Abstract
Recovery of bioactive compounds from wastes is gaining interest because they could add value to by-products arising from, for example, the oil extraction processes. In this work, green solvent extraction (water/ethanol under sub-critical conditions) was used to obtain bioactive compounds from peanut, sesame and pistachio agro-industrial by-products. Extracts were analyzed in their overall chemical composition and tested on growth, ergosterol and fumonisin FB1 production by Fusarium verticillioides. The effects of the extracts on fungal growth rate and biochemical markers were not univocal, and could be associated to differences in their chemical profiles. Extracts obtained from peanut skin—composed mainly by monomeric and dimeric flavonoids—caused significant reductions in fungal growth rate but increased FB1 production. Extracts from sesame seeds—dominated by furofuran-type lignans—did not have a clear inhibitory effect on growth rate but strongly reduced both FB1 and ergosterol production. Extracts from pistachio nuts—characterized by monomeric flavonoids and gallic acid derivatives—showed minor effects on both fungal growth rate and biochemical markers. Sub-critical fluid extraction of peanut skin and defatted sesame seeds may provide an efficient method to obtain extracts rich in phenolic and lignan compounds with potential use as antifungal agents.
Graphic Abstract
Similar content being viewed by others
Abbreviations
- FB1 :
-
Fumonisin B1
- GA:
-
Galic acid
- HPLC–ESI–MS/MS:
-
High pressure liquid chromatography–electrospray ionization–mass spectroscopy
- PNC:
-
Pistachio nuts cake
- PS:
-
Peanut skin
- SSC:
-
Sesame seed cake
- SFE:
-
Sub-critical fluid extraction
- TPC:
-
Total phenol content
References
Banerjee, J., Singh, R., Vijayaraghavan, R., MacFarlane, D., Patti, A.F., Arora, A.: Bioactives from fruit processing wastes: green approaches to valuable chemicals. Food Chem. 225, 10–22 (2017)
Lai, W.T., Khong, N.M.H., Lim, S.S., Hee, Y.Y., Sim, B.Y., Lau, K.Y., Lai, O.M.: A review: modified agricultural by-products for the development and fortification of food products and nutraceuticals. Trends Food Sci. Technol. 59, 148–160 (2016)
Nazzaro, F., Fratianni, F., Ombra, M.N., D’Acierno, A., Coppola, R.: Recovery of biomolecules of high benefit from food waste. Curr. Opin. Food Sci. 22, 43–54 (2018)
Sunil, L., Appaiah, P., Prasanth Kumar, P.K., Gopala Krishna, A.G.: Preparation of food supplements from oilseed cakes. J. Food Sci. Technol. 52, 2998–3005 (2014)
Sarkis, J.R., Correa, A.P.F., Michel, I., Brandeli, A., Tessaro, I.C., Marczak, L.D.F.: Evaluation of the phenolic content and antioxidant activity of different seed and nut cakes from the edible oil industry. J. Am. Oil Chem. Soc. 91, 1773–1782 (2014)
Terpinc, P., Ceh, B., Ulrih, N.P., Abramoviˇc, H.: Studies of the correlation between antioxidant properties and the total phenolic content of different oil cake extracts. Ind. Crops Prod. 39, 210–217 (2012)
Ramachandran, S., Singh, S.K., Larroche, C., Soccol, C.R., Pandey, A.: Oil cakes and their biotechnological applications—a review. Bioresour. Technol. 98, 2000–2009 (2007)
Meriles, J.M., Giorda, L.M., Maestri, D.M.: Effect of planting date on Fusarium spp. and Diaporthe/Phomopsis complex incidence and its relationship with soybean seed quality. J. Phytopathol. 150, 606–610 (2002)
IARC: International Agency for Research on Cancer.: IARC Monographs on the Evaluation of the Carcinogenic Risks to Humans: Some Traditional Herbal Medicines, Some Mycotoxins, Naphthalene and Styrene, vol. 82, pp. 301–366. International Agency for Research on Cancer, Lyon (2002)
Agrios, G.: Plant Pathol, 5th edn. Elsevier Academic Press, Nueva York (2005)
Błaszczak-Świątkiewicz, K., Sikora, J., Szymański, J., Danilewicz, M., Mikiciuk-Olasik, E.: Biological evaluation of the toxicity and the cell cycle interruption by some benzimidazole derivatives. Tumor Biol. 37, 11135–11145 (2016)
Seiber, J.N., Coats, J., Duke, S.O., Gross, A.D.: Biopesticides: state of the art and future opportunities. J. Agric. Food Chem. 62, 11613–11619 (2014)
Barral, B., Chillet, M., Minier, J., Lechaudel, M., Schorrgalindo, S.: Evaluating the response to Fusarium ananatum inoculation and antifungal activity of phenolic acids in pineapple. Fungal Biol. 121, 1045–1053 (2017)
Wang, S., Zheng, Y., Xiang, F., Li, S., Yang, G.: Antifungal activity of Momordica charantia seed extracts toward the pathogenic fungus Fusarium solani L. J. Food Drug Anal. 24, 881–887 (2016)
Brado Avanço, G., Dias Ferreira, F., Silva Bomfim, N., De Souza, A., Rodrigues dos Santos, P., Peralta, R.M., Brugnari, T., Mallmann, C.A., de Abreu, Alves, Filho, B., Graton Mikcha, J.M., Machinski, M.: Curcuma longa L. essential oil composition, antioxidant effect, and effect on Fusarium verticillioides and fumonisin production. Food Control 73, 806–813 (2017)
Dambolena, J.S., López, A.G., Meriles, J.M., Rubinstein, H.R., Zygadlo, J.A.: Inhibitory effect of 10 natural phenolic compounds on Fusarium verticillioides. A structure property activity relationship study. Food Control 28, 63–70 (2012)
Da Silva, Bomfim N., Polis Nakassugi, L., Faggion Pinheiro Oliveira, J., Yumie Kohiyama, C., Aparecida, S., Mossini, G., Grespan, R., Botião Nerilo, S., Mallmann, C.A., Abreu Filho, B.A., Machinski, M.: Antifungal activity and inhibition of fumonisin production by Rosmarinus officinalis L. essential oil in Fusarium verticillioides (Sacc.) Nirenberg. Food Chem. 166, 330–336 (2015)
Bodoira, R., Velez, A., Andreatta, A.E., Martinez, M., Maestri, D.: Extraction of bioactive compounds from sesame (Sesamum indicum L.) defatted seeds using water and ethanol under sub-critical conditions. Food Chem. 237, 114–120 (2017)
Ben Othman, S., Katsuno, N., Kanamaru, Y., Yabe, T.: Water-soluble extracts from defatted sesame seed flour show antioxidant activity in vitro. Food Chem. 175, 306–314 (2015)
Esmaeilzadeh, B.S., Sharifi, M., Behmanesh, M., Safaie, N., Murata, J., Araki, R., Yamagaki, T., Satake, H.: Time-course changes in fungal elicitor-induced lignan synthesis and expression of the relevant genes in cell cultures of Linum album. J. Plant Physiol. 169, 487–491 (2012)
Kulik, T., Busko, M., Pszczółkowska, A., Perkowsk, J., Okorski, A.: Plant lignans inhibit growth and trichothecene biosynthesis in Fusarium graminearum Lett. Appl. Microbiol. 59(99), 107 (2014)
Barbary, O.M., El-Sohaimy, S.A., El-Saadani, M.A., Zeitoun, A.M.A.: Antioxidant, antimicrobial and anti-HCV activities of lignan extracted from flaxseed. Res. J. Agric. Biol. Sci. 6, 247–256 (2010)
Nishiwaki, H., Nakazaki, S., Akiyama, K., Yamauchi, S.: Structure-antifungal activity relationship of fluorinated dihydroguaiaretic acid derivatives and preventive activity against Alternaria alternata Japanese pear pathotype. J. Agric. Food Chem. 65, 6701–6707 (2017)
Ma, Y.Y., Cagnazzo, A.K., Kerr, W.L., Amarowicz, R., Swanson, R.B., Pegg, R.B.: Separation and characterization of phenolic compounds from dry-blanched peanut skins by liquid chromatography–electrospray ionization mass spectrometry. J. Chromatogr. A 1356, 64–81 (2014)
Bodoira, R., Rossi, Y., Montenegro, M., Maestri, D., Velez, A.: Extraction of antioxidant polyphenolic compounds from peanut skin using water-ethanol at high pressure and temperature conditions. J. Supercrit. Fluid 128, 57–65 (2017)
Pizzolitto, R.P., Dambolena, J.S., Zunino, M.P., Larrauri, M., Grosso, N.R., Nepote, V., Dalcero, A.M., Zygadlo, J.A.: Activity of natural compounds from peanut skins on Fusarium verticillioides growth and fumonisin B1 production. Ind. Crops Prod. 47, 286–290 (2013)
Sarnoski, P., Boyer, R., O’Keefe, S.F.: Application of proanthocyanidins from peanut skins as a natural yeast inhibitory agent. J. Food Sci. 77, 242–249 (2012)
Rajaei, A., Barzegar, M., Mobarez, A.M., Sahari, M.A., Esfahani, Z.H.: Antioxidant, anti-microbial and antimutagenicity activities of pistachio (Pistachio vera) green hull extract. Food Chem. Toxicol. 48, 107–112 (2010)
Chemat, F., Rombaut, N., Meullemiestre, A., Turk, M., Perino, S., Fabiano-Tixier, A.S., Abert-Vian, M.: Review of green food processing techniques. Preservation, transformation and extraction. Innov Food Sci. Emerg. Technol. 41, 357–377 (2017)
Martínez, M.M., Bordón, M.G., Lallana, R.L., Ribotta, P.D., Maestri, D.M.: Optimization of sesame oil extraction by screw-pressing at low temperature. Food Bioprocess Tech. 10, 1113–1121 (2017)
Singleton, V.L., Orthofer, R., Lamuela-Raventós, R.M.: Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 299, 152–178 (1999)
Ersan, S., Ustundag, O.G., Carle, R., Schweiggert, R.F.: Identification of phenolic compounds in red and green pistachio (Pistacia vera L.) hulls (exo- and mesocarp) by HPLC-DAD-ESI-(HR)-MS. J. Agric. Food Chem. 64, 5334–5344 (2016)
Leslie, J.F., Plattner, R.D., Desjardins, A.E., Klittich, C.J.: Fumonisin B1 production by strains from different mating populations of Gibberella fujikuroi (Fusarium section Liseola). Phytopathology 82, 341–345 (1992)
Shephard, G.S., Sydenham, E.W., Thiel, P.G., Gelderblom, W.C.A.: Quantitative determination of fumonisin B1 and B2 by high-performance liquid chromatography with fluorescence detection. J. Liq. Chromatogr. 13, 2077–2087 (1990)
Dambolena, J.S., López, A.G., Canepa, M.C., Theumer, M.G., Zygadlo, J.A., Rubinstein, H.R.: Inhibitory effect of cyclic terpenes (limonene, menthol, menthone and thymol) on Fusarium verticillioides MRC 826 growth and fumonisin B1 biosynthesis. Toxicon 51, 37–44 (2008)
Sichetti Munekata, P.E., Paseto Fernandes, R.P., Pires de Melo, M., Trindade, M.A., Lorenzo, J.M.: Influence of peanut skin extract on shelf-life of sheep patties. Asian Pac. J. Trop. Med. 6, 586–596 (2016)
Sarnoski, P.J., Johnson, J.V., Reed, K.A., Tanko, J.M., O’Keefe, S.F.: Separation and characterisation of proanthocyanidins in Virginia type peanut skins by LC–MS. Food Chem. 131, 927–939 (2012)
Moazzami, A.A., Andersson, R.E., Kamal-Eldin, A.: HPLC analysis of sesaminol glucosides in sesame seeds. J. Agric. Food Chem. 54, 633–638 (2007)
Dar, A.A., Arumugam, N.: Lignans of sesame: Purification methods, biological activities and biosynthesis—a review. Bioorg. Chem. 50, 1–10 (2013)
Nadeem, M., Situ, C., Mahmud, A., Khalique, A., Imran, M., Rahman, F., Khan, S.: Antioxidant activity of sesame (Sesamum indicum L.) cake extract for the stabilization of olein based butter. J. Am. Oil Chem. Soc. 91, 967–977 (2014)
Shan, B., Cai, Y.Z., Brooks, J.D., Corke, H.: Antibacterial properties of Polygonum cuspidatum roots and their major bioactive constituents. Food Chem. 109, 530–537 (2008)
Hwang, B., Lee, J., Liu, Q., Woo, E., Lee, D.G.: Antifungal effect of (+)-pinoresinol isolated from Sambucus williamsii. Molecules 15, 3507–3516 (2010)
Céspedes, C.L., Guillermo Avila, J., García, A.M., Becerra, J., Flores, C., Aqueveque, P., Bittner, M., Hoeneisen, M., Martinez, M., Silva, M.: Antifungal and antibacterial activities of Araucaria araucana (Mol.) K. Koch heartwood lignans. Zeitschrift für Naturforschung C 61, 35–43 (2006)
Reynoso, M., Torres, A., Ramírez, M.L., Rodríguez, M., Chulze, S., Magan, N.: Efficacy of antioxidant mixtures on growth, fumonisins production and hydrolyticenzyme production by Fusarium verticillioides and F. proliferatum in vitro on maize-based media. Mycol. Res. 106, 1093–1099 (2002)
Bendaha, H., Yu, L., Touzani, R., Souane, R., Giaever, G., Nislowc, C., Boone, C., El Kadiri, S., Brownb, G.W., Bellaoui, M.: New azole antifungal agents with novel modes of action: synthesis and biological studies of new tridentate ligands based on pyrazole and triazole. Eur. J. Med. Chem. 46, 4117–4124 (2011)
Acknowledgements
Financial support was provided from CONICET, FONCYT, SECyT-UNC and MINCyT-Córdoba. We are indebted to Romina Di Paola Naranjo (ICYTAC-CONICET) and Damián Barrionuevo (IMBIV-CONICET-UNC) for their assistance in HPLC–ESI–MS/MS and HPLC–UV analyses.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bodoira, R., Velez, A., Maestri, D. et al. Bioactive Compounds Obtained from Oilseed By-Products with Subcritical Fluids: Effects on Fusarium verticillioides Growth. Waste Biomass Valor 11, 5913–5924 (2020). https://doi.org/10.1007/s12649-019-00839-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12649-019-00839-y