Accepted Manuscript Effects of sprouting and postharvest storage under cool temperature conditions on starch content and antioxidant capacity of green pea, lentil and young mung bean sprouts Michał Świeca, Urszula Gawlik-Dziki PII: DOI: Reference:

S0308-8146(15)00480-X http://dx.doi.org/10.1016/j.foodchem.2015.03.108 FOCH 17355

To appear in:

Food Chemistry

Received Date: Revised Date: Accepted Date:

24 October 2014 26 March 2015 27 March 2015

Please cite this article as: Świeca, M., Gawlik-Dziki, U., Effects of sprouting and postharvest storage under cool temperature conditions on starch content and antioxidant capacity of green pea, lentil and young mung bean sprouts, Food Chemistry (2015), doi: http://dx.doi.org/10.1016/j.foodchem.2015.03.108

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Abbreviated running title: Effects of sprouting and postharvest storage on sprouts quality

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Effects of sprouting and postharvest storage under cool temperature conditions on starch content and

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antioxidant capacity of green pea, lentil and young mung bean sprouts

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Michał Świeca*, Urszula Gawlik-Dziki

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Department of Biochemistry and Food Chemistry, University of Life Sciences, Skromna Str. 8, 20-704

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Lublin, Poland

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*Corresponding author: Department of Biochemistry and Food Chemistry, University of Life

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Sciences, Skromna Str. 8, 20-704 Lublin, Poland; Tel.: +48-81-4623327; fax: +48-81-4623324; email:

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[email protected]

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Abstract

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The effects of germination of selected legumes and further storage of sprouts under cool

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conditions on the phenolics, antioxidant activity and starch content and their potential bioaccessibility

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were elucidated. In green pea and mung bean sprouts a slight increase of chemically extractable

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phenolics (including flavonoids) during the first four days of sprouting was observed. Digestion in

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vitro released phenolics; however, flavonoids were poorly bioaccessible. Storage of green pea sprouts

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decreased reducing power and increased the antiradical ability. Reducing potential of potentially

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bioaccessible fraction of stored lentil sprouts was elevated of 40%, 31% and 23% in 3-, 4- and 5-day-

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old sprouts, respectively. Postharvest storage significantly increases the starch digestibility and values

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of expected glycemic index (eGI) - the highest eGIs were determined for 5-day-old stored sprouts;

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75.17-green pea, 83.18–lentil and 89.87 –mung bean. Bioactivity and nutritional quality of legumes is

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affected by sprouting and further storage at low temperatures.

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Key words: sprouts; low-temperature storage; antioxidant capacity, bioaccessibility in vitro, starch,

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expected glycemic index

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1. Introduction

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Sprouting is a cheap, effective and simple tool useful for improving the nutritional and

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nutraceutical quality of cereals, pseudocereals, cruciferous and legumes (Paja̧ k, Socha, Gałkowska,

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Rożnowski, & Fortuna, 2014; Cevallos-Casals & Cisneros-Zevallos, 2010; Świeca, Gawlik-Dziki,

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Kowalczyk, & Złotek, 2012; Guo, Yuan, & Wang, 2011). Germination is a very dynamic process,

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which causes significant qualitative and quantitative changes in the nutrients and bioactive

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compounds. These changes are associated with activation the enzymatic pathways involved in energy

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obtaining (e.g. amylases, proteases), new structures building (the phenylpropanoids pathway, laccase)

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as well as the metabolism of functional compounds such as hormones, regulators etc. (Rosental,

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Nonogaki, & Fait, 2014).

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The quality of sprouted food may be created on each step of its production but depends mainly

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on seeds quality, germination conditions and further storage. The modifications of seeds and/or

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germination conditions may improve the microbiological quality of sprouts e.g. combined treatments

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of mung bean with high pressure, temperature and antimicrobial products (Peñas, Gómez, Frías, &

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Vidal-Valverde, 2010). Additionally, such treatments enhance production of pro-health components

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eg. an increase of phenolics in lentil sprouts treated with hydrogen peroxide (Świeca, & Baraniak,

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2014a) or broccoli sprouts treated with yeast and willow bark extracts (Gawlik-Dziki, Świeca, Dziki,

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& Sugier, 2013) and diversify nutrients content and digestibility e.g. starch and protein digestibility of

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lentil sprouts by abiotic stress treatments (Świeca, & Baraniak, 2014ab; Świeca, Baraniak, & Gawlik-

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Dziki, 2013; Gulewicz, Martinez-Villaluenga, Kasprowicz-Potocka, & Frias, 2014). On the other

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hand, one of the key factors affecting sprouts quality is its age. Sprouts are usually consumed fresh;

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however to inhibit their growth and retain quality (microbial, nutritional and nutraceutical) they are

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stored at low temperatures (e.g. refrigerator). So far there are no studies about the effect of storage on

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the nutritional quality of sprouts and only few studies are available concerning the changes of its

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nutraceutical quality (Świeca, Surdyka, Gawlik-Dziki, Złotek, & Baraniak, 2014c; Goyal, Siddiqui,

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Upadhyay, & Soni, 2014; Force, O'Hare, Wong, & Irving, 2007; Song, & Thornalley, 2007); however,

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in these studies there is no simple relationship between these determinants and sprouts age,

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germination conditions as well as time and storage conditions.

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Biological activity of phytochemicals and nutritional potential of sprouts is strongly affected

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by their metabolic fate, including bioaccessibility and bioavailability (study of chemical extracts does

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not always mirror the real activity in vivo; however, it provides valuable information about mechanism

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of phytochemicals action). Accordingly, for evaluation of nutritional and nutraceutical quality of

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sprouts using the systems determining potential bioaccessibility (conditions simulating those observed

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during the gastrointestinal digestion) is very important. Digestive tract usually acts as an effective

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extractor realizing bioactive compounds from food matrix (Gawlik-Dziki, Jezyna, Świeca, Dziki,

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Baraniak, & Czyz, 2012; D'Archivio, Filesi, Di Benedetto, Gargiulo, Giovannini, & Masella, 2007);

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however, these phytochemicals may interact with nutrients/enzymes, thus limiting nutritional potential

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(Świeca, Gawlik-Dziki, Dziki, Baraniak, & Czyz, 2013b; Świeca, Sȩczyk, Gawlik-Dziki, & Dziki,

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2014e).

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Oxidative damage, caused by the excess of reactive oxygen and nitrogen species, is proved to

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be the cause of many disorders such as cancer, diabetes, and inflammation. Thus, the fundamental

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property of phenolic food compounds is antioxidant activity, that is important for health protectin

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(Rajendran et al., 2014; Gawlik-Dziki et al., 2012). A very important role in dietary prevention,

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specially visible in case of diabetes and Alzheimer disease, plays also nutrients (their level and

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quality) (Rajendran et al., 2014). In this study, the effects of germination and further storage of

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sprouts under cool temperature conditions on the phenolic compounds (strong antioxidants) and starch

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contents (component creating glycemic response) were elucidated. Furthermore, the potential

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bioaccessibility and antioxidative activity of these compounds, the in vitro digestibility of starch and

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expected glycemic index (eGI) were evaluated.

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2. Material and methods

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2.1. Chemicals

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ABTS (2,2-diphenyl-1-picrylhydrazyl), α-amylase (E.C. 3.2.1.1), pancreatin, gallic acid,

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quercetin, amyloglucosidase (EC 3.2.1.3), ammonium thiocyanate, Trolox (6-hydroxy-2,5,7,83

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tetramethylchroman-2-carboxylic acid), invertase (EC 3.2.1.26), pepsin A (EC 3.4.2.3.1) were

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purchased from Sigma–Aldrich company (Poznan, Poland). All others chemicals were of analytical

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grade.

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2.2. Material

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Green pea, lentil and mung bean seeds were purchased from the PNOS S.A. in Ozarów

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Mazowiecki, Poland. Seeds were sterilized in 1% (v/v) sodium hypochlorite for 10 min, then drained

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and washed with distilled water until they reached neutral pH. They were placed in distilled water and

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soaked for 6 hours at 25 °C. Seeds (approximately 150 per plate) were dark-germinated 6 days in a

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growth chamber (SANYO MLR-350H) on Petri dishes (φ 125 mm) lined with absorbent paper

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(relative humidity 70%, 25 °C). Seedlings were watered daily with 5 ml of Milli-Q water. Sprouts

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from subsequent days of cultivation (1-6 day-old; 1F-6F, respectively) were manually collected,

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rapidly frozen, lyophilized, grounded in a labor mill, sieved (60 mesh) and kept in polyethylene bags

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at -20 °C. For postharvest storage experiment ready-to-eat sprouts (3-, 4- and 5-day-old fresh sprouts)

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were manually collected and kept at polypropylene boxes at 4 °C for 7 days (3S, 4S and 5S,

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respectively). After one week storage, sprouts were collected from boxes, rapidly frozen, lyophilized,

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grounded in a labor mill, sieved (60 mesh) and kept in polyethylene bags at -20 °C.

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2.3. Extraction procedures

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2.3.1. Chemical extraction (CE)

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For chemical extraction (CE) sprouts (200 mg of dry mass (d.m.)) were extracted with 5 ml 60

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mM HCl in 70% acetone (v:v:v) for 1 hr at room temperature (22°C ± 2°C), centrifuged (15 min, 3000

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x g, 22°C) and the supernatants were recovered. The procedures were repeated and the supernatants

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combined (Xu and Chang, 2007).

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2.3.2.

Digestion in vitro

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For simulated mastication and gastrointestinal digestion sprouts (200 mg of d.m.) were

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homogenized in 3.5 mL of simulated salivary fluid (2.38g Na2HPO4, 0.19g KH2PO4 and 8g NaCl,

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200U α-amylase (E.C. 3.2.1.1. in 1 liter H2O, pH - 6.75) and shaken for 10 minutes at 37 °C. Next, the

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samples were adjusted to pH = 1.2 with HCl (5 mol/L), suspended in 1.25 mL of simulated gastric 4

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fluid (300 U/mL of pepsin A, EC 3.4.2.3.1 in 0.03 M HCl, pH = 1.2) and shaken for 120 min. at 37

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°C. After simulated gastric digestion, samples were adjusted to pH = 6 with 0.1 mol/L NaHCO3 and

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suspended in simulated intestinal juice (0.05 g of pancreatin (activity equivalent 4 x USP) and 0.3g of

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bile extract in 2.0 mL 0.1mol/L NaHCO3; adjusted to pH = 7 with 1 mol/L NaOH and finally 1.25 mL

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of 120 mmol/L NaCl and 5 mmol/L KCl was added to the sample. The prepared samples underwent in

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vitro intestinal digestion for 120 minutes (Świeca et al., 2013a).

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2.4.

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2.4.1. Determination of total phenolic compounds (TPC)

Determination of phenolics content

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The amount of total phenolics was determined using Folin-Ciocalteau reagent (Singleton,

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Orthofer, & Lamuela-Raventos, 1974). The amount of total phenolics was calculated as a gallic acid

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equivalent (GAE) in mg per g of d.m.

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2.4.2.

Determination of total flavonoids content (TFC)

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Total flavonoids content was determined according to the method described by Lamaison &

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Carnat (1990). One milliliter of extract was mixed with 1 mL of 2% AlCl3 x 6H2O solution and

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incubated at room temperature for 10 min. Thereafter, absorbance at 430 nm was measured. Total

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flavonoids content was calculated as a quercetin equivalent (QE) in mg per g of d.m.

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2.5.

Determination of antioxidant capacity

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2.5.1.

Radical scavenging activity

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The experiments were carried out using an improved ABTS decolorization assay (Re,

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Pellegrini, Proteggente, Pannala, Yang, & Rice-Evans, 1999). The affinity of test material to quench

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ABTS free radical was evaluated according to the following equation:

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scavenging % = [(AC – AA) / AC)] × 100

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where: AC – absorbance of control, AA –absorbance of sample

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Free radical scavenging ability was calculated using the Trolox standard curve prepared and expressed

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as mg Trolox equivalent (TE) per g of d.m.

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2.5.2.

Reducing power

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Reducing power was determined by the method of Oyaizu (1986). Reducing power was

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expressed as Trolox equivalent (TE) in mg per g of d.m.

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2.6.

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2.6.1. Total starch content

Starch content and digestibility

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Total starch (TS) content was determined after dispersion of the starch granules in 2 mol/L

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KOH (50 mg sample, 6 ml KOH) at room temperature (30 min, constant shaking) and hydrolysis of

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the solubilized starch with 80 µL (1mg/ mL) amyloglucosidase (14 U mg-1; EC 3.2.1.3) at 60 ºC for 45

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min (Goni, Garcia-Alonso, & Saura-Calixto, 1997). Glucose content was determined by using the

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standard dinitrosalicylic acid (DNSA) method (Miller, 1959). Total starch was calculated as glucose x

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0.9. The free reducing sugar content of the samples was determined in order to correct the total starch

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values. The sucrose content of the samples was also determined in order to correct the obtained total

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starch values. The samples dispersed in sodium acetate buffer, pH 5.0 were treated with 200 µL of (10

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mg in 1 mL of 0.4 M sodium acetate buffer, pH 5.0) invertase (EC 3.2.1.26., 300 U mg-1) for 30 min at

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37 ºC. After centrifugation, reducing sugars were analyzed in the supernatants, using the DNS reagent.

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After centrifugation (3000 x g, 15 min) and removal of supernatant, the pellet was dispersed with 2

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mol/L KOH, hydrolyzed with amyloglucosidase and liberated glucose was quantified, as described

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above, for total starch (TS).

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2.6.2. The resistant (RS) and potentially bioavailable (AS) starch content

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The resistant (RS) and potentially bioavailable (AS) starch content was analyzed on the basis

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the results obtained after simulated gastrointestinal digestion (2.3.2.). After simulated digestion

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samples were centrifuged (3000 x g, 15 min) and supernatants were removed. The pellets were washed

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2 times with H2O and centrifuged. After that pellets were dispersed with 2 mol/L KOH, hydrolyzed

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with amyloglucosidase and liberated glucose was quantified, as described above, for total starch (TS).

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Resistant starch (RS) was calculated as glucose x 0.9. The potentially bioavailable starch (AS) content

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was calculated as the differences between TS and RS.

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2.6.3. Starch digestibility

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The in vitro digestibility of starch was evaluated on the basis of total starch content (TS) and resistant starch (RS) determined after digestion in vitro according to Świeca et al. (2013a). 6

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 RS  SD [%] = 100% −  × 100%  , where:  TS 

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SD- in vitro digestibility of starch,

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TS- total starch content,

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RS- resistant starch content.

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2.6.4.

In vitro starch digestion rate and expected glycemic index

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The digestion kinetics and expected glycemic index (eGI) of the lentil sprouts were calculated

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in accordance with the procedure established by Goni, Garcia-Alonso, & Saura-Calixto (1998). A non-

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linear model following the equation [C = C∝(1 – e-kt )] was applied to describe the kinetics of starch

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hydrolysis, where C, C1 and k were the hydrolysis degree at each time, the maximum hydrolysis

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extent and the kinetic constant, respectively. The hydrolysis index (HI) was calculated as the relation

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between the areas under the hydrolysis curve (0–240 min) of the sprout sample and the area of

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standard material from white bread. The expected glycemic index (eGI) was calculated using the

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equation proposed by Granfeldt, Björck, Drews, & Tovar (1992): eGI = 8.198 + 0.862HI.

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2.7.

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The following factors were determined for better understanding of the relationships between

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biologically active compounds in the light of their bioaccessibility (Gawlik-Dziki et al., 2012).

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- the relative phenolics bioaccessibility factor (RBF):

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RBF = CD/CCE

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where: CD – concentration of compounds after simulated gastrointestinal digestion, CCE - concentration

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of compounds after chemical extraction,

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- the relative antioxidant efficiency factor (REF):

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REF = AD /ACE

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where: AD – activity of extract after simulated gastrointestinal digestion, ACE - activity of chemical

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extract.

Theoretical approach

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2.8.

Statistical analysis

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All experimental results were mean ± S.D. of three parallel experiments. Two-way analysis of

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variance ANOVA and Turkey’s post-hoc test were used to compare groups. P values < 0.05 were

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regarded as a significant.

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3. Results and discussion

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The nutraceutical potential of legumes sprouts is usually determined by phenolics compounds

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content that exhibit antioxidant, anti-inflammatory, and anticancer properties (Gawlik-Dziki et al.,

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2012; Świeca and Baraniak, 2014ab; Chon, S., 2013). Between the studied sprouts the highest contents

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of total phenolics, including flavonoids, were found for lentil sprouts; however, it should be noted that

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their contents determined after chemical extraction (CE) were significantly lower than those found for

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dry seeds (Figs. 1, 2). In the case of green pea and mung bean sprouts a slight increase in chemically

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extractable total phenolics during the first four days of sprouting (1F-4F) was observed. Similar trend

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was found for flavonoids; however, in case of mung bean sprouts its content remained at a constant

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level (Figs. 1, 2). Digestion in vitro released phenolics from fresh sprouts (RBF values significantly

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exceeding 1); however, flavonoids fraction was poorly bioaccessible (Table 1). Storage at low-

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temperature did not affect on the total phenolics and flavonoids in lentil sprouts (both, chemically

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extractable and potentially bioavailable) as well as total phenolics in mung bean sprouts (potentially

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bioaccessible). In the case of stored, 3-day-old green pea sprouts (3S) the level of potentially

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bioaccessible phenolics was higher than that determined for fresh ones (an increase of 8%), whereas

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for 5-day-old (5S) adverse effect was observed (a decrease of 6%). In case of potentially bioaccessible

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flavonoids, there was a noteworthy increase (about 2- and 3-fold in respect to fresh ones (4F and 5F))

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in 4-, and 5-day-old green pea sprouts (4S and 5S). A slight, but statistically significant, reduction of

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flavonoids content was determined after storage of the 3-day-old green pea (3F) and 5-day-old mung

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bean sprouts (5F) (Figs. 1, 2).

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Germination positively affected the reducing potential of chemically extractable and

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potentially bioaccessible fractions of green pea sprouts (Table 2). Storage caused a slight decrease of

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reducing power and an increase of antiradical abilities of green pea sprouts. It should be also noted 8

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that antioxidants were highly bioaccessible (REF value ca. 3 for reducing power and ca. 10 for

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antiradical activity). The observed changes of reducing potential of chemically extractable fraction of

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lentil and mung bean sprouts did not exceed 10% during germination. Digestion in vitro decreased the

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reducing abilities (lentil and mung bean) and antiradical potential (mung bean) of sprouts (REF values

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lower than 1). In the light of this very valuable is the fact that reducing potential of potentially

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bioaccessible fraction of stored lentil sprouts was increased (in respect to appropriate fresh one) of

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40%, 31% and 23% for 3-, 4- and 5-day-old sprouts, respectively. On the other hand antiradical

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components of green pea and lentil sprouts were effectively extracted during digestion in vitro. Most

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importantly, free radical scavenging abilities of those sprouts were stable during storage (changes did

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not exceed 10%) (Table 2).

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The highest starch contents were found for dry seeds (regardless of the legume type) but starch

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levels were decreased during germination (after 6 days of sprouting a decrease of 43%, 37% and 44%

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in green pea, lentil and mung bean sprouts, respectively) (Table 3). In green pea sprouts, the total

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starch content did not change after storage but it should be noted that the resistant starch contents were

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significantly lower than those determined for fresh sprouts (a decrease of 35%, 36% and 28% for 3-,

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4-, and 5-day old sprouts, respectively). There were no significant changes of the resistant starch

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content, except for 3-day-old lentil sprouts, between fresh and stored mung bean and lentil sprouts.

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Sprouting caused an increase of starch digestibility that was clearly visible in case of lentil sprouts (an

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increase of about 70% after 4-6 day of sprouting in respect to dry seeds). Most importantly storage of

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sprouts significantly elevated values of expected glycemic index (eGI), wherein the highest eGI were

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determined for 5-day-old stored sprouts; 75.17 - green pea, 83.18 – lentil and 89.87 – mung bean (Tab.

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3).

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In foods of plant origin antioxidant potential is closely linked with its

low-molecular

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antioxidants level, especially phenolics. Generally, the determined amounts of phenolics and

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antioxidant capacities levels, as well as a kinetic of changes during sprouting are comparable with

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available literature data (Pająk et al., 2014; Świeca, Sȩczyk, Gawlik-Dziki, 2014d; Cevallos-Casals, &

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Cisneros-Zevallos, 2010). The differences may be caused by the different start material (varieties),

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variable sprouting conditions and extraction systems (Xu & Chang, 2007; Świeca et al., 2012). 9

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Digestion in vitro released phenolics from sprouts which confirm results obtained for total phenolics.

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Similar observations were found previously for sprouts e.g. broccoli (Gawlik-Dziki et al., 2012), lentil

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(Świeca et al., 2013a) or food products enriched with polyphenols e.g. bread enriched with quinoa

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leaves (Świeca et al., 2014d) and coffee enriched with willow bark (Durak, Gawlik-Dziki and Sugier,

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2014). Surprisingly, flavonoids were poorly bioaccessible (Table 1). According to literature data

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flavonoids are stable during digestion (pH and temperature as well as enzymes released phenolics

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from glycosides and/or cell wall elements). Lowered bioaccessibility may be caused by formation of

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complexes with components of digestive tract and/or sprouts protein and starch (Scalbert &

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Williamson, 2000).

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According to RBF value a reductive potential of lentil sprouts is mainly created by

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flavonoids. Although, total phenolics of lentil sprouts were well bioaccessible a reducing powers of

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extracts obtained after digestion were significantly lower than those determined for chemical extracts.

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This observation highly corresponded with changes in flavonoids fraction. Phenolics play a key role as

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antioxidants in legumes; however, according to these studies it may be speculated that creation of

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antioxidant activity may also contribute to other compounds. In some cases, especially in green pea

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sprouts, an increase in antioxidant activity was disproportionate to increase in polyphenols content,

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both during germination and after in vitro digestion. Thus, it may be speculated that in this case the

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role in the creation of antioxidant potential is also played by bioactive peptides and oligosaccharides.

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The presence of antioxidant peptides in legume proteins hydrolysates obtained after treatment with

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digestive enzymes was already confirmed by Karaś, Jakubczyk, & Baraniak (2010). On the other hand

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these disparities may be caused by the interaction of sprouts phenolics among themselves and with

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other sprouts components. There are only few studies concerning changes in the antioxidant level of

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sprouts during storage at low temperatures; however, they do not provide any information about the

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effects of postharvest storage on the antioxidant activity and level and bioaccessibility of bioactive

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constituents.

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In the study performed by Świeca et al. (2014c), potentially bioaccessible fraction of lentil

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sprouts, treated during germination at low and high temperature, recorded the same reducing and

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chelating power as fresh samples. Goyal et al. (2014) proved that during storage of mung bean at room 10

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and low temperature ascorbic acid, total phenols and antioxidant activity of sprouts firstly increased

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and then decreased significantly. Similar observation was found in this study where reducing potential

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of mung bean sprouts was lowered after storage; however, antiradical activity of sprouts has not been

277

changed. During 1 week storage of broccoli sprouts at 4 °C and 8 °C ascorbic acid contents were

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decreased, while total phenol contents were generally stable (Waje, Jun, Lee, Moon, Choi, & Kwon,

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2009). The effect of cold storage of the 7-day-old-sprouts of broccoli, kohl rabi, white radish and

280

rocket was studied by Force et al. (2007). They proved that there is no significant loss of

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glucosinolates (potential anticancer compounds) under domestic refrigeration conditions.

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Sprouting significantly changes the nutritional quality of legumes seeds. Nutrients and micro-

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and macroelements are more accessible; usually vitamin content is also increased. Legumes are known

284

to be an excellent source of nutrients (valuable source of starch and protein) and importantly their

285

consumption does not cause an abrupt increase in postprandial blood glucose level, which in turn

286

induces immediate oxidative stress (Hoover & Zhou, 2003). Somehow pro-health benefits of legume

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sprout-rich diet is linked with a high content of phenolics, an important role plays also starch content

288

and its quality. On germination, a significant decrease in the starch contents was observed, which

289

could be due to the use of starch as an energy source in the sprouting process. These data agree with

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the findings of Ghavidel and Prakash (2007) for the germinated green gram, cowpea, lentil, and

291

chickpea. Relatively high amounts of resistant starch, in comparison to other studies (Hoover & Zhou,

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2003; Eyaru, Shrestha, & Arcot, 2009), are probably caused by the method used for its determination -

293

in vitro conditions (gastrointestinal digestion). Generally, no information is available on changes in

294

starch content and its digestibility during cool storage. Some researchers postulate that the changes are

295

linked with modification of the starch structure (reduction of amylose content, which is very resistant

296

due to its higher crystallinity), and content and the structure and/or activity of factors influencing the

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rate of its mobilization (e.g., amylase inhibitors, tannins, phytic acid) (Cevallos-Casals & Cisneros-

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Zevallos, 2010; Ghavidel & Prakash, 2007; Hoover and Zhou, 2003). It is thus suggested that during

299

storage (similarly to sprouting), starch structure is loosened, which probably creates a large space

300

within the matrix and increases the susceptibility to enzymatic attack (Benítez et al., 2013). This

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statement is also supported by the previous studies of Fernandez and Berry (1989) and Frias, Fornal, 11

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Ring, & Vidal-Valverde (1998), who observed that germination sharply increased the susceptibility of

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chickpea and lentil starch to digestion by α-amylase, indicating the influence of dextrination in

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producing material more susceptible to enzymatic attack. On the other hand, although at low

305

temperature metabolic rate is reduced, germination caused dynamic changes in the amylases level and

306

activity. These factors consequently improved the digestibility of starch and reduced the resistant

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starch content which may partially explain a significant increase of starch digestibility and expected

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glycemic index values (in respect to fresh sprouts) determined after 1 week storage at 4°C.

309 310

Conclusion

311

Legumes are food products highly desired by the modern communities because of their low

312

glycemic index and high amounts of potentially resistant starch and polyphenolics. Sprouting and

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further storage can effectively modify the nutraceutical and nutritional values. Both, time of

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germination and storage, diversified the phenolics antioxidant levels, antioxidant activity of sprouts

315

and affect their bioaccessibility in vitro. Postharvest storage significantly increases the starch

316

digestibility and expected glycemic index value that was linked with reduction of resistant starch

317

content. In the light of these results, it may be concluded that the bioactivity and nutritional quality of

318

sprouted legumes are affected by storage at low temperatures, however, there is no a simple pattern

319

which could predict potential changes.

320 321

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Świeca, M., Sȩczyk, Ł., Gawlik-Dziki, U., & Dziki, D. (2014d). Bread enriched with quinoa leaves -

421

the influence of protein-phenolics interactions on the nutritional and antioxidant quality. Food

422

Chemistry, 162, 54-62.

423

Świeca, M., Sȩczyk, Ł., & Gawlik-Dziki, U. (2014e). Elicitation and precursor feeding as tools for the

424

improvement of the phenolic content and antioxidant activity of lentil sprouts. Food Chemistry,

425

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426

Waje, C. K., Jun, S. -., Lee, Y. -., Moon, K. -., Choi, Y. H., & Kwon, J. -. (2009). Seed viability and

427

functional properties of broccoli sprouts during germination and postharvest storage as affected by

428

irradiation of seeds. Journal of Food Science, 74(5), C370-C374.

429

Xu, B. J., & Chang, S. K. C. (2007). A comparative study on phenolic profiles and antioxidant

430

activities of legumes as affected by extraction solvents. Journal of Food Science, 72(2), S159-

431

S166.

432 433 434 435 436 437 438 16

439

Figure captions

440 441

Fig. 1. Total phenolics content in fresh and stored sprouts. A- green pea; B- lentil; C-mung bean.

442

Values on selected figures designated by the different letters are significantly different (P < 0.05).

443

1F-6F – 1-6-day-old fresh sprouts; 3S-5S – 3-5-day-old stored sprouts

444 445 446

Fig. 2. Total flavonoids content in fresh and stored sprouts. A- green pea; B- lentil; C-mung bean.

447

Values on selected figures designated by the different letters are significantly different (P < 0.05).

448

1F-6F – 1-6-day-old fresh sprouts; 3S-5S – 3-5-day-old stored sprouts

449

17

5,0

A h gh

Total phenolics content [mg/ g d.m.]

4,5

fg

def e

4,0

d

g

e

f

d

cd

fg

ef

c

c

3,5 bc

b

b

bc

3,0 a 2,5 0

1

2

3

4

5

6

450

B

11 10

c

c

c

Total phenolics content [mg/ g d.m.]

c 9

bc

8

bc

c

c

bc bc

b

7 a 6 a

a

a

a

a

a a

a

5 4 0

1

2

3

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5

6

451

C

6,0 5,5

f

ef ef

Total phenolics content [mg/ g d.m.]

5,0 e 4,5

d

4,0

c

ef

c

bc

ab

a

2,5 0 seeds

453

c

c

e

e

3,5 3,0

1 1F

fresh-chemical extracts stored- chemical extracts

452

de

cde

2 2F

3 3F 3S

a

abc

a

4 4F 4S

55F 5S

fresh- extracts after digestion stored- extracts after digestion

Fig. 1. 18

6 6F

0,8

A f

Flavonoids content [mg/ g d.m.]

ef

de

e

0,5

de d

d

de

de cd

c 0,3

ab

b ab

a

de

de

a

a

5

6

a 0,0 0

1

2

3

4

454 1,8

B f

Flavonoids content [mg/ g d.m.]

1,5 1,3

de

de

cde

cde

cd

1,0

c

d c

c 0,8 ab

a

0,5

ab

a

b a

ab

a

ab

a

0,3 0,0 0

1

2

3

4

5

6

455 0,7

C g

f

f

Flavonoids content [mg/ g d.m.]

f

e e

d c 0,2

a

abc

a

a

a

1 1F

b

b

a

fresh-chemical extracts stored- chemical extracts

456

ef e

0,0 0 seeds

457

ef

0,5

2 2F

a

3 3F 3S

4 4F 4S

5 5F 5S

fresh- extracts after digestion stored- extracts after digestion

Fig. 2. 19

6 6F

458 459 460

Table 1. The relative phenolics bioaccessibility (RBF) of fresh and stored sprouts Green pea

Seeds 1F 2F 3F 4F 5F 6F 3S 4S 5S 461 462 463

Total phenolics 1.23±0.06b 1.09±0.05a 1.10±0.06a 1.12±0.06ab 1.23±0.06b 1.29±0.06bc 1.57±0.08d 1.37±0.07c 1.26±0.06bc 1.11±0.06a

Flavonoids 0.16±0.01a 0.21±0.01b 0.39±0.02e 0.57±0.03g 0.47±0.02f 0.28±0.01c 0.31±0.02d 0.56±0.03g 0.86±0.04h 1.00±0.05i

Lentil Total phenolics 1.21±0.06a 1.46±0.07b 1.41±0.07b 1.48±0.07bc 1.51±0.08bc 1.65±0.08c 1.40±0.07b 1.44±0.07bc 1.57±0.08bc 1.53±0.08bc

Flavonoids 0.32±0.02a 0.36±0.02a 0.50±0.03cd 0.55±0.03d 0.44±0.02b 0.58±0.03de 0.57±0.03de 0.48±0.02bc 0.51±0.03cd 0.62±0.03e

Mung bean Total phenolics 1.35±0.07c 1.12±0.06a 1.17±0.06ab 1.25±0.06bc 1.35±0.07c 1.46±0.07c 1.76±0.09d 1.41±0.07c 1.43±0.07c 1.34±0.07c

Flavonoids 0.32±0.02b 0.36±0.02c 0.33±0.02b 0.42±0.02d 0.44±0.02d 0.52±0.03e 0.570.03±e 0.660.03±f 0.550.03±e 0.30±0.02a

Values (± SD), in columns, designated by the different letters are significantly different (P < 0.05). 1F-6F – 1-6-day-old fresh sprouts; 3S-5S – 3-5-day-old stored sprouts

464 465 466 467 468 469 470 471 472 473 474 475 476 477

20

478 479

481

Table 2. Antioxidant activity of fresh and stored sprouts Reducing power Antiradical activity REF REF [µmol TE/g d.m.] [µmol TE/g d.m.] CE DE CE DE Seeds 0.65±0.10a 8.06±0.71g 12.43 1.72±0.21ab 30.91±1.03fg 17.93 1F 0.47±0.09a 8.14±0.48g 17.45 1.11±0.41a 25.56±3.05ef 22.99 2F 0.93±0.07b 6.25±0.61f 6.69 1.13±0.61ab 25.58±0.75e 22.6 3F 1.23±0.08c 8.96±0.49gh 7.28 1.14±1.06ab 25.60±1.42e 22.36 Green 4F 1.97±0.33d 8.36±1.28fg 4.25 1.22±0.86ab 30.08±3.12fg 24.73 5F 2.53±0.35de 9.33±0.35h 3.68 1.97±0.32b 31.28±2.86efg 15.9 pea 6F 2.85±0.36e 9.33±0.42gh 3.27 4.97±0.18d 33.46±1.57fg 6.73 3S 2.36±0.11de 6.87±0.76fg 2.91 2.55±0.20bc 31.60±1.82fg 12.4 4S 2.30±0.14de 7.59±1.44fg 3.3 2.43±0.14b 28.84±1.38fg 11.85 5S 2.28±0.09d 6.92±1.10fg 3.04 2.92±0.23c 25.21±3.07ef 8.62 Seeds 55.59±3.68de 49.94±1.22c 0.9 54.74±1.41c 61.31±0.43e 1.12 1F 58.19±1.57e 22.63±0.75a 0.39 33.95±2.31b 60.39±0.67e 1.78 2F 54.00±1.26d 21.25±4.03a 0.39 30.91±1.38ab 56.90±3.04cde 1.84 3F 54.17±7.47de 23.02±6.40ab 0.42 30.02±3.62ab 59.11±1.51cd 1.97 4F 61.39±5.24de 26.08±2.40a 0.42 31.66±2.09ab 60.23±0.84ef 1.9 Lentil 5F 51.96±8.01de 27.30±4.07ab 0.53 26.58±5.10ab 56.48±4.29cd 2.12 6F 53.84±7.31de 28.33±4.61ab 0.53 26.62±4.24ab 58.49±0.50d 2.2 3S 53.94±8.06de 32.02±4.75b 0.59 28.91±0.91b 59.68±1.89cd 2.06 4S 54.75±3.09de 34.24±4.42b 0.63 24.90±1.08a 59.06±0.72d 2.37 5S 50.99±5.62de 33.43±6.87b 0.66 27.73±2.68ab 60.42±1.10de 2.18 Seeds 51.93±1.07h 15.86±1.98a 0.31 86.79±0.75g 19.57±1.26c 0.23 1F 54.62±1.18i 18.29±1.46ab 0.33 78.38±3.46e 22.81±1.05d 0.29 2F 55.18±1.58hi 18.07±1.92ab 0.33 79.17±2.00e 22.63±1.31d 0.29 3F 53.48±1.21hi 19.24±2.33abc 0.36 84.79±0.34f 19.66±1.35c 0.23 4F 48.71±0.69fg 21.51±2.03bc 0.44 82.43±2.07ef 17.85±2.52c 0.22 Mung 5F 50.10±2.26fgh 25.63±1.58cd 0.51 84.57±1.42f 15.78±0.24b 0.19 bean 6F 45.04±0.39e 29.90±1.91d 0.66 85.29±0.54f 16.97±0.80b 0.2 3S 46.12±2.20ef 20.46±0.19b 0.44 86.26±1.35fg 14.90±0.51a 0.17 4S 47.38±0.65f 20.82±0.28b 0.44 84.43±2.48efg 15.41±0.12a 0.18 5S 49.93±0.87g 23.72±1.30c 0.48 82.211.45e 16.24±0.22b 0.2 Values, within the selected activity and species, designated by the different letters are significantly

482

different (P < 0.05).

483

CE- chemical extracts; DE- extracts obtained after digestion in vitro; REF- the relative antioxidant

484

efficiency factor

485

1F-6F – 1-6-day-old fresh sprouts; 3S-5S – 3-5-day-old stored sprouts

480

21

486 487 488

Table 3. Starch content and digestibility, expected glycemic index of fresh and stored sprouts

Green pea

Lentil

Total Resistant starch starch [mg/ g d.m.] [mg/ g d.m.] Seeds 325.5±32.9d 125.4±12.85d 1F 257.8±0.3c 94.9±14.81c 2F 258.5±43.7abcd 91.8±23.74bcd 3F 240.1±46.9abcd 79.3±16.93bc 4F 221.0±0.5a 75.9±8.14bc 5F 218.2±20.7ab 71.6±20.66abc 6F 213.3±43.8abc 59.9±13.77ab 3S 236.7±0.2b 58.1±0.05a 4S 217.3±14.8a 56.1±14.78ab 5S 213.2±40.4abc 55.9±10.39ab

Available starch [mg/ g d.m.] 200.2±10.02d 162.9±6.68bc 166.7±13.34bc 160.8±8.20bc 145.1±4.50a 146.6±2.93a 153.3±4.31ab 178.5±9.10c 161.2±6.61b 157.3±9.44ab

Starch digestibility [%] 61.49±3.07a 63.18±2.21a 64.50±3.22ab 66.96±2.68ab 65.66±3.28ab 67.18±3.36ab 71.89±2.52bc 75.43±3.77c 74.18±2.97c 73.78±3.69bc

Expected glycemic index 27.61±0.69a 32.19±0.80b 36.57±0.91c 39.31±0.98d 39.04±0.98d 43.07±1.08e 44.85±1.12f 45.51±1.14f 46.11±1.15f 75.17±1.88g

Seeds 1F 2F 3F 4F 5F 6F 3S 4S 5S

128.1±6.53b 41.62±2.08a 131.1±5.37b 46.26±1.62b 133.2±10.65bc 52.82±2.64c 142.2±7.25c 49.23±1.97bc 144.0±4.47c 71.64±3.58e 114.7±2.29a 67.52±3.38de 130.5±3.67b 72.26±2.53e 140.4±7.16cb 71.27±3.56e 144.4±5.92c 67.68±2.71ed 122.4±7.35ab 63.21±3.16d

36.00±0.90a 44.75±1.12b 48.57±1.21c 49.07±1.23c 55.90±1.40d 63.09±1.58e 69.04±1.73f 57.74±1.44d 58.54±1.46d 83.18±2.08g

307.8±8.5e 283.4±8.4d 271.0±21.3d 268.5±36.2cde 201.1±22.2b 169.9±2.0a 180.5±25.6ab 196.9±23.0b 213.3±30.1bc 193.7±14.1b

179.7±1.63d 152.3±9.24c 137.9±13.82bc 126.3±7.02b 57.0±4.12a 55.2±13.68a 50.1±11.25a 56.6±10.61a 68.9±7.23a 71.3±16.34a

489

Seeds 310.1±8.9e 151.9±14.23d 158.1±8.06e 51.00±2.55a 32.68±0.82a 1F 244.3±1.5d 104.7±9.46bc 139.5±5.72d 57.13±2.00bc 37.33±0.93b 2F 236.2±1.1c 102.2±9.21bc 144.0±11.52de 60.98±3.05c 42.48±1.06c 3F 230.3±1.1bc 110.4±3.27bc 119.9±6.12bc 55.90±2.24ab 46.03±1.15d 4F 221.9±5.1b 83.0±1.43a 138.9±4.30d 62.60±3.13c 53.81±1.35e Mung bean 5F 210.9±15.7ab 81.5±2.46a 129.4±2.59c 61.37±3.07c 61.75±1.54f 6F 192.4±4.1a 79.9±0.89a 112.5±3.16ab 58.47±2.05c 76.73±1.92g 3S 229.1±14.8bcd 91.5±5.47b 137.5±7.01d 60.04±3.00c 52.77±1.32e 4S 222.4±2.8b 78.4±14.06ab 144.0±5.90d 49.92±2.00a 60.54±1.51f 5S 174.2±26.0a 70.0±7.14a 104.2±6.25a 59.82±2.99c 89.87±2.25h Values, within the selected characteristic, designated by the different letters are significantly different

490

(P < 0.05).

491

1F-6F – 1-6-day-old fresh sprouts; 3S-5S – 3-5-day-old stored sprouts

492 493 22

494 495

Highlights

496 497 498

Green pea, lentil and mung bean were sprouted and storage under cool condition

499

Phenolics, antioxidant capacity and starch quality in legume sprouts were studied

500

Reducing potential of bioavailable fraction of stored lentil sprouts was elevated

501

Storage of sprouts significantly elevated values of expected glycemic index

502 503

23

Effects of sprouting and postharvest storage under cool temperature conditions on starch content and antioxidant capacity of green pea, lentil and young mung bean sprouts.

The effects of germination of selected legumes and further storage of sprouts under cool conditions on the phenolics, antioxidant activity and starch ...
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