Elsevier

Bioorganic Chemistry

Volume 104, November 2020, 104175
Bioorganic Chemistry

Pehuén (Araucaria araucana) seed residues are a valuable source of natural antioxidants with nutraceutical, chemoprotective and metal corrosion-inhibiting properties

https://doi.org/10.1016/j.bioorg.2020.104175Get rights and content

Highlights

  • The Pehuén (Araucaria araucana) is a prehistoric tree adapted to hostile environments.

  • 97% of antioxidant power in piñón were in its coat, which is discarded as waste.

  • Piñón coat extract increases antioxidant defenses of cyclophosphamide treated rats.

  • Piñón extract inhibits more than 60% of the acid corrosion of steel.

  • The valorization of piñón waste expands possible applications in industrial fields.

Abstract

In the last decade, green chemistry has been attracting great interest in many contexts, including, among others, natural antioxidants. However, only a few works deal with natural residue extracts and biowaste, which could be an efficient, economical and environmentally friendly source for the production of useful compounds. In this study, we look for antioxidant activity in Araucaria araucana seeds, an iconic pine species of the Argentine and Chilean Patagonia commonly known as “pehuén”. Piñones are the edible pehuén seeds, and it is estimated that approximately 40 tons of piñones are harvested annually in Argentina and Chile. The chemical composition, antioxidants, metal corrosion-inhibiting properties and biological activity of edible and discarded piñón tissues were determined. Acute toxicity was discarded by in vitro testing and double fluorescent staining. Biological activity was evaluated in vivo by determining redox markers in salivary glands from rats treated with Cyclophosphamide (an oncological drug). All piñón tissues had antioxidants and antioxidant activity, with the coats showing the highest levels (up to 404 µg ascorbic acid equivalent per mg). The coats, in particular, had high gallic acid, catechin, quercetin and tannin contents, and more antioxidant activity, polyphenols and flavonoids than berries from the region. Results by X-ray fluorescence spectrometry showed that Na, Mg, P, S, Cl, K, and Ca were majority elements in the coat, embryo and endosperm. Furthermore, coat extract also showed significant anti-corrosion activity and in vivo protection against oxidative damage. The results indicate that piñón biowaste is a low-cost attractive source of natural antioxidants with potential nutraceutical, medical and metal corrosion protection applications.

Introduction

When free radicals are increased by cellular aerobic metabolism or exogenous factors, such as solar radiation, electromagnetic fields, pharmacological drugs or cigarette smoke (among others), an increase in antioxidants is required to maintain redox balance in the human body [1], [2], [3]. Otherwise, oxidative stress is promoted, causing structural and functional alterations in essential biomolecules of living organisms. Since oxidative stress plays an important role in many human diseases, the characterization of a new source of antioxidants has attracted increasing interest. In particular, vegetable sources are being intensely studied for their preventive and therapeutic uses in cancer, Parkinson's, Alzheimer's, atherosclerosis, liver injury, rheumatoid arthritis, type 2 diabetes, neurodegeneration, kidney failure and aging, and also as chemoprotective agents in cancer therapy [4], [5], [6], [7], [8]. In addition, these compounds have increased industrial applications; for example, they are used as ingredients in the formulation of dietary supplements, as reservatives for food and cosmetics, and to prevent the degradation of rubber and oil-derived compounds [9], [10]. Furthermore, many vegetable antioxidants are being investigated as green inhibitors for corrosion protection of metals and alloys [11], [12].

In the context of a circular economy, working with biological waste (biowaste) is crucial, because using such bioactive waste provides an efficient, economical and environmentally friendly source for the production of useful compounds. In this regard, high antioxidant content has been described in several species of the genus Araucaria [13], [14], [15], [16], [17], [18]. However, only a few works deal with its residue extracts and biowaste, which are usually released into the environment [19], [20], [21], [22].

In this work, we looked for antioxidant activity in the discarded coats of Araucaria araucana seeds, an iconic pine species of Patagonia. As a matter of fact, the residual coat of seeds from Araucaria angustifolia, a similar species present in southern Brazil and northern Argentina, has been described as rich in phenolic compounds and antioxidant capacity [17], [18]. Araucaria is one of the three genera that belong to the Araucariaceae family, occupying a unique position among conifers, now restricted to the South American and Southwest Asia-Western Pacific region despite their extensive distribution in both hemispheres during the Mesozoic [23], [24]. Therefore, most, if not all, of the current Araucarian taxa have evolved since the early Tertiary Period, suggesting that the success of these conifers may be governed by their ability to survive for long periods under adverse climatic conditions, such as drought, cold, fire, low fertility soil, or destructive volcanic disturbance. Perhaps for these reasons, Araucaria araucana (common name “pehuén”, Fig. 1) has been successful in the volcanic environment of the Argentine and Chilean Patagonia, with trees more than 1000 years old [23], [24], [25], [26]. Pehuén forest occupies a total area of approximately 450,000 ha, of which 263,525 ha belong to Chile and 179,289 ha to Argentina [27]. The pehuén is considered a prehistoric tree, and is protected by law in both countries. Pehuén seeds, locally called “piñones” (singular “piñón”), have been used for food and for medicinal and religious purposes since ancient times. Nowadays, piñones also have great value for gastronomic tourism in some Patagonian localities. According to published data, approximately 90 kg/ha and 273 kg/ha of piñones are harvested annually in Argentina and Chile, respectively [27], [28]. Piñón pulp (mean weight 1.8 g per piñón) consists of endosperm and embryo, and is the edible part of the seed (Fig. 1). As a by-product of food preparation, piñón coat, which weighs approximately 0.7 g, is usually discarded and takes considerable time to decompose. Whole piñones are light yellow in color, covered by an adherent membrane (thin coat) and encased in a very resistant reddish-brown coat (thick coat). Piñones are fleshy and have an ovate-oblong shape, measuring 4–5 cm in length and 1.5–2.0 cm in width, and weighing approximately 2.5 g (Fig. 1). Our previous results indicate that both the edible part of piñones and the biotechnologically obtained callus of piñón embryos show antioxidant capacity [29], [30]. Therefore, the piñón coat from A. araucana (biowaste) could be a valuable source of natural antioxidants that has not yet been explored.

Given the enormous scientific, medicinal and industrial interest surrounding natural antioxidants, the objective of this study was to analyze and compare the chemical composition and antioxidant properties of the edible and discarded parts from piñones, seeking better properties in the residues. Considering that antioxidants obtained from biowaste are environmentally and ecologically friendly, inexpensive and readily available, we advanced in the study of possible applications for piñón coat extract as a therapeutic agent and green corrosive inhibitor.

Section snippets

Chemical reagents

Dulbecco modified essential medium (DMEM), antibiotics, reagents, and standards for HPLC were purchased from Sigma-Aldrich. HPLC grade solvents were purchased from Fisher Scientific Co. Fetal bovine serum was purchased from Natocor (www.natocor.com.ar). The RANSOD kit (SD 125) for superoxide dismutase activity (SOD) determination was from RANDOX Laboratories Ltd. Malondialdehyde (MDA) Assay Kit (ab118970) to detect lipid peroxidation was from Abcam Laboratory. Uricostat enzimático AA (Cod.

Results and discussion

In order to identify the contributions of separate piñón components to the overall antioxidant activity and chemical composition, Fig. 2 summarizes the results regarding antioxidant capacity, and the phenolic and flavonoid content of the different tissues from one dried fresh seed. The most relevant result was that 97% of antioxidant power, 93% of total phenols and 75% of flavonoids of the piñón were found in the coat, which represents 27% of the seed (w/w) and is discarded as waste. Therefore,

Conclusion

The results shown here indicate that the piñón coat, which is discarded as waste (biowaste), has very high antioxidant power. Hence, residues from the piñón food industry are rich in valuable phytochemicals such as tannins, quercetin and gallic acid, as well as significant nutritional elements and other not yet identified components, which contribute to their nutritive and free radical scavenging activity. Furthermore, these properties are responsible, at least in part, for inducing a

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

This work was supported by the FONCyT (PICT 2013-0458-2014/2018), the CONICET (PIP0239-2016/2019, PUE0067-2017-2021), the National University of Comahue (PIN04/N025-2015/2019), and the Ministry of Education of Argentina (VT12-UNCOMA4094-2016/2017), SeCyT-UNC (33620180100930CB). Elemental analysis work was developed in the framework of activities of the CEX2018-000794-S project (Spanish Ministry of Science and Innovation). The authors thank Nelda B. Gaydou, CT, American Translators Association

Declaration of Interest statement

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

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