, Aspergillus et Fusarium. J Food Protect 2010; 73(6): 1124-8.
Foolad MR, Panthee DR. Marker-assisted selection in tomato breeding. Crit Rev Plant Sci 2012; 31(2): 93-123.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Page: [662 - 671]
Pages: 10
DOI: 10.2174/1573401314666180515114935
Price: $65

Article Metrics

PDF: 25
PRC: 1