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Total phenolics, resveratrol content and antioxidant activity of seeds and calluses of pinto peanut (Arachis pintoi Krapov. & W.C. Greg.)

Authors:
Isabela Brandão de Sousa-Machado at Rio de Janeiro State University
Isabela Brandão de Sousa-Machado
Tayanne Felippe
Tayanne Felippe
Tayanne Felippe
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R.O. Garcia at Rio de Janeiro State University
R.O. Garcia
Georgia Pacheco at Rio de Janeiro State University
Georgia Pacheco
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Abstract and Figures

Arachis pintoi is a peanut species native to Brazil, which is cultivated in many countries for animal forage, soil cover, landscaping, and recovery of degraded areas. Tissue culture studies for this species have been focused in plant production, whereas works on in vitro secondary metabolites production are scarce. The goal of the present work was to establish callus cultures from different seed explants of A. pintoi, aiming at evaluating the potential for metabolites production and antioxidant activity. Embryonic axes, leaflets, and cotyledons were cultured on solidified MS medium supplemented with picloram (PIC), 2,4-dichlorophenoxyacetic acid (2,4-D), thidiazuron (TDZ) or different combinations of 6-benzyladenine (BA) and α-naphthaleneacetic acid (NAA), under light or dark conditions. Friable calluses with a high biomass (4.3 ± 0.3 g FW per callus) were obtained from embryonic leaflets cultured on medium supplemented with 17.6 µM BA plus 5.4 µM NAA, in the dark. Cotyledons and embryonic axes cultured in the presence of 4.4 µM BA combined with 10.8 µM NAA formed heterogeneous calluses with a compact base and a large friable surface. Trans-resveratrol and other stilbenes that were not found in seeds were detected in callus extracts, especially those originated from cotyledons, although these materials showed lower total phenolic contents (TPC) when compared with seeds with and without testa, as well as cotyledons. Extracts from seeds with testa and from calluses derived from cotyledons and embryonic axes showed the highest EC50 in DPPH assays. No correlation between TPC, trans-resveratrol and antioxidant activity was observed.
Callus formation from A. pintoi seed explants cultured on MS medium supplemented with different growth regulators for 60 days, in the presence or absence of light. a Heterogeneous callus obtained from cotyledons cultured on medium containing 22.6 µM 2,4-D, in the presence of light, b Mucilaginous callus obtained from cotyledons in response to 12.4 µM PIC, in the dark, c compact organogenic callus derived from embryonic axes cultured in the presence of 4.5 µM TDZ, in the presence of light, d heterogeneous organogenic callus derived from embryonic axes in response to 13.2 µM BA and 2.7 µM NAA, in the presence of light, e heterogeneous callus derived from embryonic axes in response to 4.4 µM BA and 10.8 µM NAA, in the absence of light, f Friable callus obtained from immature leaflets cultured on medium supplemented with 17.6 µM BA and 5.4 µM NAA, and maintained in the dark. Bars = 1 cm
Callus formation from A. pintoi seed explants cultured on MS medium supplemented with different growth regulators for 60 days, in the presence or absence of light. a Heterogeneous callus obtained from cotyledons cultured on medium containing 22.6 µM 2,4-D, in the presence of light, b Mucilaginous callus obtained from cotyledons in response to 12.4 µM PIC, in the dark, c compact organogenic callus derived from embryonic axes cultured in the presence of 4.5 µM TDZ, in the presence of light, d heterogeneous organogenic callus derived from embryonic axes in response to 13.2 µM BA and 2.7 µM NAA, in the presence of light, e heterogeneous callus derived from embryonic axes in response to 4.4 µM BA and 10.8 µM NAA, in the absence of light, f Friable callus obtained from immature leaflets cultured on medium supplemented with 17.6 µM BA and 5.4 µM NAA, and maintained in the dark. Bars = 1 cm
… 
Biomass accumulation (g) of A. pintoi calluses obtained in response to MS medium supplemented with combinations of BA and NAA, after 60 days in the dark. a Cotyledons, b embryonic axes and c immature leaflets. Different letters within graphs indicate statistically significant differences in the fresh weight (lower case) or dry weight (upper case) values (Tukey test, p ≤ 0.05)
Biomass accumulation (g) of A. pintoi calluses obtained in response to MS medium supplemented with combinations of BA and NAA, after 60 days in the dark. a Cotyledons, b embryonic axes and c immature leaflets. Different letters within graphs indicate statistically significant differences in the fresh weight (lower case) or dry weight (upper case) values (Tukey test, p ≤ 0.05)
… 
Chromatogram of extract from cotyledon calluses (total run time = 11 min) with expansion of the trans-resveratrol peak (tR = 8.4 min): a sample, b standard
Chromatogram of extract from cotyledon calluses (total run time = 11 min) with expansion of the trans-resveratrol peak (tR = 8.4 min): a sample, b standard
… 
Chromatograms (total run time = 90 min, λmáx = 306 nm) of extracts from a calluses derived from cotyledons and b seeds with testa
Chromatograms (total run time = 90 min, λmáx = 306 nm) of extracts from a calluses derived from cotyledons and b seeds with testa
… 
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Plant Cell, Tissue and Organ Culture (PCTOC) (2018) 134:491–502
https://doi.org/10.1007/s11240-018-1438-1
ORIGINAL ARTICLE
Total phenolics, resveratrol content andantioxidant activity ofseeds
andcalluses ofpinto peanut (Arachis pintoi Krapov. & W.C. Greg.)
IsabelaBrandãodeSousa‑Machado1· TayanneFelippe1· RenataGarcia1· GeorgiaPacheco1· DavysonMoreira2·
ElisabethMansur1
Received: 19 October 2017 / Accepted: 3 June 2018 / Published online: 26 June 2018
© Springer Nature B.V. 2018
Abstract
Arachis pintoi is a peanut species native to Brazil, which is cultivated in many countries for animal forage, soil cover,
landscaping, and recovery of degraded areas. Tissue culture studies for this species have been focused in plant production,
whereas works on invitro secondary metabolites production are scarce. The goal of the present work was to establish callus
cultures from different seed explants of A. pintoi, aiming at evaluating the potential for metabolites production and antioxi-
dant activity. Embryonic axes, leaflets, and cotyledons were cultured on solidified MS medium supplemented with picloram
(PIC), 2,4-dichlorophenoxyacetic acid (2,4-D), thidiazuron (TDZ) or different combinations of 6-benzyladenine (BA) and
α-naphthaleneacetic acid (NAA), under light or dark conditions. Friable calluses with a high biomass (4.3 ± 0.3gFW per
callus) were obtained from embryonic leaflets cultured on medium supplemented with 17.6µM BA plus 5.4µM NAA, in
the dark. Cotyledons and embryonic axes cultured in the presence of 4.4µM BA combined with 10.8µM NAA formed
heterogeneous calluses with a compact base and a large friable surface. Trans-resveratrol and other stilbenes that were not
found in seeds were detected in callus extracts, especially those originated from cotyledons, although these materials showed
lower total phenolic contents (TPC) when compared with seeds with and without testa, as well as cotyledons. Extracts from
seeds with testa and from calluses derived from cotyledons and embryonic axes showed the highest EC50 in DPPH assays.
No correlation between TPC,trans-resveratrol and antioxidant activity was observed.
Keywords Phytoalexin· Stilbenoids· Auxin· Cytokinin· Seed explants· Callogenesis
Introduction
The genus Arachis L. (Fabaceae) is native to South America,
with 81 described species (Krapovickas and Gregory 1994;
Santana and Valls 2015), and Brazil is considered a major
genetic diversity center. The most economically important
species of the genus, groundnut (A. hypogaea L.), is the
fourth oilseed crop around the world, producing seeds with
high nutritional value (Silva etal. 2010), whereas some other
species have gained agronomic importance more recently.
Among these species, pinto peanut (Arachis pintoi
Krapov. & W.C. Gregory) is increasingly valued as for-
age due to its characteristics of perennial crowns, ability to
spread via stolons, high digestibility and nutritional value
(Ladeira etal. 2002), adaptability to different types of soil,
shading tolerance, cold tolerance, and good fire resistance
(Bresolin etal. 2008; Adjolohoun etal. 2013). Several stud-
ies demonstrated an increased efficiency of animal produc-
tion per hectare of pasture when using A. pintoi, which ulti-
mately reduces the need of deforestation of new areas for
this purpose. This species is also used for soil cover, as orna-
mental, and for the recovery of degraded areas (Carvalho
and Quesenberry 2009). In the last 30years, several A. pintoi
cultivars were released around the world, mainly in Australia
and Latin America. In Brazil, at least four cultivars were
Communicated by Sergio J. Ochatt.
* Isabela Brandão de Sousa-Machado
bela_biouerj@hotmail.com
Elisabeth Mansur
elisabeth.mansur@gmail.com
1 Instituto de Biologia Roberto Alcantara Gomes, Núcleo de
Biotecnologia Vegetal, Rua São Francisco Xavier 524 PHLC
sala 505, Maracanã, Universidade doEstado doRio de
Janeiro, RiodeJaneiro20550-013, Brazil
2 Instituto de Tecnologia em Fármacos, Fundação Oswaldo
Cruz, AvenidaBrasil4036,Maré, RiodeJaneiro21040-361,
Brazil
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Arachis pintoi, commonly known as pinto or forage peanuts, have garnered significant attention in recent years due to their diverse applications in agriculture and landscaping. This perennial legume plant originates from Brazil and had been successfully introduced to various tropical and subtropical regions worldwide (Azêvedo et al., 2016;de Sousa-Machado et al., 2018). Its adaptability to various soil types and climatic conditions makes it a valuable species for improving soil health and enhancing aesthetic value in landscapes. ...
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Pinto peanuts are known as versatile cover crops for soil conservation, biomulch, and ornamental plants. These plants rarely produce seeds, so they are commonly propagated vegetatively, resulting in low efficiency of seedling production and availability of cuttings. The aim of this study was to determine the effect of cutting age and auxin application on the growth of pinto peanut. This experiment used a complete randomized block factorial design. The first factor was the age of the cuttings (stolons) with three levels (young, intermediate, old). Each cutting had three nodes, with young cuttings measured from the tip, intermediate cuttings measured from the fourth node, and old cuttings measured from the seventh node. The second factor was the concentration of the commercial auxin product ROOTONE F (0 ppm, 500 ppm, 1000 ppm, 1500 ppm, 2000 ppm). The results showed that the difference in cutting age significantly affected the number of leaves (at 10 and 50 days after planting), plant length (at 10 to 50 days after planting), number of branches (at 30 to 50 days after planting), and canopy area. Differences in auxin concentration only significantly affected plant length from 10 to 30 days after planting. The interaction between cutting age and auxin concentration was significant only for the number of leaves at 10 to 20 days after planting and plant length at 50 days after planting. The highest values for the observed parameters were consistently obtained by intermediate cuttings, which are therefore recommended as planting material for ornamental peanut cuttings.
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... Young leaf tissue for callus induction have a higher regeneration rate. In addition to leaf tissues, embryos, cotyledonary nodes, and stem nodules can also be used to induce callus in wild peanuts (Gagliardi et al. 2002;de Sousa-Machado et al. 2018). ...
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... s −1 m −2 . Previous reports in plant cell, tissue and organ cultures also indicated that dark treatments caused an increase in cell biomass (Zhang et al. 2002;Andi et al. 2018;de Sousa-Machado et al. 2018). As previously reported by Andi et al. (2019), there were significant positive and negative correlations between fresh cell weight with medium pH and electrical conductivity values in the same cell cultures, respectively. ...
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  • Nov 2017
  • PLANT CELL TISS ORG
Endemic plants are under constant threat of extinction and micropropagation protocols that can provide not only mechanisms for their revitalisation, but also a possibility for potential sources of new biologically active substances. This study describes the very first use of the liquid culture system for in vitro Knautia sarajevensis shoot multiplication, production of biomass, and an increase in biological activities of the extracts. Murashige and Skoog media containing various concentrations of cytokinins (6-benzyladenine, zeatin, and kinetin) were used to establish agitated shoot cultures of this endemic plant species and to evaluate their effect on shoot morphology. HPLC analysis of phenolic compounds show that the main metabolite in all extracts was salicylic acid with accumulation of rosmarinic and 4-hydroxybenzoic acid for some treatments. The richest sources of phenolics were shoots cultivated in media containing zeatin, which also had high influence on biomass production. Analysis of antioxidant and antimicrobial potential suggests that this plant could have beneficial biological activities. Methanol extracts of shoots cultivated in media containing 2.0 mg/L 6-benzyladenine were moderately active against Staphylococcus aureus and Bacillus spizizeni. DPPH assay showed radical scavenging activity of shoot cultures with IC50 10–90 µg/mL.
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Metabolite Production and Antibacterial Activities of Callus Cultures from Rosa damascena Mill. Petals
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  • Mar 2017
Rosa damascena Mill. is a very fragrant member of Rosaceae family, exhibiting strong antioxidant and antimicrobial activity. In this study, in vitro cell cultures from Rosa damascena Mill. flower petals were established and the effects of precursor L-phenylalanine, the elicitor methyl jasmonate and light/dark treatments on the accumulation of characteristic rose volatile compounds, tocopherols and β-carotene in addition to the antibacterial activity of petal callus extracts were investigated with Solid-Phase Microextraction Combined with Gas Chromatography–Mass Spectrometry (GC–MS). The amount of β-pinene increased by 236 times when 500 µM Phe was added to the culture medium or under light treatment. Strong antibacterial activity from petal callus extracts, up to 2.6- fold compared to amikacin as well as original petal tissues, was obtained under dark treatment for P. aeruginosa ATCC 27853 and S. aureus ATCC 25923. These results revealed that petal callus extracts are sources of natural antioxidants and antibacterial compounds.
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Allelopathic Activity of Extracts from Different Brazilian Peanut ( Arachis hypogaea L.) Cultivars on Lettuce (Lactuca sativa) and Weed Plants
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Peanut ( Arachis hypogaea L.) is the fourth most consumed oleaginous plant in the world, producing seeds with high contents of lipids, proteins, vitamins, and carbohydrates. Biological activities of different extracts of this species have already been evaluated by many researchers, including antioxidant, antitumoral, and antibacterial. In this work, the allelopathic activity of extracts from different Brazilian peanut cultivars against lettuce (Lactuca sativa) and two weed plants ( Commelina benghalensis and Ipomoea nil ) was studied. Aerial parts, roots, seeds, and seed coats were used for the preparation of crude extracts. Seed extract partitioning was performed with n -hexane, dichloromethane, ethyl acetate, n -butanol, and aqueous residue. Germination and growth of hypocotyls and rootlets were evaluated after one and five days of incubation with plant extracts, respectively. Crude seed extract and its dichloromethanic partition displayed highest allelopathic activity. These results contribute for the study of new potential natural herbicides.
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Optimized Extraction of Resveratrol from Arachis repens Handro by Ultrasound and Microwave: A Correlation Study with the Antioxidant Properties and Phenol Contents
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The vegetal species Arachis repens , commonly known as peanut grass, was studied and, for the first time, we detected the presence of the bioactive compound trans- resveratrol ( t -RSV). We compared the efficiency of three different methodologies (conventional maceration [CM], ultrasound-assisted extractions [UAE], and microwave-assisted extractions [MAE]) concerning total phenolics (TP) and resveratrol ( t -RSV) content, followed by antioxidant activity (AA) evaluation. By CM, at 1 h, the highest RSV content ( 1.024±0.036 mg/L) and, correspondingly, the highest DPPH capture ( 23.90±0.04 %) were found. The TP contents, at 1 h, presented the highest value ( 27.26±0.26 mg/g GAE). By the UAE, the maximum yields of TP (357.18 mg/g GAE) and RSV (2.14 mg/L), as well as, the highest AA (70.95%), were obtained by 5 min after a maceration pretreatment, on the solid-solvent ratio 1 : 40 w/v. For MAE, a central composite rotatable design (CCRD) was applied followed by the FFD design in order to evaluate the statistical effects of four independent variables on the extraction of RSV. The optimal conditions established for obtaining the highest recovery (2.516 mg/g) were 20 min; 90% MeOH aq.; 120 rpm; 60°C; and solid-solvent ratio: 1 : 35 w/v. Relevant correlations were established considering the TP and RSV contents, as well as the AA, corroborating obvious advantages of such techniques in terms of high extraction efficiency in shorter times.
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Fruit and vegetable intake and the risk of cardiovascular disease, total cancer and all-cause mortality-A systematic review and dose-response meta-analysis of prospective studies
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  • Feb 2017
  • INT J EPIDEMIOL
Background: Questions remain about the strength and shape of the dose-response relationship between fruit and vegetable intake and risk of cardiovascular disease, cancer and mortality, and the effects of specific types of fruit and vegetables. We conducted a systematic review and meta-analysis to clarify these associations. Methods: PubMed and Embase were searched up to 29 September 2016. Prospective studies of fruit and vegetable intake and cardiovascular disease, total cancer and all-cause mortality were included. Summary relative risks (RRs) were calculated using a random effects model, and the mortality burden globally was estimated; 95 studies (142 publications) were included. Results: For fruits and vegetables combined, the summary RR per 200 g/day was 0.92 [95% confidence interval (CI): 0.90-0.94, I 2 = 0%, n = 15] for coronary heart disease, 0.84 (95% CI: 0.76-0.92, I 2 = 73%, n = 10) for stroke, 0.92 (95% CI: 0.90-0.95, I 2 = 31%, n = 13) for cardiovascular disease, 0.97 (95% CI: 0.95-0.99, I 2 = 49%, n = 12) for total cancer and 0.90 (95% CI: 0.87-0.93, I 2 = 83%, n = 15) for all-cause mortality. Similar associations were observed for fruits and vegetables separately. Reductions in risk were observed up to 800 g/day for all outcomes except cancer (600 g/day). Inverse associations were observed between the intake of apples and pears, citrus fruits, green leafy vegetables, cruciferous vegetables, and salads and cardiovascular disease and all-cause mortality, and between the intake of green-yellow vegetables and cruciferous vegetables and total cancer risk. An estimated 5.6 and 7.8 million premature deaths worldwide in 2013 may be attributable to a fruit and vegetable intake below 500 and 800 g/day, respectively, if the observed associations are causal. Conclusions: Fruit and vegetable intakes were associated with reduced risk of cardiovascular disease, cancer and all-cause mortality. These results support public health recommendations to increase fruit and vegetable intake for the prevention of cardiovascular disease, cancer, and premature mortality.
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Direct organogenesis from cotyledonary node explants suitable for Agrobacterium-mediated transformation in peanut (Arachis hypogaea L.)
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  • Jan 2017
  • PLANT CELL TISS ORG
Efficient and genotype-independent in vitro regeneration is an essential prerequisite for incremental trait improvement in peanut (Arachis hypogaea L.) via genetic transformation. We have optimized a facile and rapid method to obtain direct shoot organogenesis from cotyledonary node (CN) explants excised from peanut seedlings germinated on cytokinin-supplemented Murashige and Skoog (MS) basal salt medium. Starting with mature embryos, shoot induction occurred in approximately 7 weeks, followed by 4 weeks for rooting of excised shoots and 3 weeks of acclimatization of regenerated plantlets in soil. The regeneration and transformation system described here is time-efficient, yielding greenhouse-acclimatized plantlets within 14 weeks, in contrast to 12–14 months required for initiating and regenerating somatic embryogenic cultures, currently the most tractable method available for peanut transformation. The highest shoot induction frequency and shoot quality was obtained with 6.66 μM 6-benzylaminopurine, followed by adequate root induction at 5.37 μM α-Naphthaleneacetic acid. New Mexican Valencia A was chosen for Agrobacterium-mediated transformation. Stable GUS expression from pWBvec10a was obtained at a transformation rate of 1.25 %. Furthermore, results from genomic PCR and Southern blot analyses showed that 14 out of 576 putative transgenic regenerants contained transgene pSag12::IPT, therefore yielding a total transformation rate of 2.43 %. The cotyledonary node-based direct regeneration system described here is time-efficient and amenable to Agrobacterium-mediated transformation, and therefore should be further explored for peanut transgenic improvement.
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Influence of oven and microwave roasting on bioproperties, phenolic compounds, fatty acid composition, and mineral contents of nongerminated peanut and germinated peanut kernel and oils: ALJUHAIMI and ÖZCAN
Article
  • Sep 2017
While antioxidant activity values of nongerminated peanut kernel extracts change between 46.58% (raw peanut) and 49.63% (oven), this values of germinated kernel extracts varied between 38.67 (oven) and 44.83 mgGAE/100 g (germinated). In addition, total phenolic contents of both nongerminated and germinated peanut kernels changed between 12.68 (oven) and 19.73 mgGAE/100 g (raw) and 23.81 (oven) and 41.62 mgGAE/100 g (germinated), respectively. p‐Hydroxybenzoic, vanillic, ferulic, quercetin, and p‐coumaric and cinnamic acids were the dominant compounds of both germinated and nongerminated peanut kernels. It was observed statistically differences in fatty acid composition of peanut oils (p < .05). The highest oleic acid contents (62.74%) were determined in nongerminated kernel oil roasted in oven. The contents of α‐tocopherol in nongerminated peanut ranged from 16.58 mg/100 g (oven roasted) to 18.64 mg/100 g (raw),while α‐tocopherol contents of germinated kernel oils change between 14.72 mg/100 g (microwave roasted) and 16.49 mg/100 g (germinated). Mineral contents of germinated peanut kernels decreased partially compared to nongerminated peanut kernels. Practical applications Nut oils are receiving growing interest due to their high concentration of bioactive lipid components, which have shown various health benefits. Germination produced high phenolic content and antioxidant activities in lupin seeds. Phenolic compounds are generally secondary metabolite produced in plants, and they might be correlated to antioxidant activity, which has been shown to retain various biological benefits; microwave energy and conventional heating are currently being used for food processing operations, including cooking, drying, tempering, baking, pasteurization, and sterilization.
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