Impaginato 541 Adv. Hort. Sci., 2018 32(4): 541-548 DOI: 10.13128/ahs-22211 Yield, quality, antioxidants and mineral nutrients of Physalis angulata L. and Physalis pubescens L. fruits as affected by genotype under organic management N.A. Golubkina 1 (*), H.G. Kekina 2, M.R. Engalichev 1, M.S. Antoshkina 1, S.M. Nadezhkin 1, G. Caruso 3 1 Agrochemical Research Center, Federal Scientific Center of Vegetable Production, 143080 Moscow region, Odintsovo district, VNIISSOK, Selectsionnaya 14, Russia. 2 Medical Academy of Postgraduate Education, 123995 Moscow, Russia. 3 Dipartimento di Scienze Agrarie, Università degli Studi di Napoli Federico II, Via Università, 100, 80055 Portici (Na), Italy. Key words: antioxidants, mineral nutrients, Physalis angulata L., Physalis pubes- cens L., production, sugars, taste. Abstract: Introduction and selection of unconventional plants with high con- centration of biologically active compounds is one of the worthy ways for pro- ducing functional food, which is beneficial to human health. Research was car- ried out in northern Europe (Russia) with the purpose to assess yield, quality and biologically active compounds concentration in Physalis angulata and Physalis pubescens fruits. P. angulata cultivars Konditer and Konditer 2 gave the highest yield (11.3 and 11.0 t·ha-1 respectively), due to the highest mean fruit weight (80 and 70 g respectively); P. pubescens variety Zolotaya rossip had the worst outcome due to the very small berries (3 g), in spite of their highest number per plant (165). ‘Zolotaya rossip’ fruits overall attained higher values of quality indicators compared to all P. angulata cultivars. Positive correlations were recorded between dry matter and polyphenols as well as between total sugars and polyphenols. Physalis fruits showed to be a good source of antioxi- dants, K, Mg and P for human beings. Taste index turned out highly reliable in evaluating fruit quality and it was dependant on dry matter, total sugars, polyphenols and Ca. 1. Introduction The availability of new functional food has been becoming more and more important for human health regulation and protection against the major diseases of the millennium. Physalis fruit is mostly an exotic product, imported from tropical and subtropical regions, particularly from Central America, where this genus is characterized by the highest biodiversity (Medina-Medrano et al., 2015). The popularity of this genus plants has been increasing in several world (*) Corresponding author: segolubkina45@gmail.com Citation: GOLUBKINA N.A., KEKINA H.G., ENGALICHEV M.R., ANTOSHKINA M.S., NADEZHKIN S.M., CARUSO G., 2018 - Yield, quality, antioxidants and minearl nutrients of Physalis angulata L. and Physalis pubescens L. fruits as affected by geno- type under organic management. - Adv. Hort. Sci., 32(4): 541-548 Copyright: © 2018 Golubkina N.A., Kekina H.G., Engalichev M.R., Antoshkina M.S., Nadezhkin S.M., Caruso G. This is an open access, peer reviewed article published by Firenze University Press (http://www.fupress.net/index.php/ahs/) and distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Competing Interests: The authors declare no competing interests. Received for publication 1 December 2017 Accepted for publication 12 July 2018 AHS Advances in Horticultural Science Adv. Hort. Sci., 2018 32(4): 541-548 542 Countries, due not only to its high nutritional value and exclusive taste (Puente et al., 2011), but also to its effectiveness as a medical plant. Indeed, all plant parts are useful in modern medicine for their proper- ties: antiasthma, antihepatitis, antimalaria and anti- dermatitis (Chang et al., 2008), antiallergenic, anti- carcinogenic, anti-inflammatory, antihyperglycemic, antimicrobial, antiseptic, antiviral, cardio-protective, diuretic, expectorant, febrifuge (Bastos et al., 2006; Sharma et al., 2015). In this respect, a negative corre- lation has been shown between the level of Physalis consumption and the risk of cardiovascular, pul- monary and gastrointestinal diseases (Leenders et al., 2014; Hjartaker et al., 2015). Moreover, the high antioxidant activity of water and alcoholic extracts of Physalis is reportedly beneficial to patients suffering from Alzheimer’s disease as well as from memory and concentration deficit (Susanti et al., 2015). Among the tens of Physalis species, P. angulata and P. pubescens are the most suitable for production in the northern Europe, due to their frost resistance and tolerance to fungal and bacterial diseases (Mamedov et al., 2017). Notably, the genetic selec- tion carried out in Russia allowed to create interest- ing varieties, suitable for cultivation both in central Russia (Kondratieva and Engalichev, 2013; Mamedov et al., 2017) and in Siberia (Makarov, 2002), mainly belonging to P. angulata. However, a few results con- cerning the variability of interspecies quality charac- teristics and even no cultivar comparisons of biologi- cally active compounds accumulation in Physalis fruits have been published so far. Taking into account the scarcity of literature reports, the present research was aimed at evaluat- ing the varietal differences in yield, quality and antioxidant content of P. angulata and P. pubescens fruits grown in northern Europe. 2. Materials and Methods Growth conditions Six P. angulata L. cultivars (Violet, Lakomka, Konditer, Konditer 2, Lezhky, Korolek) and one P. pubescens L. cultivar (Zolotaya rossip) were com- pared in a research carried out, under the organic farming management, in the experimental fields of the Federal Scientific Center of Vegetable Production (Moscow region, 55° 39’ 23’’ N, 37° 12’ 43’’ E) in 2015 and 2016. The trial was conducted on a clay-loam soil, with рН 6.8, 2.1% organic matter, 108 mg·kg-1 N, 450 mg·kg-1 P2O5, 357 mg·kg-1 K2O, exchangeable bases sum as much as 95.2%. The air temperature values, recorded at plant level, were: 14.2°C and 13.5°C in May, 16.9°C and 17.1°C in June, 21.2°C and 20.4°C in July, 19.3°C and 18.0°C in August, 12.1°C and 12.2°C in September, in 2015 and 2016 respec- tively. A randomized complete blocks design, with three replicates, was used for treatments distribution in the field; each treatment had a 19.25 m2 (5.5 × 3.5 m) surface area, including 50 plants. Physalis seeds were sown in peat boxes on 14 April and the seedlings were transplanted in the field on 23 May, spaced 55 cm along the rows, the latter being 70 cm apart. As for P. angulata, the six culti- vars chosen for the trial are the most spread in Russia, whereas within P. pubescens only the cultivar Zolotaya rossip tested in our research is cultivated in this Country. The organic farming practice complied with EC Regulation 834/2007. Physalis crops were preceded by pea and each year the fertilization supplied the crops with 56 kg ha-1 of N, 16 of P2O5 and 98 of K2O. Half of the fertilizers dose was given just before transplanting and the remaining 50% on dressing at two week intervals. Drip irrigation was practiced for watering the crops when needed. Plant protection from fungal diseases and insects was achieved by adopting Trichoderma suspensions, copper, sulphur, azadirachtin. Harvests were carried out from mid-August to the end of September. General analytical methods Ripe, undamaged and regularly shaped fruits were classified as “marketable”. At each harvest, the weight and number of marketable fruits in each plot was recorded and the mean weight was assessed on random samples of 50 fruits per plot. Cumulative plant biomass was calculated as the sum of the above-ground plant biomass at the end of the experi- ment plus the total fruit production from the begin- ning of the harvest period. Dry weight was assessed after dehydration of the fresh samples in an oven at 70°C until they reached constant weight. In each plot, a sample of twenty-five fruits was collected and transferred to the laboratory for analysis. Samples preparation Prior to analyses, Physalis fruits were extracted from papery husk and homogenized with a stainless steel blender for 1 min. The resulting homogenates Golubkina et al. - Physalis spp. under organic management 543 were immediately subjected to the analysis. Total soluble solids (TSS) and sugars Determination of total soluble solids was carried out by a refractometer (IRF-22, Russia). The results were reported as °Brix at 20°C. Mono- and disaccharides were determined using cyanide method (Kidin, 2008). Titratable acidity (TA) T A w a s m e a s u r e d u s i n g 2 0 m l o f t h e w a t e r Physalis extract (1:1), titrated to pH 8.1 using 0.1 N NaOH (GOST, 1996). The following formula was used for calculation: TA= V 1 x 0.1x0.064x100:20 where V-1 is the volume of NaOH used; 0.1 is the NaOH normality; 0.064 is the weight of a citric acid milliequivalent in g; 20 is the volume of the Physalis extract used. Mineral nutrients K, Mg, Mn, Ca, Na and P contents in dried homog- enized fruit samples were assessed using ICP-MS on q u a d r u p l e m a s s - s p e c t r o m e t e r N e x o n 3 0 0 D (Golubkina et al., 2017). Nitrate content in fresh fruits of Physalis species was determined using ion- selective electrode on ionomer Expert-001 (Russia), as previously described (Golubkina et al., 2017). Antioxidants Total polyphenols were assessed using Folin- Ciocalteu colorimetric method (Sagdic et al., 2011). The ascorbic acid content was determined by visual titration of fruit extracts in 6% trichloracetic acid with Tillmans reagent (AOAC, 2012). Taste The assessment of Physalis taste was performed using two methods: chemical and organoleptic. Taste index was calculated starting from the Brix degree and acidity values, using the equation proposed by Navez et al. (1999) and Nielsen (2003) for tomato fruits: TI = (Brix/20 TA) + TA where TI is the taste index and TA is the titratable acidity calculated referring to citric acid. Though organoleptic perception of taste depends on the cultural background of judges and cannot be considered universally objective, Physalis fruit taste was evaluated additionally by 10 experts, via sensory analysis using 5 balls scales (Krueger and Casey, 2000). Statistical analysis Data were processed by analysis of variance and mean separations were performed through the Duncan multiple range test, with reference to 0.05 probability level, using SPSS software version 21. Data expressed as percentage were subjected to angular transformation before processing. Notably, the factor “year of research” had no significant effects on the variables examined, both in terms of main effects and of interactions with the other experimental factor. Therefore, we have reported the results obtained from the data statistical process- ing as means of the two years of research. 3. Results and Discussion Plant growth and yield As it can be seen in Table 1, a correspondence between plant height and dry matter was recorded in P. pubescens variety Zolotaya rossip, which had the smallest plants and the lowest dry matter, whereas within P. angulata the cultivar Korolek showed the Table 1 - Biometrical, growth and yield parameters of P. angulata and P. pubescens cultivars Within each column, means followed by different letters are significantly different according to the Duncan multiple range test at p≤0.05. Cultivar Plant height (cm) Plant dry weight (g·m-2) Planting to harvest beginning (days) Fruits per plant (no.) Yield (t·ha-1) Mean fruit weight (g) Violet (P. angulata) 90 d 296.6 c 105 bc 58 cd 9.0 b 60 c Korolek (P. angulata) 130 a 320.3 c 108 b 64 b 9.3 b 56 cd Lakomka (P. angulata) 105 c 200.7 d 90 d 47 f 7.3 c 60 c Konditer (P. angulata) 125 ab 402.5 a 115 a 62 bc 11.3 a 70 b Konditer 2 (P. angulata) 120 b 368.3 b 102 c 53 e 11.0 a 80 a Lezhky (P. angulata) 110 c 223.6 d 118 a 55 de 7.7 c 54 d Zolotaya rossip (P. pubescens) 80 e 133.3 e 85 e 165 a 1.3 d 3 e Adv. Hort. Sci., 2018 32(4): 541-548 544 tallest plants but ‘Konditer’ and ‘Konditer 2’ pro- duced the highest dry matter amounts. The latter cultivar was characterized by the longest crop cycle, similarly to Lezhky, and P. pubescens Zolotaya rossip resulted in the earliest fruit ripening; among P. angu- l a t u m v a r i e t i e s , o n l y ‘ L a k o m k a ’ s h o w e d e a r l y r i p e n e s s c o m p a r a b l e t o ‘ Z o l o t a y a r o s s i p ’ o n e . Correspondently to plant dry matter production, P. angulata cultivars Konditer and Konditer 2 also gave the highest yield (11.3 and 11.0 t·ha-1 respectively), due to the highest mean berry weight (80 and 70 g respectively), whereas P. pubescens variety Zolotaya rossip had the worst outcome, in spite of the huge number of fruits per plant which were, however, very small (3 g). Among P. angulatum varieties, Lakomka and Lezhky showed the lowest values (7.3 and 7.7 t·ha-1 respectively), due to the lowest prolificity and the smallest fruits respectively. Quality indicators and mineral nutrient content As reported in Table 2, the fruits of P. pubescens cultivar Zolotaya rossip overall attained higher values of quality indicators than the six P. angulata varieties examined; compared to the average of the latter six cultivars, P. pubescens fruits showed 1.6 and 1.95 times higher content of total sugars and monosac- charides respectively as well as 1.27 times higher titratable acidity. Among P. angulata cultivars, in ‘Violet’ fruits the highest levels of dry residue, solu- ble solids and total sugars were recorded and in ‘Lezhky’ the lowest. Otherwise, ‘Lakomka’ showed the highest monosaccharide content (32.2% out of total sugars) and cultivar Violet the lowest (18.8%); the variation coefficient relevant to monosaccharide content in P. angulata species attained 18.3%. As for quality indicators, the Physalis cultivars tested showed high variability in the content of dry matter (15.0%) and sugars (28.2%) as well as in juice acidity (16.7%), whereas the juice pH variability was low (2.1%). In our research, dry matter and sugar content in P. pubescens are similar to those detected in Physalis berries grown in tropical and subtropical countries (Yildiz et al., 2015). Notably, soluble sugars highly affect flavour quality of tomato fruits (Doras et al., 2001) and, according to Olivares-Tenorio et al. (2016) reports, the main carbohydrates of Physalis fruits are sucrose and glucose, whereas fructose content is neglectable. The analysis of mineral nutrient content per- formed in our research showed the close element concentrations of P. pubescens and P. angulata fruits grown in the same environmental conditions (Table 3). As for varietal differences in mineral nutrient Table 2 - Quality indicators of Physalis angulata and P. pubescens cultivars fruits Table 3 - Mineral nutrient concentrations in Physalis angulata and P. pubescens cultivars fruits (mg kg-1 d.w.) Within each column, means followed by different letters are significantly different according to the Duncan multiple range test at p≤0.05. Cultivar Dry matter (%) Soluble solids (°Brix) Total sugars (%) Reducing sugars (%) Titratable acidity (%) рН Violet 10.5 b 8.1 b 7.8 b 1.8 d 0.79 c 4.82 ab Korolek 9.3 d 5.9 c 5.6 d 1.8 d 0.70 d 4.65 bc Lakomka 8.7 e 6.1 c 6.0 c 2.9 b 0.45 f 4.94 a Konditer 10.0 bc 6.0 c 5.9 cd 1.6 d 0.88 b 4.62 bc Konditer 2 9.7 cd 6.1 d 5.9 c 2.2 c 0.79 c 4.51 c Lezhky 8.5 e 4.9 d 4.7 e 1.7 d 0.63 e 4.70 ac Zolotaya rossip 15.5 a 9.7 a 9.6 a 3.9 a 0.90 a 4.72 ac Mean 9.5 6.2 6.0 2.0 0.71 4.71 Within each column, means followed by different letters are significantly different according to the Duncan multiple range test at p≤0.05. Cultivar Ca K Mg Na P NO3 - Violet 415 b 2465 ab 1449 c 51 b 3483 c 2390 a Korolek 722 a 2013 d 1740 ab 48 b 3825 b 2108 b Lakomka 763 a 1284 f 1845 a 53 b 4345 a 2365 a Konditer 720 a 2300 bc 1809 a 34 b 4277 a 1990 bc Konditer 2 739 a 1723 e 1614 b 6 c 3503 c 1876 c Lezhky 797 a 2152 cd 1286 d 61 b 3509 c 2287 a Zolotaya rossip 414 b 2561 a 1708 ab 293 a 3572 c 1181 d Golubkina et al. - Physalis spp. under organic management 545 accumulation, in P. angulata fruits the variability was high in Na concentration (33%) and low in Mg, P and nitrates (11.6, 8.5 and 6.9%). Recently, the element composition of vegetable edible parts has been drawing attention as one of the most important factors affecting human being inges- tion of mineral nutrients. Unfortunately, the few lit- erature reports available do not give the opportunity to perform correct interspecific or varietal compar- isons, due to research carried out under different environmental conditions and species (El-Sheikha et al., 2010; Eken et al., 2014). Referring to recommended dietary allowance val- ues (Institute of Medicine, 2001), the consumption of 300 g fresh Physalis fruits per day results in the inges- tion of 24.8% potassium, 14.4% phosphorous and 12.3% magnesium needed by human organism. The latter benefits from these mineral nutrients in terms of optimization of carbohydrates, protein and lipid metabolism, bone integrity and brain activity, protec- tion against cancer as well as cardiovascular diseases, obesity and diabetes. In this respect, P. angulata and P. pubescens fruits as well as the P. peruviana ones (Zhang et al., 2013) may be considered as good sources of several elements. Antioxidants Polyphenols. In the present research, P. pubescens and P. angulata cultivars growing in the same geo- chemical environment (central Russia) resulted in fruit polyphenols accumulation ranging between 18.7 and 25.1 mg GAE/g d.w. (Fig. 1). Notably, the top concentration detected in the cultivar Violet was 34.2% higher than the lowest level recorded in ‘Korolek’, both belonging to P. angulata species; P. pubescens cultivar Zolotaya rossip ranked third (20.5 mg GAE/g d.w.). Compared to our findings, in previ- ous research (Medina-Medrano et al., 2015) higher phenolic values were detected in the fruits of five Physalis wild species grown in Mexico (32 to 86 mg AGE/g d.w.), with the lowest concentrations record- ed in P. angulata berries. Moreover, P. peruviana fruits produced in Colombia accumulated 400 to 600 mg GAE/g f.w. of polyphenols (Narvaez-Cuenca et al., 2014), but unfortunately this species is not suitable for cultivation in northern Europe (Kondratieva and Engalichev, 2013). Indeed, among natural secondary plant metabolites, polyphenols are considered to be the strongest antioxidants, which are able to inhibit carcinogenesis at initial and development stages, thus suggesting the great importance of their accu- mulation in agricultural plants (Yang et al., 2001). The correlations between polyphenols and total sugars concentrations and between polyphenols and dry matter content were positive and highly signifi- cant (r= 0.99 and r= 0.91, respectively, at P≤0.001). The first one is supposed to reflect the existance of phenolic glycosides, identified as the main phenolics in wild Physalis species (Medina-Medrano et al., 2015). The second correlation explains the higher dry matter and phenolics contents detected in Physalis fruits produced in southern Countries compared to those obtained in central Russia. The high statistical significance of the correlations between the above parameters gives the opportunity to highlight the q u a l i t y p e r f o r m a n c e s o f c u l t i v a r V i o l e t , w h i c h showed the highest concentrations of polyphenols as well as the highest carbohydrates and dry matter content among P. angulata varieties and P. pubes- cens cultivar Zolotaya rossip, with the highest con- tent of dry matter and carbohydrates. These parame- ters may be used in Physalis breeding for increasing fruit nutritional quality. Ascorbic acid. In our research, vitamin C concen- tration in P. angulata cultivars ranged from 0.96 mg/g d.w. (cultivar Violet) to 1.33 mg/g d.w. (cultivar Korolek); however, the lowest value was recorded in the berries of P. pubescens cultivar Zolotaya rossip (Fig. 2). These results show that the synthesis of this antioxidant in Russia is much lower than that report- ed for P. peruviana and P. pubescens in tropical and subtropical areas: i.e. 10 to 30 vs 20 to 50 mg/100 g f.w. (El Sheikha et al., 2008, 2010; Olivares-Tenorio et al., 2016). Indeed, the higher light intensity occurring at lower latitudes enhances ascorbic acid accumula- tion (Bartoli et al., 2006), whereas in previous investi- Fig. 1 - Polyphenol concentration as a function of Physalis culti- var. Means followed by different letters are significantly different according to the Duncan multiple range test at p≤0.05. 546 Adv. Hort. Sci., 2018 32(4): 541-548 gations carried out in Colombia, Kenia and Southern Africa (Fischer et al., 2000), no relationship of this antioxidant with the altitude was found. Moreover, the low vitamin C variability obtained in the present intestigation prove the predominance of environ- mental effects on the genetic one in affecting this antioxidant accumulation in Physalis fruits (Fig. 1). Notably, the outer husk of Physalis fruits is known to prevent ascorbic acid oxidation (Valdenegro et al., 2012) and, despite the relatively low vitamin C con- tent, 100 g of fresh Physalis fruits produced in the northern hemisphere can supply human organism with 14 to 21% of the required vitamin C consump- tion (70 mg per day). Taste Among P. angulata and pubescens cultivars exam- ined, the highest taste index (TI) and nutritional val- ues were recorded in ‘Zolotaya rossip’ (P. pubescens) and ‘Violet’ (P. angulata). As far as taste assessment is concerned, it is a critical point in nonconventional plants produce and, indeed, this determination has never been performed on Physalis fruits up to date. A general approach based on tomato berry testing sug- gests several significant factors affecting taste: dry matter, soluble solids, juice electrical conductivity, carbohydrates and organic acids contents (Adams and Ho, 1989; Clement et al., 2008). In our research, we have assessed that the taste index (TI) used for tomato fruits can be successfully used for Physalis berries. Indeed, the organoleptic analysis and TI approach in evaluating Physalis fruit quality show a good convergence of the results and suggest signifi- cant prospects of TI utilization in determining new varieties quality (Fig. 3). In this respect, several correlations arose between the taste index and the following quality parameters of Physalis fruits: total sugar content (r=+0.98; P<0.001), dry matter (r = +0.92; P<0.001), polyphenol content (r= +0.96; P<0.001); calcium (r= -0.91; P<0.001). Notably, the two latter correlations had never been reported previously, neither in Physalis nor in tomato. 4. Conclusions The present research, carried out in central Russia, allowed to assess interspecies and varietal differences in yield and quality characteristics of P. angulata and P. pubescens fruits grown under organ- ic management. In this respect, this investigation provided with interesting clues, mainly concerning the nutritional and antioxidant properties of the cul- tivars tested and their growing prospects by organic farming procedures in northern Europe. The variabili- ty of biologically active compounds, macroelement content and Taste Index, as well as their significant correlations may serve as the basis for enhancing the high potential of the Physalis varieties examined for functional food production. Acknowledgements We would like to thank Dr. M. Mamedov for his effective help with the research team arrangement. Fig. 2 - Ascorbic acid concentration as a function of Physalis cul- tivar. 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