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Phenolic content, antioxidant and antifungal activity of jackfruit extracts (Artocarpus heterophyllus Lam.).

Abstract

Jackfruit (Artocarpus heterophyllus Lam.) is a fruit of tropical and subtropical zones of the world, is an important source of phytochemicals (phenolic acids, flavonoids and tannins). Several studies have associated phytochemicals with antioxidant and antimicrobial properties. The objective of this work was to analyze the polyphenolic content, the antioxidant and antifungal properties of jackfruit extracts on phytopathogenic fungi. Two phenolic extracts of jackfruit of different maturity level (J1-J2) were used. The total polyphenol content (TPC) was determined by Folin-Ciocalteu method and total flavonoids (TFC) by the aluminum chloride method, the free radical trapping potential was measured using FRAP and ORAC methods. The results showed a TPC of 844 and 1,178 mgEAG/100 g and TFC of 37 and 68 mgQE/100 g, of dry jackfruit, the antioxidant potential analysis by FRAP was 7,575 and 8,691, by ORAC was 13.369 and 14.728 µmol Trolox/100 g, of dry jackfruit for J1 and J2 respectively. Additionally, it was observed that the phenolic extracts of jackfruit reduced the mycelial growth of: Penicillium digitatum (20-14%), Geotrichum candidum (56-55%), Aspergillus niger (72-67%) and Botrytis cinerea (100%-100%) for J1 and J2 respectively. We conclude that regardless of the degree of maturity, jackfruit has antioxidant and antifungal properties on phytopathogens important in agriculture.

Keyword
s: Artocarpus heterophyllus; antifungal; antioxidant; polyphenols

1 Introduction

Artocarpus heterophyllus Lam. is a plant from the Moraceae family commonly known as jackfruit or “tree bread” in Latin America, a common name of Artocarpus genus like: Artocarpus brasiliensis Gomez., Artocarpus heterophylla Lam., Artocarpus maxima Blanco, Artocarpus philippinensis Lam., among others. Native to Southeast Asia and is widely cultivated in Malaysia and the Western Ghats of India. (Prakash et al., 2009Prakash, O., Kumar, R., Mishra, A., & Gupta, R. (2009). Artocarpus heterophyllus (Jackfruit): an overview. Pharmacognosy Reviews, 3(6), 353.; Vazhacharickal et al., 2016Vazhacharickal, P. J., Sajeshkumar, N. K., Mathew, J. J., Kuriakose, A. C., Abraham, B., Mathew, R. J., Albin, A. N., Thomson, D., Thomas, R. S., Varghese, N., & Jose, S. (2016). Chemistry and medicinal properties of jackfruit (Artocarpus heterophyllus): a review on current status of knowledge. International Journal of Innovative Research and Review, 3(2), 83-95.; Nayak et al., 2017Nayak, M., Nagarajan, A., & Majeed, M. (2017). Pharmacognostic evaluation of leaf and stem wood extracts of Artocarpus hirsutus Lam. Pharmacognosy Journal, 9(6), 887-894. http://dx.doi.org/10.5530/pj.2017.6.139.
http://dx.doi.org/10.5530/pj.2017.6.139...
). Jackfruit is not a very widespread crop in America. However, it is considered of importance in Brazil, Puerto Rico and in some Caribbean islands such as Jamaica and Bahamas, also is cultivated in southern Florida, California, and Hawaii in the United States (Crane et al., 2016Crane, J. H., Balerdi, C., & Maguire, I. (2016). Jackfruit growing in the Florida home landscape. Fact Sheet, HS-882, 1-10.). Jackfruit cultivation was introduced in Mexico in 1985 and is currently distributed in the states of Nayarit, Jalisco, Veracruz, Tabasco, and Chiapas, among others (Luna et al., 2016Luna, G., Alejo, G., Ramírez, L., & Arévalo, M. (2016). La Yaca, un fruto de exportación. Agroproductividad, 6(5), 65-70.). The fruits are compounds or aggregates with a weight of 4.5 to 27.3 kg each; some varieties produce small fruits that weigh from 1.4 to 4.5 kg. The period between flowering and fruit ripening varies between 150 and 180 days (Jagtap & Bapat, 2010Jagtap, U. B., & Bapat, V. A. (2010). Artocarpus: a review of its traditional uses, phytochemistry and pharmacology. Journal of Ethnopharmacology, 129(2), 142-166. http://dx.doi.org/10.1016/j.jep.2010.03.031. PMid:20380874.
http://dx.doi.org/10.1016/j.jep.2010.03....
). The edible part surrounds each seed and is composed of a sweet, aromatic, crisp and smooth pulp; its exotic characteristic resides in its flavors, which is a mixture of tropical fruits such as pineapple (Ananas comosus), banana (Musa paradisiaca), mango (Mangifera indica), orange (Citrus sinensis), melon (Cucumis melo) and papaya (Carica papaya) (Servicio de Información Agroalimentaria y Pesquera, 2017Servicio de Información Agroalimentaria y Pesquera – SIAP. (2017). Jackfruit, jaca, yaca… ¿la conoces? Retrieved from https://www.gob.mx/siap/articulos/jackfruit-jaca-yaca-la-conoces?idiom=es
https://www.gob.mx/siap/articulos/jackfr...
). A. heterophyllus Lam. has been shown to have a wide variety of secondary metabolites, including various types of flavonoids, carotenoids, prenylflavones, and sterols; of which stand out artocarpine, artocarpetine, norartocarpetine, morine, artonin, isocarpine, artocapesine, tannins and sapogenins (Hari et al., 2014Hari, A., Revikumar, K. G., & Divya, D. (2014). Artocarpus: a review of its phytochemistry and pharmacology. Journal of Pharma Search, 9(1), 7-12. http://dx.doi.org/10.1016/j.jep.2010.03.031.
http://dx.doi.org/10.1016/j.jep.2010.03....
; Vazhacharickal et al., 2016Vazhacharickal, P. J., Sajeshkumar, N. K., Mathew, J. J., Kuriakose, A. C., Abraham, B., Mathew, R. J., Albin, A. N., Thomson, D., Thomas, R. S., Varghese, N., & Jose, S. (2016). Chemistry and medicinal properties of jackfruit (Artocarpus heterophyllus): a review on current status of knowledge. International Journal of Innovative Research and Review, 3(2), 83-95.). In addition to the above, this species contains lectins (jacaline and jackin), which have been shown to inhibit the growth of Fusarium moniliforme and Sacharomyces cerevisiae, due to their affinity for chitin, which is a key component of the cell wall of these microorganisms, altering the synthesis and / or arrangement of chitin in the cell wall (Prakash et al., 2009Prakash, O., Kumar, R., Mishra, A., & Gupta, R. (2009). Artocarpus heterophyllus (Jackfruit): an overview. Pharmacognosy Reviews, 3(6), 353.). Isoprenyl flavones, artocarpine and artocarpesin, obtained from methanolic extracts, have also been shown to inhibit the formation of cariogenic bacteria Streptococcus mutans and plaque formation in the prevention of dental caries (Theivasanthi et al., 2011Theivasanthi, T., Venkadamanickam, G., Palanivelu, M., & Alagar, M. (2011). Nano sized powder of jackfruit seed: spectroscopic and anti-microbial investigative approach. Nano Biomedicine and Engineering, 3(4), 215-221. http://dx.doi.org/10.5101/nbe.v3i4.p215-221.
http://dx.doi.org/10.5101/nbe.v3i4.p215-...
). There is a current need in agriculture to offer new alternatives in the control of diseases caused by phytopathogens, mainly those of fungal and bacterial origin. A great variety of genera of fungi of agronomic and food importance cause losses in cultivation, post-harvest, storage, and distribution; damage can reach the fruit, stem, leaves, roots, or tubers of the plant (Andrade-Bustamante et al., 2017Andrade-Bustamante, G., García-López, A. M., Cervantes-Díaz, L., Aíl-Catzim, C. E., Borboa-Flores, J., & Rueda-Puente, E. O. (2017). Estudio del potencial biocontrolador de las plantas autóctonas de la zona árida del noroeste de México: control de fitopatógenos. Revista de la Facultad de Ciencias Agrarias, 49(1), 127-142. Retrieved from http://www.redalyc.org/articulo.oa?id=382852189011
http://www.redalyc.org/articulo.oa?id=38...
). In recent years, the use of pesticides has increased, worldwide, especially in countries with intensive production schemes; the abuse and ignorance of the side effects of these products have caused problems of environmental imbalance, human health and pest resistance (Vázquez, 2018Vázquez, U. G. (2018). Evaluación de principios activos de origen botánico para el control de hongos y algas de importancia agrícola [Tesis de licenciatura]. Universidad Autónoma Agraria Antonio Narro, Coahuila, México.). This has boosted the search for new sources of biocidal agents, friendly to the environment, among which essential oils and plant extracts with antioxidant and antimicrobial properties (Juárez-Becerra et al., 2010Juárez-Becerra, G. P., Sosa-Morales, M. E., & López-Malo, A. (2010). Hongos fitopatógenos de alta importancia económica: descripción y métodos de control. Temas selectos de Ingeniería de Alimentos, 4(2), 14-23.). The objective of this work was to evaluate the polyphenolic, antioxidant, and antimicrobial chemical composition of jackfruit extracts on phytopathogenic fungi.

2 Materials and methods

2.1 Materials

The jackfruit (A. heterophyllus Lam.) was obtained from the local market of the city of Reynosa, Tamaulipas, Mexico, during the winter period 2018-2019 (fruits specimens were chosen randomly). The samples were identified as J1 and J2, according to characteristics and sensorial and visuals (surface structure, solidity, external and internal visual color), of each fruit (Kader, 2002Kader, A. A. (2002). Postharvest technology of horticultural crops. In University of California Agriculture and Natural Resources (Ed.), Maturation and maturity indices (Vol. 3311, Chap. 6, pp. 55-62). USA: Agriculture & Natural Resources.), it stands out that J2 was the fruit with the highest degree of ripeness (see Figure 1). The samples were cleaned, and the seeds were separated from the pulp, the latter being used for extraction. The pulp was weighted and subsequently oven-dehydrated (DHG-9145A Drying Oven) at 65 °C for 72 h. The dried jackfruit pulp was pulverized and sieved on No. 40 mesh (<420 µm). The samples were stored in a dry environment until further analysis.

Figure 1
Jackfruit (a) J1, (b) J2 and cutted bulbs (c) J1 and (d) J2.

2.2 Extracts

A 1:10 (m:v) solution of dried jackfruit was prepared with a 70% (v/v) ethanol-water solution and stored in the dark for 15 days according to Barrientos et al., 2013Barrientos, L., Herrera, C. L., Montenegro, G., Ortega, X., Veloz, J., Alvear, M., Cuevas, A., Saavedra, N., & Salazar, L. A. (2013). Chemical and botanical characterization of Chilean propolis and biological activity on cariogenic bacteria Streptococcus mutans and Streptococcus sobrinus. Brazilian Journal of Microbiology, 44(2), 577-585. http://dx.doi.org/10.1590/S1517-83822013000200038. PMid:24294257.
http://dx.doi.org/10.1590/S1517-83822013...
. Subsequently, the mixture was vacuum filtered using filter paper (Munktell) grade 929ª. The mixture was concentrated with a rotary evaporator (40 ºC; 100 RPM), until obtaining one tenth of the initial volume. The phenolics extracts of jackfruit (JFE) were sterilized using a 0.22 µm pore filter (Syringe). Finally, they were stored at -18 °C until its analysis.

2.3 Determination of total phenolic content (TPC)

Total phenolic analyzes were performed on a Cytation 5 multimode microplate reader from BioTek Instruments, Inc. (Winooski, VT, USA), using 96-well polystyrene microplates. 125 µL of Folin-Ciocalteu reagent, 25 µL of diluted JFE (1: 100) and 100 µL of 7.5% Na2CO3 were added to each well (Bridi et al., 2019Bridi, R., Atala, E., Pizarro, P. N., & Montenegro, G. (2019). Honeybee pollen load: phenolic composition and antimicrobial activity and antioxidant capacity. Journal of Natural Products, 82(3), 559-565. http://dx.doi.org/10.1021/acs.jnatprod.8b00945. PMid:30839214.
http://dx.doi.org/10.1021/acs.jnatprod.8...
; Folin & Ciocalteu, 1927Folin, O., & Ciocalteu, V. (1927). On tyrosine and tryptophane determinations in proteins. The Journal of Biological Chemistry, 73(2), 627-650. http://dx.doi.org/10.1016/S0021-9258(18)84277-6.
http://dx.doi.org/10.1016/S0021-9258(18)...
). The samples were incubated for 60 min at 37 °C in the microplate reader and its absorbance was subsequently measured at 765 nm. Quantification was carried out by linear regression from a standard curve of the gallic acid (G7384-100G Sigma-Aldrich). The results were expressed as milligrams (mg) gallic acid equivalents of (GAE) per 100 g of dried jackfruit (mg GAE / 100 g of dried jackfruit).

2.4 Total flavonoid content (TFC)

In a 96-well microplate were added: 105 µL of methanol, 20 µL of diluted JFE (1:10) and 125 µL of 2% AlCl3. The mixture stood for 60 min at room temperature and subsequently absorbance at 420 nm was measured using a Cytation 5 multimode microplate reader (Bridi et al., 2019Bridi, R., Atala, E., Pizarro, P. N., & Montenegro, G. (2019). Honeybee pollen load: phenolic composition and antimicrobial activity and antioxidant capacity. Journal of Natural Products, 82(3), 559-565. http://dx.doi.org/10.1021/acs.jnatprod.8b00945. PMid:30839214.
http://dx.doi.org/10.1021/acs.jnatprod.8...
; Heimler et al., 2005Heimler, D., Vignolini, P., Dini, M. G., & Romani, A. (2005). Rapid tests to assess the antioxidant activity of Phaseolus vulgaris L. dry beans. Journal of Agricultural and Food Chemistry, 53(8), 3053-3056. http://dx.doi.org/10.1021/jf049001r. PMid:15826058.
http://dx.doi.org/10.1021/jf049001r...
). Quantification was carried out by linear regression from a standard curve using quercetin (Q4951-100G Sigma-Aldrich). Total flavonoid content was reported as mg of quercetin equivalents (QE) per 100 g of dried jackfruit (mg QE / 100 g of dried jackfruit).

2.5 Ferric reducing antioxidant potential (FRAP)

The ferric reducing power of JFE was determined according to Bridi et al., 2019. The FRAP solution was prepared daily: 10 parts of acetate buffer (0.3 M; pH 3.6), one part of TPTZ (2,4,6-Tripyridyl-S-triazine) 10 mM (Sigma), and one part of ferric chloride 20 mM. Aliquots of 270 µL of FRAP solution were blended with 30 µL of diluted JFE (1: 250). The samples were incubated for 30 min at 37 °C, and its absorbance was measured at 594 nm using a Cytation 5 multimode microplate reader. As positive controls, a solution of pure ethanol and Trolox (0- 30 μM) (Benzie & Strain, 1996Benzie, I. F., & Strain, J. J. (1996). The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Analytical Biochemistry, 239(1), 70-76. http://dx.doi.org/10.1006/abio.1996.0292. PMid:8660627.
http://dx.doi.org/10.1006/abio.1996.0292...
; Bridi et al., 2019Bridi, R., Atala, E., Pizarro, P. N., & Montenegro, G. (2019). Honeybee pollen load: phenolic composition and antimicrobial activity and antioxidant capacity. Journal of Natural Products, 82(3), 559-565. http://dx.doi.org/10.1021/acs.jnatprod.8b00945. PMid:30839214.
http://dx.doi.org/10.1021/acs.jnatprod.8...
). The results were reported as μmol Trolox equivalent per 100 g of dried jackfruit (μmol TE / 100 g of dried jackfruit).

2.6 Oxygen Radical Absorbing Capacity (ORAC)

The antioxidant capacity of JFE was determined using the ORAC-fluorescein assay (ORAC-FL) using a fluorescent microplate reader (Cytation 5), according to Bridi et al. (2019)Bridi, R., Atala, E., Pizarro, P. N., & Montenegro, G. (2019). Honeybee pollen load: phenolic composition and antimicrobial activity and antioxidant capacity. Journal of Natural Products, 82(3), 559-565. http://dx.doi.org/10.1021/acs.jnatprod.8b00945. PMid:30839214.
http://dx.doi.org/10.1021/acs.jnatprod.8...
. Fluorescein consumption was assessed by decreasing the fluorescence intensity of the sample (excitation 493 nm; emission 515 nm). AAPH (2,2'-azo-bis (2-amidino-propane) dihydrochloride) was used as peroxyl ion generator and Trolox µM as standard (0−100 µM). Results are expressed as μmol equivalent Trolox per 100 g dried jackfruit (μmol TE / 100 g dried jackfruit).

2.7 Antifungal activity

The strains of Penicillium digitatum, Aspergillus niger, Geotrichum candidum and Botrytis cinerea, from the collection of the Laboratorio de Patología Frutal of the Facultad de Agronomía e Ingeniería Forestal, Pontificia Universidad Católica de Chile, were used. The phytopathogens were activated in potato dextrose agar medium (PDA) at 20 °C ± 2 °C, with 12 h light / 12 h darkness periods for 7 days. Bioassays were performed as follows: one part of the micellar growth of the strains was used and they were resuspended in 10 mL of a solution with 0.05% Tween 80, mixing until a homogeneous solution. The solution was filtered with a sterile two-layer gauze to remove hyphae or mycelium of phytopathogens, then a count of the conidia was carried out in the Neubauer chamber until the following concentrations were obtained: P. digitatum (2 x105), A. niger (2.7 x107) G. candidum (3.2 x105) and B. cinerea (3.4 x106) conidia / mL respectively. A random design was used evaluating 4 treatments for each fungus: I) PDA medium in which J1 extract was added until reaching a concentration of 40% v/v; II) PDA medium with the addition of J2 extract until reaching a concentration of 40% v/v; III) a negative control that consisted of a PDA medium supplemented with a commercial solution based on the fungicide Iprodione (Agrospec) at 100 µL / L and IV) a positive control without inhibitors. Each treatment had 6 repetitions. Subsequently, 10 µL of conidial suspension of each strain were incorporated into each Petri dish and incubated at 20 °C ± 2 °C, with 12 h light / 12 h dark periods for 7 days. Measurements of the diameter of mycelial growth were carried out for each of the phytopathogens on days 1, 3, 5 and 7 (Cabrera & Montenegro, 2013Cabrera, C., & Montenegro, G. (2013). Pathogen control using a natural Chilean bee pollen extract of known botanical origin. Ciencia e Investigación Agraria, 40(1), 223-230. http://dx.doi.org/10.4067/S0718-16202013000100020.
http://dx.doi.org/10.4067/S0718-16202013...
).

2.8 Statistical data analysis

All experiments were carried out in triplicate twice (n=6). All data are the mean ± standard deviation (S.D.). All data were analyzed using the Student’s t-Test and the analysis of variance (One-way ANOVA) and comparisons using the Tukey Test, employing the Origin Pro 8 statistical program (SRO v8. 0724 B724, Massachusetts, USA).

3 Results and discussion

3.1 Determination of total phenolic content (TPC)

The TPC concentration in JFE are shown in Table 1. The J2 extract had a concentration of 1,178 mg EAG per 100 g of dried jackfruit, this value was 28% higher than the J1 extract (p = 0.0475). There are variations of the TPC reported in studies of A. heterophyllus: Jagtap & Bapat (2010)Jagtap, U. B., & Bapat, V. A. (2010). Artocarpus: a review of its traditional uses, phytochemistry and pharmacology. Journal of Ethnopharmacology, 129(2), 142-166. http://dx.doi.org/10.1016/j.jep.2010.03.031. PMid:20380874.
http://dx.doi.org/10.1016/j.jep.2010.03....
mentioned for jackfruit pulp from West Ghats, India, a concentration of 46 mg EAG / 100 g dried jackfruit in ethanolic extracts. Shafiq et al. (2017)Shafiq, M., Mehmood, S., Yasmin, A., Khan, S. J., Khan, N. H., & Ali, S. (2017). Evaluation of phytochemical, nutritional and antioxidant activity of indigenously grown jackfruit (Artocarpus heterophyllus Lam). Journal of Scientific Research, 9(1), 135-143. http://dx.doi.org/10.3329/jsr.v1i1.29665.
http://dx.doi.org/10.3329/jsr.v1i1.29665...
evaluated TPC in jackfruit pulp from Lahore, Pakistan and found 239.87 mg EAG / 100 g of dried jackfruit, in methanolic extracts, which represents 20% of amount quantified in this study. Jalal et al. (2015)Jalal, T. K., Ahmed, I. A., Mikail, M., Momand, L., Draman, S., Isa, M. L., Abdull Rasad, M. S., Nor Omar, M., Ibrahim, M., & Abdul Wahab, R. (2015). Evaluation of antioxidant, total phenol and flavonoid content and antimicrobial activities of Artocarpus altilis (breadfruit) of underutilized tropical fruit extracts. Applied Biochemistry and Biotechnology, 175(7), 3231-3243. http://dx.doi.org/10.1007/s12010-015-1499-0. PMid:25649443.
http://dx.doi.org/10.1007/s12010-015-149...
, reported results of the analysis of Artocarpus altilis from Kuantan, Malaysia, in which methanolic extractions were performed and found 78,100 mg EAG / 100 g of dried jackfruit. In 2011 Almeida et al. (2011)Almeida, M. M. B., de Sousa, P. H. M., Arriaga, Â. M. C., do Prado, G. M., Magalhães, C. E. C., Maia, G. A., & de Lemos, T. L. G. (2011). Bioactive compounds and antioxidant activity of fresh exotic fruits from northeastern Brazil. Food Research International, 44(7), 2155-2159. http://dx.doi.org/10.1016/j.foodres.2011.03.051.
http://dx.doi.org/10.1016/j.foodres.2011...
report a 29.0 mg EAG per 100 g of fresh weight Artocarpus integrifolia. These differences are closely related to the complex nature of polyphenols, their extraction method, as well as intrinsic factors (genus, species, or cultivar) and extrinsic (agronomic, environmental or storage) (Kalt et al., 2001Kalt, W., Ryan, D. A., Duy, J. C., Prior, R. L., Ehlenfeldt, M. K., & Vander Kloet, S. P. (2001). Interspecific variation in anthocyanins, phenolics, and antioxidant capacity among genotypes of highbush and lowbush blueberries (Vaccinium section cyanococcus spp.). Journal of Agricultural and Food Chemistry, 49(10), 4761-4767. http://dx.doi.org/10.1021/jf010653e. PMid:11600018.
http://dx.doi.org/10.1021/jf010653e...
; Tomás‐Barberán & Espín, 2001Tomás‐Barberán, F. A., & Espín, J. C. (2001). Phenolic compounds and related enzymes as determinants of quality in fruits and vegetables. Journal of the Science of Food and Agriculture, 81(9), 853-876. http://dx.doi.org/10.1002/jsfa.885.
http://dx.doi.org/10.1002/jsfa.885...
). The phenolics compounds in fruits are diverse and abundant group of metabolites such as phenolic acids, flavonoids, or tannins. They have responsible of color and flavor characteristics and are related to antioxidant and antiradical activities. However its content decreases during maturity stages (Redondo et al., 2021Redondo, D., Gimeno, D., Calvo, H., Venturini, M. E., Oria, R., & Arias, E. (2021). Antioxidant activity and phenol content in different tissues of stone fruits at thinning and at commercial maturity stages. Waste and Biomass Valorization, 12(4), 1861-1875. http://dx.doi.org/10.1007/s12649-020-01133-y.
http://dx.doi.org/10.1007/s12649-020-011...
). The decrease in phenolic content in fruits is attributed to a series of chemical and enzymatic alterations of some polyphenols during ripening, mainly hydrolysis of glycosides by glycosidase, oxidation of polyphenols by phenoloxidases and polymerization of free phenols (Zheng et al., 2012Zheng, H. Z., Kim, Y. I., & Chung, S. K. (2012). A profile of physicochemical and antioxidant changes during fruit growth for the utilisation of unripe apples. Food Chemistry, 131(1), 106-110. http://dx.doi.org/10.1016/j.foodchem.2011.08.038.
http://dx.doi.org/10.1016/j.foodchem.201...
). The results obtained in this study have a similar tendency to that reported in studies related to alcoholic extractions. Due to the polarity of primary alcohols (mainly methanol and ethanol), they are excellent as solvents for phytochemicals, especially those with high polarity (Zhang et al., 2007Zhang, Z. S., Li, D., Wang, L. J., Ozkan, N., Chen, X. D., Mao, Z. H., & Yang, H. Z. (2007). Optimization of ethanol–water extraction of lignans from flaxseed. Separation and Purification Technology, 57(1), 17-24. http://dx.doi.org/10.1016/j.seppur.2007.03.006.
http://dx.doi.org/10.1016/j.seppur.2007....
). Similar studies have been reported in tropical fruits, the total phenolic content in pineapple (Ananas comosus L.) fluctuate between 38.1 and 67.2 mg of GAE / 100 g fresh weight, in plum (Spondias purpurea L.) 55.0 mg of GAE / 100 g fresh weight, soursop (Annona muricata L.) 54.8 to 120 mg GAE / 100 g, papaya (Carica papaya L.) 53.2 mg of GAE / 100 g fresh weight (Almeida et al., 2011Almeida, M. M. B., de Sousa, P. H. M., Arriaga, Â. M. C., do Prado, G. M., Magalhães, C. E. C., Maia, G. A., & de Lemos, T. L. G. (2011). Bioactive compounds and antioxidant activity of fresh exotic fruits from northeastern Brazil. Food Research International, 44(7), 2155-2159. http://dx.doi.org/10.1016/j.foodres.2011.03.051.
http://dx.doi.org/10.1016/j.foodres.2011...
; Hassimotto et al., 2005Hassimotto, N. M. A., Genovese, M. I., & Lajolo, F. M. (2005). Antioxidant activity of dietary fruits, vegetables, and commercial frozen fruit pulps. Journal of Agricultural and Food Chemistry, 53(8), 2928-2935. http://dx.doi.org/10.1021/jf047894h. PMid:15826041.
http://dx.doi.org/10.1021/jf047894h...
) and sapota fruit (Achras sapota Linn.) 134.6 mg GAE / 100 g (Kulkarni et al., 2007Kulkarni, A. P., Policegoudra, R. S., & Aradhya, S. M. (2007). Chemical composition and antioxidant activity of sapota (Achras sapota Linn.) fruit. Journal of Food Biochemistry, 31(3), 399-414. http://dx.doi.org/10.1111/j.1745-4514.2007.00122.x.
http://dx.doi.org/10.1111/j.1745-4514.20...
).

Table 1
Total phenol content (TPC), total flavonoid (TFC) and antioxidant activity by ORAC and FRAP of jackfruit.

3.2 Determination of total flavonoids content (TFC)

Flavonoids are a family of polyphenols, content in fruits and vegetables. They are the main components of fruits with yellow, red, and blue colors (Erlund, 2004Erlund, I. (2004). Review of the flavonoids quercetin, hesperetin, and naringenin. Dietary sources, bioactivities, bioavailability, and epidemiology. Nutrition Research (New York, N.Y.), 24(10), 851-874. http://dx.doi.org/10.1016/j.nutres.2004.07.005.
http://dx.doi.org/10.1016/j.nutres.2004....
; Hýsková & Ryšlavá, 2019Hýsková, V., & Ryšlavá, H. (2019). Antioxidant properties of phenylpropanoids. Biochemistry and Analytical Biochemistry, 8, e171. http://dx.doi.org/10.35248/2161-1009.19.8.e171.
http://dx.doi.org/10.35248/2161-1009.19....
). The concentration of total flavonoids determined in JFE is shown in Table 1; where it was observed that J2 had the highest content with 68 mg QE / 100 g of dried jackfruit, this value was 45% higher with respect to J1 (p = 0.0472). The difference between J1 and J2 is their degree of maturation. Jagtap & Bapat (2010)Jagtap, U. B., & Bapat, V. A. (2010). Artocarpus: a review of its traditional uses, phytochemistry and pharmacology. Journal of Ethnopharmacology, 129(2), 142-166. http://dx.doi.org/10.1016/j.jep.2010.03.031. PMid:20380874.
http://dx.doi.org/10.1016/j.jep.2010.03....
reported high solubility of flavonoids in methanolic extracts of mature jackfruit. Some studies relate the degree of maturation with the increase in the concentration of polyphenolic compounds such as flavonoids in fruits such as: watermelon cultivars (Tlili et al., 2011Tlili, I., Hdider, C., Lenucci, M. S., Ilahy, R., Jebari, H., & Dalessandro, G. (2011). Bioactive compounds and antioxidant activities during fruit ripening of watermelon cultivars. Journal of Food Composition and Analysis, 24(7), 923-928. http://dx.doi.org/10.1016/j.jfca.2011.03.016.
http://dx.doi.org/10.1016/j.jfca.2011.03...
), custard apple (Harris & Brannan, 2009Harris, G. G., & Brannan, R. G. (2009). A preliminary evaluation of antioxidant compounds, reducing potential, and radical scavenging of pawpaw (Asimina tribloba) fruit pulp from different stages of ripeness. Lebensmittel-Wissenschaft + Technologie, 42(1), 275-279. http://dx.doi.org/10.1016/j.lwt.2008.05.006.
http://dx.doi.org/10.1016/j.lwt.2008.05....
) and jackfruit (Jagtap & Bapat, 2010Jagtap, U. B., & Bapat, V. A. (2010). Artocarpus: a review of its traditional uses, phytochemistry and pharmacology. Journal of Ethnopharmacology, 129(2), 142-166. http://dx.doi.org/10.1016/j.jep.2010.03.031. PMid:20380874.
http://dx.doi.org/10.1016/j.jep.2010.03....
). The polyphenolic compounds reported in jackfruit include phenolic acids such as gallic acid, ferulic acid and tannic acid and flavonoids mainly catechin, rutin and myricetin. (Singh et al., 2015Singh, A., Maurya, S., Singh, M., & Singh, U. P. (2015). Studies on the phenolic acid contents in different parts of raw and ripe jackfruit and their importance in human health. International Journal of Applied Science-Research and Review, 2(2), 69-73. Retrieved from http://www.imedpub.com/articles/studies-on-the-phenolic-acid-contents-in-different-parts-ofraw-and-ripe-jackfruit-and-their-importance-in-humanhealth.pdf
http://www.imedpub.com/articles/studies-...
; Sharma et al., 2015Sharma, A., Gupta, P., & Verma, A. K. (2015). Preliminary nutritional and biological potential of Artocarpus heterophyllus L. shell powder. Journal of Food Science and Technology, 52(3), 1339-1349. http://dx.doi.org/10.1007/s13197-013-1130-8. PMid:25745202.
http://dx.doi.org/10.1007/s13197-013-113...
; Anaya-Esparza et al., 2018Anaya-Esparza, L. M., González-Aguilar, G. A., Domínguez-Ávila, J. A., Olmos-Cornejo, J. E., Pérez-Larios, A., & Montalvo-González, E. (2018). Effects of minimal processing technologies on jackfruit (Artocarpus heterophyllus Lam.) quality parameters. Food and Bioprocess Technology, 11(9), 1761-1774. http://dx.doi.org/10.1007/s11947-018-2136-z.
http://dx.doi.org/10.1007/s11947-018-213...
).

3.3 Antioxidant potential using FRAP assay

The antioxidant potential determined by the FRAP method showed a difference of 12% between J1 (7,575 μmol Trolox / 100 g dry weight) and J2 (8,691 μmol Trolox / 100 g dry weight), finding significant statistical differences between both extracts (p = 0.0079). Loizzo et al. (2010)Loizzo, M. R., Tundis, R., Chandrika, U. G., Abeysekera, A. M., Menichini, F., & Frega, N. G. (2010). Antioxidant and antibacterial activities on foodborne pathogens of Artocarpus heterophyllus Lam. (Moraceae) leaves extracts. Journal of Food Science, 75(5), M291-M295. http://dx.doi.org/10.1111/j.1750-3841.2010.01614.x. PMid:20629886.
http://dx.doi.org/10.1111/j.1750-3841.20...
reported the analysis of extracts of A. heterophyllus Lam. in relation to the reduction of the antioxidant ability when reacting with the ferric tripyridyltriazine complex (Fe3+ -TPTZ) and producing ferrous tripyridyltriazine (Fe2+ -TPTZ). The reducing ability of JFE is strongly related to the presence and concentration of polyphenolic compounds (Jagtap & Bapat, 2010Jagtap, U. B., & Bapat, V. A. (2010). Artocarpus: a review of its traditional uses, phytochemistry and pharmacology. Journal of Ethnopharmacology, 129(2), 142-166. http://dx.doi.org/10.1016/j.jep.2010.03.031. PMid:20380874.
http://dx.doi.org/10.1016/j.jep.2010.03....
). This chemical behavior is similar to the observed in this study. On the other hand, the redox properties that polyphenols can have (reducing agents, donors of hydrogens or oxygen reactants through processes such as excitation reactions, energy transfer, complex formation and collisional quenching) must be considered (Soong & Barlow, 2004Soong, Y. Y., & Barlow, P. J. (2004). Antioxidant activity and phenolic content of selected fruit seeds. Food Chemistry, 88(3), 411-417. http://dx.doi.org/10.1016/j.foodchem.2004.02.003.
http://dx.doi.org/10.1016/j.foodchem.200...
). The redox potential of polyphenols plays a crucial role in determining antioxidant properties (Rice-Evans et al., 1997Rice-Evans, C., Miller, N., & Paganga, G. (1997). Antioxidant properties of phenolic compounds. Trends in Plant Science, 2(4), 152-159. http://dx.doi.org/10.1016/S1360-1385(97)01018-2.
http://dx.doi.org/10.1016/S1360-1385(97)...
).

3.4 Antioxidant ORAC assay

The antioxidant potential using the ORAC method proved a 4% superiority of J1 (13,369 μmol Trolox / 100 g dry weight) in comparison to J2 (14, 728.81 μmol Trolox / 100 g dry weight); however, there were no significant statistical differences (Table 1). Pavan et al. (2014)Pavan, V., Sancho, R. A. S., & Pastore, G. M. (2014). The effect of in vitro digestion on the antioxidant activity of fruit extracts (Carica papaya, Artocarpus heterophillus and Annona marcgravii). Lebensmittel-Wissenschaft + Technologie, 59(2), 1247-1251. http://dx.doi.org/10.1016/j.lwt.2014.05.040.
http://dx.doi.org/10.1016/j.lwt.2014.05....
reported values of 2,117 μmol Trolox for 100 g of dried jackfruit, approximately 15% of the concentration determined in this study. Phytochemical studies on jackfruit have reported the content of polyphenolic compounds and their antioxidant activity (Baliga et al., 2011Baliga, M. S., Shivashankara, A. R., Haniadka, R., Dsouza, J., & Bhat, H. P. (2011). Phytochemistry, nutritional and pharmacological properties of Artocarpus heterophyllus Lam (jackfruit): a review. Food Research International, 44(7), 1800-1811. http://dx.doi.org/10.1016/j.foodres.2011.02.035.
http://dx.doi.org/10.1016/j.foodres.2011...
; Saha et al., 2015Saha, R. K., Jamiruddin, M., & Acharya, S. (2015). Comparative analysis of lectins isolated from seed and testa of Artocarpus heterophyllus Lam. International Journal of Current Research in Chemistry and Pharmaceutical Sciences, 2(1), 65-75. Retrieved from http://ijcrcps.com/pdfcopy/jan2015/ijcrcps9.pdf
http://ijcrcps.com/pdfcopy/jan2015/ijcrc...
). The differences in antioxidant capacity are directly related to the phytochemicals contained in the fruit, mainly those having functional groups such as hydroxyl (-OH) and that abound in compounds of the polyphenolic type such as: phenolic acids (gallic acid, ferulic acid and tannic acid), flavonoids (catechin, rutin and myricetin) and/or tannins (condensed/hydrolysable) mainly (González-Aguilar et al., 2008González-Aguilar, G., Robles-Sánchez, R. M., Martínez-Téllez, M. A., Olivas, G. I., Álvarez-Parrilla, E., & De La Rosa, L. A. (2008). Bioactive compounds in fruits: health benefits and effect of storage conditions. Stewart Postharvest Review, 4(3), 1-10. http://dx.doi.org/10.2212/spr.2008.3.8.
http://dx.doi.org/10.2212/spr.2008.3.8...
; Singh et al., 2015Singh, A., Maurya, S., Singh, M., & Singh, U. P. (2015). Studies on the phenolic acid contents in different parts of raw and ripe jackfruit and their importance in human health. International Journal of Applied Science-Research and Review, 2(2), 69-73. Retrieved from http://www.imedpub.com/articles/studies-on-the-phenolic-acid-contents-in-different-parts-ofraw-and-ripe-jackfruit-and-their-importance-in-humanhealth.pdf
http://www.imedpub.com/articles/studies-...
; Sharma et al., 2015Sharma, A., Gupta, P., & Verma, A. K. (2015). Preliminary nutritional and biological potential of Artocarpus heterophyllus L. shell powder. Journal of Food Science and Technology, 52(3), 1339-1349. http://dx.doi.org/10.1007/s13197-013-1130-8. PMid:25745202.
http://dx.doi.org/10.1007/s13197-013-113...
; Anaya-Esparza et al., 2018Anaya-Esparza, L. M., González-Aguilar, G. A., Domínguez-Ávila, J. A., Olmos-Cornejo, J. E., Pérez-Larios, A., & Montalvo-González, E. (2018). Effects of minimal processing technologies on jackfruit (Artocarpus heterophyllus Lam.) quality parameters. Food and Bioprocess Technology, 11(9), 1761-1774. http://dx.doi.org/10.1007/s11947-018-2136-z.
http://dx.doi.org/10.1007/s11947-018-213...
).

3.5 Antifungal activity of the extracts

The inhibitory effect of extracts J1 and J2 did not show significant differences (p ≥ 0.05), which can be attributed to the fact that the component with antifungal activity is present in both extracts. The mycelial growth of the phytopathogens decreased: P. digitatum (20% vs. 14%), G. candidum (56% vs. 55%), A. niger (72% vs. 67%) and B. cinerea (100% vs. 100%) for J1 and J2 respectively (Table 2). This suggests that the ripe jackfruit, which is no longer pleasant to the consumer, can be used to obtain extracts with an antifungal effect. Manikandan et al. (2017)Manikandan, V., Yi, P. I., Velmurugan, P., Jayanthi, P., Hong, S. C., Jang, S. H., Su, J. M., & Sivakumar, S. (2017). Production, optimization and characterization of silver oxide nanoparticles using Artocarpus heterophyllus rind extract and their antifungal activity. African Journal of Biotechnology, 16(36), 1819-1825. http://dx.doi.org/10.5897/AJB2017.15967.
http://dx.doi.org/10.5897/AJB2017.15967...
reported the studies of the development of silver nanoparticles with extracts of A. heterophyllus Lam. against phytopathogens and demonstrated to be superior to the control and reference agents, similar behavior to that reported in this work. On the other hand, Tao et al. (2010)Tao, S., Zhang, S., Tsao, R., Charles, M. T., Yang, R., & Khanizadeh, S. (2010). In vitro antifungal activity and mode of action of selected polyphenolic antioxidants on Botrytis cinerea. Archiv für Phytopathologie und Pflanzenschutz, 43(16), 1564-1578. http://dx.doi.org/10.1080/03235400802583834.
http://dx.doi.org/10.1080/03235400802583...
reported the antifungal activity of polyphenols (gallic acid, catechin and quercetin 3-galactoside) at different concentrations at each stage of development of B. cinerea and demonstrated the inhibitory effect at each phase of growth of the pathogen. This indicates that the different compounds have effects on the sensitivity of fungi that can change at different stages of development as well as by various antifungal mechanisms such as the ability to inhibit the germination of fungal spores or effects on deformation and cellular lysis (Pusztahelyi et al., 2015Pusztahelyi, T., Holb, I. J., & Pócsi, I. (2015). Secondary metabolites in fungus-plant interactions. Frontiers in Plant Science, 6, 573. http://dx.doi.org/10.3389/fpls.2015.00573. PMid:26300892.
http://dx.doi.org/10.3389/fpls.2015.0057...
). Phenolic compounds are related to defense response in plants against pathogen attack (Pusztahelyi et al., 2015Pusztahelyi, T., Holb, I. J., & Pócsi, I. (2015). Secondary metabolites in fungus-plant interactions. Frontiers in Plant Science, 6, 573. http://dx.doi.org/10.3389/fpls.2015.00573. PMid:26300892.
http://dx.doi.org/10.3389/fpls.2015.0057...
; Joaquín-Ramos et al., 2020Joaquín-Ramos, A. D. J., López-Palestina, C. U., Pinedo-Espinoza, J. M., Altamirano-Romo, S. E., Santiago-Saenz, Y. O., Aguirre-Mancilla, C. L., & Gutiérrez-Tlahque, J. (2020). Phenolic compounds, antioxidant properties and antifungal activity of jarilla (Barkleyanthus salicifolius ENT# 91; KunthENT# 93; H. Rob & Brettell). Chilean Journal of Agricultural Research, 80(3), 352-360. http://dx.doi.org/10.4067/S0718-58392020000300352.
http://dx.doi.org/10.4067/S0718-58392020...
). Some small chemical structure phenolic compounds such as phenolic acids alter the fungal membranes and adhere and polymerize within the wall of the fungal hyphae, thus reducing the plasticity of the fungus for growth (Wang et al., 2008Wang, S. Y., Maas, J. L., Payne, J. A., & Galletta, G. J. (2008). Ellagic acid content in small fruits, mayhaws, and other plants. Journal of Small Fruit & Viticulture, 2(4), 39-49. http://dx.doi.org/10.1300/J065v02n04_03.
http://dx.doi.org/10.1300/J065v02n04_03...
).

Table 2
% Mycelial growth inhibition of P. digitatum, G. candidum, A. niger and B. cinerea by jackfruit.

4 Conclusions

In this study, the jackfruit (A. heterophyllus Lam.) extracts were found to have a high content of polyphenols like flavonoids, and these compounds are related to strong antioxidant capacity. The results showed that, regardless of the degree of maturation, jackfruit has antioxidant phytochemicals with potential antifungal effects on fungi of importance in agriculture. This suggests that ripe jackfruit, which is no longer consumer-friendly, can be harnessed for the formulation of environmentally friendly biofungicides. The jackfruit is a very generous supplier of phenolic compounds and this might be an added value to be considered to develop subproducts with benefits in agriculture.

  • Practical Application: Jackfruit extracts have properties as a protective agent against phytopathogens in agriculture.

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Publication Dates

  • Publication in this collection
    28 June 2021
  • Date of issue
    2022

History

  • Received
    18 Jan 2021
  • Accepted
    10 May 2021
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