combined effect of silicon and non-thermal plasma

Plant Physiology and Biochemistry 166 (2021) 1014–1021

Available online 11 July 20210981-9428/© 2021 Elsevier Masson SAS. All rights reserved.

Combined effect of silicon and non-thermal plasma treatments on yield, mineral content, and nutraceutical proprieties of edible flowers of Begonia cucullata

Silvia Traversari a,*, Laura Pistelli b,c, Bianca Del Ministro a, Sonia Cacini a, Giulia Costamagna d, Marco Ginepro d, Ilaria Marchioni b, Alessandro Orlandini a, Daniele Massa a

a CREA Research Centre for Vegetable and Ornamental Crops, Via dei Fiori 8, 51017, Pescia (PT), Italy b Department of Agriculture, Food and Agro-environment, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy c Interdepartmental Research Center Nutraceuticals and Food for Health (NUTRAFOOD), University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy d Dipartimento di Chimica, Universita di Torino, Via P. Giuria 5, 10125, Torino, Italy

A R T I C L E I N F O

Keywords: Antioxidant activity Begonia semperflorens Comestible blooms Flower colour Ionomics Water sanitization

A B S T R A C T

Edible flowers are becoming popular as a nutraceutical and functional food that can contribute to human nutrition with high antioxidant molecules and mineral elements. While comparative studies between different flower species have been performed, less is known about the best agronomical practices to increase yield and nutraceutical proprieties of blooms. Silicon stimulates plant resistance against stress and promotes plant growth while non-thermal plasma (NTP) technology has been applied for the disinfection and decontamination of water, as well as for increasing plant production and quality. The application of silicon and NTP technology through nutrient solution and spraying was investigated in edible flowers given that the combination of these treatments may play a role in promoting their nutritional and nutraceutical proprieties. The treatments were applied on two varieties of Begonia cucullata Willd. (white and red flowers) to explore their effects on different flower pig-mentations. Plants with red flowers showed higher nutraceutical proprieties than the white ones but yielded a lower flower number. While the NTP treatment did not improve flower yield and quality, the silicon treatment increased anthocyanins and dry weight percentage in red flowers. NTP treatment increased zinc concentration, while it decreased potassium, magnesium, and manganese, and increased silicon concentration in white flowers. The combination of silicon and NTP showed negative effects on some nutraceutical proprieties of red flowers thus highlighting that the two treatments cannot be combined in edible flower production. In conclusion, the positive effect of silicon use in edible flower production has been demonstrated while the NTP technology showed contrasting results and its use should be explored in greater depth, including a consideration of its role in biotic attack prevention and reduced chemical input.

1. Introduction

Edible flowers of ornamental plants have been widely employed for cooking for hundreds of years but recently there has been an increasing interest in the use of flowers in food preparation as a source of many beneficial chemical compounds and related nutraceutical proprieties (Fernandes et al., 2017; Lu et al., 2016; Marchioni et al., 2020). Comestible blooms also provide essential mineral elements and vita-mins, such as carotenoids (Drava et al., 2020; Gonzalez-Barrio et al., 2018). Moreover, they present bioactive compounds, like phenols, with

an antioxidant activity that show an inhibitive effect on free radicals, such as reactive oxygen species (ROS) and reactive nitrogen species (RNS), thus avoiding damage to DNA, proteins, lipids, and enzymes (Chen et al., 2018; Mlcek and Rop, 2011). Edible flowers have different phenolic composition and bioactive potential depending on the plant species (Najar et al., 2019; Pires et al., 2018) and peculiar characteristics such as their colour (Benvenuti et al., 2016). In particular, flower colour is principally determined by anthocyanin pigments and these molecules also have a strong antioxidant activity in addition to other beneficial properties (De Pascual-Teresa and Sanchez-Ballesta, 2008). Among the

* Corresponding author. E-mail address: [email protected] (S. Traversari).

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journal homepage: www.elsevier.com/locate/plaphy

https://doi.org/10.1016/j.plaphy.2021.07.012 Received 18 November 2020; Received in revised form 21 June 2021; Accepted 10 July 2021


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species with edible flowers, Begonia cucullata Willd. (synonym of B. semperflorens Link & Otto) is commonly used as an ornamental plant and its blooms have a high content of total polyphenols and flavonoids (Kwon et al., 2019).

Many experimental assays have been carried out with the aim of improving produce yield and quality of edible flowers, including the application of agronomical practices (Lim, 2014), exogenous eustressors like saline ions (Chrysargyris et al., 2018), and beneficial nutrient ele-ments like Silicon (Si) (Savvas and Ntatsi, 2015). In particular, Si is the second most abundant element in soil, but it is mostly present in the solid phase while in the liquid phase it occurs mainly as monomeric, oligomeric, or polymeric acid (Tubana and Heckman, 2015). The monosilicic acid (H4SiO4) is the plant bioavailable form and if used in fertilizers can have a concentration up to 2 mM in soil solution at pH less than 9: a higher concentration results in an increase of polysilicic acids that are not available for plant nutrition (Mandlik et al., 2020; Mat-ichencov and Bocharnikova, 2001). Following the criteria proposed by Arnon and Stout (1939), Si is not considered as an essential element for higher plants. However, new insights suggest that Si plays an important role as a beneficial element by alleviating both abiotic and biotic stresses, such as drought, lodging, salinity, freezing, nutrient imbalance, heavy metal excess, or pests and diseases (Liang et al., 2007; Ma, 2015; Ma and Yamaji, 2008). Moreover, Si promotes plant growth and yield as well as the production of antioxidants and enzymes for the detoxifica-tion from free radicals such as ROS (Mandlik et al., 2020; Zargar et al., 2019). Therefore, its use in the horticultural crop sector is receiving more attention, including for flower production (Savvas and Ntatsi, 2015; Vasanthi et al., 2014).

Non-Thermal Plasma (NTP) technology is based on the production of plasma, an ionized gas with a significant number of energetic electrons, free radicals, excited species, and photons, that is far from the equilib-rium state and therefore can be used at room temperature (Zhang et al., 2017). Among several applications, this technology could be applied in the horticultural sector to treat the irrigation water. The NTP-treated water contains ROS and RNS that can be beneficial or harmful for plants, depending on their amount (Cui et al., 2019). Even though an excess of ROS and RNS can trigger negative effects on plant health, a small amount has positive effects on cellular proliferation and differ-entiation, and it also supports essential cellular processes (Mittler, 2017), such as the activation of antioxidant responses associated with the abiotic and biotic stress resistance (Hossain et al., 2015; Perez and Brown, 2014). Indeed, Arabidopsis plants irrigated with NTP-treated water showed an increase in yield, seed germination, plant tolerance to dehydration, number of seeds and flowers while there was a reduction in water consumption (Brar et al., 2016; Cui et al., 2019; Peethambaran et al., 2015), thus supporting the beneficial effect of small amounts of ROS and RNS in water following the NTP treatment. Some signalling molecules involved in the response to oxidative stress, such as H2S, have also been found improving the biostimulant effect of Si (Rai et al., 2021), which would support the idea that the action of Si under NTP applica-tion can be more effective. The NTP technology is commonly used for the sanitization of irrigation water to eliminate the presence of patho-genic microorganisms, such as Aspergillus spp. and Penicillium spp. (Panngom et al., 2014). The production of edible flowers with zero chemical residues is indeed a challenge for farmers (Matyjaszczyk and Smiechowska, 2019), therefore the disinfection effect obtained by NTP treatments in the cultivation environment (Scholtz et al., 2015) might represent a strategy that is worth exploring to prevent the use of chemicals in this sector and avoid the presence of microbiological im-purities. The use of NTP-treated water allows the removal of contami-nants from water as well, such as pesticides or pharmaceutical compounds (Magureanu et al., 2015; Vanraes et al., 2017). Therefore, the application of NTP treatment on edible flower species might be a way to increase produce yield and quality, including through the pro-duction of beneficial compounds with antioxidant proprieties, as well as reducing the use of pesticides and microbiological impurities.

The aim of this work was to evaluate the application of both Si fertilization and NTP technology for increasing the yield and nutra-ceutical proprieties of the edible flowers of B. cucullata. Moreover, the effect of such treatment on flower pigmentation was also explored further using two different varieties with white and red blooms.

2. Materials and methods

2.1. Plant material, treatments and growing conditions

Two varieties of Begonia cucullata Willd., with white and red flowers, were selected for the trial (n = 240 per variety). Plants were trans-planted on April 23, 2019, into 1.5 L pots (∅ 14 cm) filled with peat and placed on benches for pot cultivation (10 plants m−2) inside a green-house. Plants were fed with nutrient solution by a drip irrigation system with a flow rate of 2 L h−1. Plants were maintained in the same exper-imental greenhouse described by Cannazzaro et al. (2021), located at CREA Research Centre for Vegetable and Ornamental Crops in Pescia, Tuscany, Italy (lat. 43◦54′ N, long. 10◦42′ E). This greenhouse is equipped with NTP technology to treat the irrigation water. The low temperature plasma was generated by a Dielectric Barrier Discharge device (Jonix srl, Tribano, PD, Italy) set to 5–25 kV thereby producing 1012–1015 charged molecules cm−3.

After the transplant, plants were randomly divided in 12 blocks of 20 plants for each variety (3 blocks, i.e., replicates per treatment). Treat-ments started one week after transplant and can be summarised in three main procedures: I) plants were fed with a nutrient solution continu-ously treated with NTP before irrigation and sprayed on the canopy, twice a week, with deionized water pre-treated by NTP; II) plants were fed with a nutrient solution containing 2 mM Si and sprayed on the canopy, twice a week, with deionized water containing 2 mM Si; and III) the combination of I) and II). Control plants were fed with the basic nutrient solution and sprayed with distilled water alone. In the NTP treatments, the nutrient solution was prepared by a fertigation unit and stocked in a tank with a capacity of 1 m3 where 0.5 m3 of nutrient so-lution was continuously treated by bubbling NTP-treated air into the solution. In the same treatment types, the deionized water used for spraying the canopy was treated just before application, until a pre- established redox potential threshold of 800 mV was achieved. In the Si treatments, 2 mM of K2SiO3 was added in the nutrient solution while an equivalent concentration of potassium (K) was obtained in the con-trol solution using K2SO4. With this expedient, control and Si-enriched nutrient solution had the same K concentration and K:Ca:Mg ratio as suggested by other authors (Costan et al., 2020). Either K2SiO3 or K2SO4 were added to the following basic nutritive recipe: N-NO3 6.4 mmol L−1, N-NH4 0.8 mmol L−1, P-PO4 0.8 mmol L−1, K 4 mmol L−1, Ca 1.8 mmol L−1, Mg 0.4 mmol L−1, Na 0.5 mmol L−1, S-SO4 1.03 mmol L−1, Cl 0.5 mmol L−1, Fe 16 μmol L−1, B 12 μmol L−1, Cu 0.4 μmol L−1, Zn 3.5 μmol L−1, Mn 2 μmol L−1, Mo 0.5 μmol L−1. The pH was adjusted at 5.5 using H2SO4. Four different treatments were then applied: 1) untreated stan-dard nutrient solution and canopy spray with deionized water alone (Control); 2) NTP-treated nutrient solution and canopy spray, as described in the abovementioned procedure I (NTP); 3) Si enriched nutrient solution and canopy spray, as described in the abovementioned procedure II (Si); and 4) NTP treated + Si enriched nutrient solution and canopy spray, as described in the abovementioned procedure III (NTP +Si).

Climate parameters were monitored by meteorological sensors positioned in the cultivation area and recorded on a 5-min basis. During the treatment period, the minimum, mean, and maximum daily- averaged PAR were 125.0, 233.8, and 395.0 μmol m−2 s−1, respec-tively, with a mean daily-cumulated global radiation of 14.2 MJ m−2

s−1. The minimum, mean, and maximum daily-averaged air tempera-tures were 15.5, 21.8, and 26.8 ◦C, respectively. The air’s mean daily relative humidity averaged 61.8%.

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2.2. Plant sampling

Mature flowers were harvested once a week during the cultivation, starting from two weeks after the onset of treatment until the end of the experiment (5 harvests in total). Flower fresh weight (FW) was deter-mined at each sampling while flower dry weight (DW) was determined at the end of the cultivation on a sub-sample of 50 flowers for all rep-licates (65 ◦C until constant weight). Single flower weight was deter-mined as the mean of three harvests (1st, 2nd, and 5th) on counted blooms and used for the calculation of total flower number. One week before the experiment end (8 weeks after treatment initiation), the leaf chlorophyll (namely SPAD units) was measured using a SPAD-502 (Konica Minolta, Chiyoda, Japan) by averaging 3 measures (bottom, middle, and top leaves) on 10 plants per replicate. Flower disks (∅ 5 mm) were then sampled, weighted, and stored at −80 ◦C for the quan-tification of pigments (chlorophyll a, b, carotenoids, phenols) and an-thocyanins. The dried samples were grinded in a mill and the powder was used for the quantification of mineral elements. The remaining flowers were stored at −80 ◦C for total polyphenols, antioxidant activity, and ascorbic acid analyses. All plants were harvested, weighed to determine the total FW biomass, and 5 plants per replicate were further used for the shoot FW and DW measures.

2.3. Pigments and antioxidant activity measures

Chlorophyll a, b, carotenoids, and total phenols were extracted from flower disk samples (100 mg FW) in two technical replicates for each biological replicate with MeOH (0.1 ml mg−1 FW) keeping the samples 2 days at −20 ◦C and renewing the solution after 1 day. The extracts were measured using a spectrophotometer (Evolution™ 300 UV–Vis Spec-trophotometer, Thermo Fisher Scientific Inc., MA, USA) and pigment concentrations were obtained following the procedure reported by Lichtenthaler and Buschmann (2001) using the following formulas:

Chlorophyll a (μg ml−1) = 16.72 × A665.2–9.16 × A652.4 Chlorophyll b (μg ml−1) = 34.09 × A652.4–15.28 × A665.2 Carotenoids (μg ml−1) = (1000 × A470 – 1.63 × chlorophyll a – 104.96 × chlorophyll b)/221.

Data were finally expressed on a FW basis. Total phenols (A320 g−1 FW) were determined directly measuring the

extracts at 320 nm (Maggini et al., 2018). Anthocyanins were extracted from flower disk samples (100 mg FW)

in two technical replicates using a mixture 80:17.7:2.3 v/v/v of MeOH: dH2O:37%HCl (0.1 ml mg−1 FW) keeping the samples 2 days at −20 ◦C and renewing the solution after 1 day, following the procedure reported by Hradzina et al. (1982). Anthocyanin concentration was measured at 530 nm by a spectrophotometer comparing the absorbance against a calibration curve with Cyanidin 3-galactoside chloride (Merck KGaA, Darmstadt, Germany).

Two technical replicates of frozen flower samples (200 mg FW) were homogenized in a mortar with 2 ml of cold 70% MeOH and centrifuged at 14,000 rpm for 10 min at 20 ◦C. The supernatant was used for the quantification of total polyphenols, following the procedure reported by Bretzel et al. (2014), as well as the quantification of antioxidant activity. Briefly, the total polyphenols were quantified following the Folin-Ciocalteau procedure using a Gallic acid calibration curve, while the antioxidant activity was determined using the DPPH (2,2-diphe-nyl-1-picryl-hydrazyl-hydrate) assay that is based on a colorimetric re-action comparing the absorbance at 517 nm against a calibration curve with Trolox (Merck KGaA, Darmstadt, Germany).

Ascorbic acid was determined following the procedure reported by Wang et al. (1991) on frozen flower samples (1.5 mg FW) homogenized in 3 ml of cold 5% (w/v) trichloroacetic acid, comparing the absorbance at 534 nm against a calibration curve with L-ascorbic acid (Merck KGaA, Darmstadt, Germany).

2.4. Quantification of mineral elements

Si, K, Ca, Mg, P, Fe, Mn, and Zn were quantified by ICP-OES analysis (Optima 7000, PerkinElmer, Waltham, MA, USA). Flower samples (0.4 g DW) were mineralized using 9 ml HNO3 and 1 ml H2O2 in Teflon vessels with a high-performance microwave digestion system (Ethos Up, Mile-stone, Sorisole, BG, Italy) for 45 min at 800 W. At the end of the mineralization process, the acid solution was diluted to 50 ml in plastic material containers and forthwith analysed. Si was also determined using the fusion process. As a first step, flower samples (0.4 g DW) were burnt down in a muffle at 550 ◦C for 12 h. Mixing 0.2 g of lithium metaborate, the ashes were digested throughout fusion process in a graphite melting pot at 900 ◦C for 30 min. The resulting samples were put in contact with a 50 ml 10% (w/v) HNO3 solution, dissolved, and analysed by ICP-OES technique. These two different methods for Si determination achieved very similar results. For both protocols, the analyses were opportunely verified through standard addition method. Si content was stated as a weighted average result of these two analytical methods. The Si concentration in irrigation water was 1.65 mg L−1.

Nitrates were quantified by nitration of salicylic acid using the pro-cedure reported by Cataldo et al. (1975) comparing the absorbance at 410 nm against a calibration curve obtained with a 1000 ppm nitrate standard solution (Merck KGaA, Darmstadt, Germany).

2.5. Experimental design and statistics

The experiment was carried out in a complete randomized block design. Data were tested for normal distribution using the Shapiro-Wilk normality test and eventually transformed before the ANOVA. Data were analysed with a three-way ANOVA (Si, NTP, and variety as variables) and then with a two-way ANOVA and a Tukey’s post-hoc test (Si and NTP as variables) to assess significant differences (P ≤ 0.05, 0.01, and 0.001). The statistical analyses and graphs were performed with Prism 8 (GraphPad Software, Inc., La Jolla, CA, USA).

3. Results

3.1. Growth parameters

Plant biomass parameters are reported in Table 1. The plants with white flowers had a two-fold higher flower number per plant and, consequently, a higher flower FW in comparison with the red ones (on average + 59 and 28% in control plants, respectively). On the other hand, red begonias had bigger flowers than the white ones (on average + 78%, single flower FW). However, no difference in flower %DW be-tween the two varieties was observed. The NTP treatment increased the single flower FW in the white variety, while Si treatment decreased this parameter in red begonia despite the flower %DW significantly increased.

The red flower variety showed a higher shoot DW biomass in com-parison with the white variety (on average + 18% in control plants, respectively). Si and NTP treatments did not influence shoot DW in both white and red begonias. More interestingly, under NTP treatment, an increase in SPAD units was measured mostly in begonia plants with white flowers.

3.2. Flower concentrations of pigments, nitrates, and mineral elements

The pigment quantification in flowers (Table 2) showed that the chlorophyll a + b content was two-fold higher in NTP treated plants than in control ones. On the contrary, the carotenoid content significantly decreased under NTP treatment in red begonia flowers while caroten-oids were undetected in white begonia flowers. The decrease in carot-enoids in red begonia was mostly recorded under Si + NTP treatment (on average – 78% than control plants). Total phenols exhibited a high variability in white begonia flowers while a low variability was recorded



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in red begonia flowers where the total phenol concentration was lower than in the white varieties. Nitrate concentration (Table 2) was higher in red begonia flowers than in the white ones (on average + 7 mg kg−1 in control plants) and it did not show any variation due to the NTP or Si treatment. Silicon concentration (Fig. 1A) strongly increased under Si and Si + NTP treatments and was three-fold higher than in control flowers in both white and red varieties (+ 66 and 74 mg kg−1 under Si treatment, + 65 and 58 mg kg−1 under Si + NTP treatment, respec-tively). Moreover, Si concentration was also higher than in control flowers under NTP treatment alone in white begonia (+ 19 mg kg−1). Overall, NTP treatment decreased K, Mg, and Mn concentrations (Fig. 1B, D, H) while it increased Zn concentration (Fig. 1G) within both white and red flowers.

3.3. Antioxidant properties of flowers

The total polyphenol content (Fig. 2A) was higher in red begonia flowers than in the white variety (on average + 1114 μg GAE g−1 FW in control plants). The total polyphenols were affected by NTP treatment in the red flowers and the lowest concentration was measured under NTP treatment alone (on average – 42% than in control plants). The antho-cyanin content (Fig. 2B) was negligible in white begonia flowers. On the contrary, it was high in red begonia flowers (on average + 874 μg cyanidin 3-glucoside g−1 FW than white flowers in control plants) and it strongly increased under Si treatment alone in comparison with the control plants (+ 70%). Instead, the Si + NTP treatment halved the anthocyanin content in red flowers (− 50% than control plants). DPPH activity (Fig. 2C) was more than two-fold in red flowers than in the white ones (on average + 1681 μmol Trolox eq g−1 FW in control plants) and it was affected by NTP treatment alone in red begonia flowers where a slight decrease in antioxidant activity was measured (− 8% than control plants). Finally, ascorbic acid (Fig. 2D) was higher in red flowers, particularly when NTP treatment was not applied. NTP treatment slightly increased ascorbic acid concentration within white flowers (+3%, on average).

4. Discussion

The increasing use of edible flowers in human diet focuses the attention on the best agronomical practices to guarantee both flower yield, in terms of dimension and number, and high nutraceutical pro-prieties. In this work, the suitability of B. cucullata for edible flower production has been highlighted for its greater productivity and high concentration of beneficial compounds in blooms. In control conditions, the white and red varieties showed contrasting features: the white one produced more but smaller flowers than the red one. Indeed, a high level of diversity between Begonia species and clones is well documented (Hvoslef-Eide and Munster, 2007). Since the selling price of edible flowers is based on flower number rather than weight (Fernandes et al., 2020), white begonia showed more advantages in terms of producer income. However, edible blooms are also marketed in a dried form to prolong the shelf life despite the reduction of nutraceutical proprieties, particularly using natural or hot air drying (Zhao et al., 2019).

The role of Si in plant cells has been widely debated. Currently, it is recognized as a beneficial element acting as a mechanical barrier against stress and has been proved to enhance nutrient uptake (Mandlik et al., 2020). Silicon increased the flower %DW of red begonia while it did not show effects on the white variety. Indeed, plant response to Si may vary among different application methods and plant species or varieties showing either differences or any variations in the accumulation of biomass (Mattson and Leatherwood, 2010; Savvas et al., 2015). The different response observed between red and white begonias in terms of flower DW probably arose from the different biomass accumulation rate and partitioning of photoassimilates into aerial organs. The red begonia, which showed a lower flower/shoot DW ratio (data not shown), benefited from Si treatment to a greater extent than the white variety. Similarly, Mattson and Leatherwood (2010) reported contrasting results in the flower morphological traits of two varieties of Calibrachoa sup-plemented with Si.

Two main impurities, bacteria and chemical compounds, can occur in edible flowers with non-organic cultivation (Matyjaszczyk and

Table 1 Plant growth parameters of begonia plants with white (W) and red (R) flowers after 6 weeks of treatment with Si, NTP, or Si + NTP. Values represent the mean of 3 replicates of 20 plants ± SD. Two-way ANOVA (Si and NTP factors) and three-way ANOVA (variety factor) P values are reported in the table (ns, not significant; *P ≤0.05; **P ≤ 0.01; ***P ≤ 0.001).

Control Si NTP NTP + Si Si NTP Si × NTP Variety

Flower number (n plant−1) W 281 ± 14.6 272 ± 31.6 260 ± 40.2 236 ± 21.9 ns ns ns *** R 115 ± 10.0 126 ± 7.8 119 ± 17.5 122 ± 5.5 ns ns ns

Flower FW (g plant−1) W 107 ± 5.7 105 ± 9.9 110 ± 16.3 103 ± 7.1 ns ns ns *** R 78 ± 4.6 78 ± 3.2 78 ± 10.5 76 ± 3.8 ns ns ns

Single flower FW (g flower−1) W 0.38 ± 0.001 0.39 ± 0.015 0.42 ± 0.006 0.44 ± 0.015 ns *** ns *** R 0.68 ± 0.020 0.62 ± 0.031 0.65 ± 0.015 0.62 ± 0.021 ** ns ns

Flower % DW W 3.7 ± 0.20 3.6 ± 0.21 4.1 ± 0.16 3.7 ± 0.39 ns ns ns ns R 3.6 ± 0.14 3.9 ± 0.14 3.5 ± 0.07 4.2 ± 0.21 *** ns ns

Shoot DW (g plant−1) W 27 ± 1.9 25 ± 2.0 31 ± 6.0 27 ± 4.2 ns ns ns * R 33 ± 3.0 28 ± 4.2 33 ± 2.0 31 ± 1.5 ns ns ns

Leaf SPAD W 44 ± 2.2 43 ± 1.0 49 ± 0.7 47 ± 0.8 ns *** ns *** R 37 ± 0.7 38 ± 0.4 39 ± 1.7 39 ± 1.4 ns * ns

Table 2 Concentrations of pigments and nitrates within the edible blooms of begonia plants with white (W) and red (R) flowers after 6 weeks of treatment with Si, NTP, or Si +NTP. Values represent the mean of 3 replicates of 20 plants ± SD. Two-way ANOVA (Si and NTP factors) and three-way ANOVA (variety factor) P values are reported in the table (nd, not detected; ns, not significant; *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001).

Control Si NTP NTP + Si Si NTP Si × NTP Variety

Chl a + b (μg g−1 FW) W 3.4 ± 1.20 4.2 ± 2.28 7.7 ± 2.16 9.0 ± 1.50 ns *** ns *** R 7.0 ± 1.16 b 12.0 ± 1.42 ab 15.1 ± 3.83 a 14.1 ± 3.56 a ns ** *

Carotenoids (μg g−1 FW) W nd nd nd nd – – – – R 76 ± 12.2 a 77 ± 22.2 a 51 ± 7.1 b 17 ± 9.0 c ** *** **

Total phenols (А320 g−1 FW) W 11.1 ± 2.87 8.35 ± 1.31 9.6 ± 3.55 9.9 ± 2.79 ns ns ns *** R 5.7 ± 1.62 6.0 ± 1.96 6.0 ± 0.65 3.8 ± 0.61 ns ns *

Nitrates (mg kg−1 DW) W 17.1 ± 0.64 18.4 ± 2.74 19.5 ± 4.94 14.8 ± 2.95 ns ns ns *** R 24.1 ± 5.51 25.1 ± 1.60 23.4 ± 3.17 25.3 ± 2.11 ns ns ns



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Fig. 1. Silicon (A), potassium (B), calcium (C), magnesium (D), phosphorus (E), iron (F), zinc (G), and manganese (H) concentrations within the edible blooms of begonia plants with white and red flowers after 6 weeks of treatment with Si, NTP, or Si + NTP. Values represent the mean of 3 replicates of 20 plants + SD. Two-way ANOVA (Si and NTP factors) and three-way ANOVA (variety factor) P values are reported in the figure (ns, not significant; *P ≤ 0.05; **P ≤ 0.01; ***P ≤ 0.001). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 2. Total polyphenols (A), anthocyanins (B), DPPH activity (C), and ascorbic acid (D) within the edible blooms of begonia plants with white and red flowers after 8 weeks of treatment with Si, NTP, or Si + NTP. Values represent the mean of 3 replicates of 20 plants + SD. Two-way ANOVA (Si and NTP factors) and three-way ANOVA (variety factor) P values are reported in the figure (ns, not significant; *P ≤ 0.05; ***P ≤ 0.001). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)



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Smiechowska, 2019); therefore, the use of NTP treatment on water used for irrigation and spraying might be a successful strategy to preserve edible flower integrity. However, in our experiment, no bacterial or fungal diseases were reported and therefore an evaluation of NTP treatment role in preventing plant damages in terms of flower losses under a biotic attack cannot be estimated and further analyses are required. On the other hand, Si also has an important role in alleviating biotic attacks (Bakhat et al., 2018) and in our experimental conditions, in addition to the increase in red flower %DW, it showed a positive effect on nutraceutical properties of the flowers.

The NTP treatment strongly decreased the carotenoid content in red flowers, both alone and in combination with Si treatment, while also, on the contrary, increasing the Chl a + b content in the white flowers as well as the SPAD units in leaves. This increase might be due to the antioxidant function of chlorophyll and its derivatives in protecting against the oxidative stress and, particularly, the lipid peroxidation (Lanfer-Marquez et al., 2005) driven by the ROS and RNS application through the NTP-treated water. The increase of chemical compounds with antioxidant activity in edible flowers is a valuable challenge in ornamental plant sector that encourage the production of nutraceutical and functional foods (Mlcek and Rop, 2011; Takahashi et al., 2020). Antioxidant molecules, which are naturally present in food, have a fundamental role against the oxidative damage associated with, for example, cancer and neurodegenerative and cardiovascular diseases (Ali et al., 2020). In particular, B. semperflorens contains flavonoids, with a pharmaceutical activity (i.e., quercetin, kaempferol, astragalin, and isoquercetin), which have a protective role against oxidative stress in human beings (Kwon et al., 2019). The antioxidant capacity of both red and white flowers was very high compared with other air-dried edible flowers (Zheng et al., 2018), despite the water weight in fresh mass, suggesting the importance of fresh storage in edible flower markets. The level of antioxidant activity depended on flower colour and, specifically, red begonia flowers had a higher antioxidant capacity than white ones. The greatest antioxidant activity has already been found to correlate with higher anthocyanin content (Benvenuti et al., 2016); accordingly, in red begonia flowers the anthocyanins were about 90 times higher than in the white ones. Moreover, in our experimental conditions, anthocyanin concentration in red flowers was even higher than that reported by other authors (Benvenuti et al., 2016). Higher levels of both anthocyanins and antioxidant activity have also been reported in red dahlia flowers, as compared with white ones (Espejel et al., 2019). An-thocyanins are valuable molecules for functional food production as they have antioxidant, anti-inflammatory, and anti-apoptotic effects (Speer et al., 2020). Total polyphenol content was also higher in the red variety and the concentration was similar to that reported in pink begonia flowers (Chensom et al., 2019). Since the long-term consump-tion of plant polyphenols has been shown to confer protection from several age-related chronic diseases, such as cancers, cardiovascular and neurodegenerative diseases, diabetes, and osteoporosis, the red flowers showed notable nutraceutical traits (Debelo et al., 2020; Pandey et al., 2009). In addition, carotenoid concentration was higher in red flowers, reflecting a further increase in their valuable proprieties due to their positive healthy effects for both prevention and treatment of human diseases (Villa-Rivera et al., 2020). Finally, ascorbic acid was also higher in red flowers and the concentration measured in white blooms was in agreement with that found by Grzeszczuk et al. (2016) in B. semperflorens flowers of the same colour. Given that phytochemicals in edible flowers have been shown to have antioxidant, anti-inflammatory, anticancer, anti-diabetic, and cardio-protective ac-tivities (Janarny et al., 2021), all these results highlighted the better nutraceutical proprieties of red begonia flowers compared with the white ones, suggesting their preferential use in functional food production.

Anthocyanin concentration further increased under Si treatment alone in red begonias highlighting the utility of this treatment to enhance the beneficial proprieties of red flowers. Similar results have

been reported for anthocyanin concentration in two oat varieties treated with Si spraying (Wahed et al., 2019). However, under the combined NTP and Si treatment, the anthocyanin concentration was lower than in control red flowers, a decrease not reported under NTP treatment alone. Therefore, the combination of both treatments negatively affected the anthocyanin content. Moreover, NTP and Si together also decreased the carotenoids and total phenols, indicating that this combination of treatments is not suitable for increasing red flower nutraceutical properties.

Among the positive proprieties of edible flowers, their use as a source of mineral elements has also been noted mostly for P and K contents (Rop et al., 2012). In particular, in our experimental conditions, begonia flowers showed high concentrations of K, Ca, Mg, Fe, Mn, and Zn compared to other ornamental flowers, such as snapdragon, dianthus, and peony (Grzeszczuk et al., 2018). The Si treatment strongly increased the Si concentration within the flowers without influencing other nutrient concentrations. The Si increase could also enhance the nutra-ceutical proprieties of edible blossoms for its health-related effects on bone, connective, and neural tissues as well as immune or inflammatory responses in human beings (Nielsen, 2014). To this purpose, the present work confirms the key role of fertigation techniques and canopy fertil-ization in the biofortification of edible plants.

Interestingly, Si content was also enhanced by NTP treatment alone in comparison with the control conditions, which was not previously investigated in other studies to the best of our knowledge. Similarly, NTP treated plants showed higher Zn content in edible flowers. Certainly, Zn is an important element in the human diet and many people in various developing countries suffer Zn deficiency and related health outcomes; a higher intake of Zn does indeed have positive effects on human health, especially when facing cancer diseases, and therefore biofortification approaches are widely reported in relation to this issue, mostly in wheat (Bhatt et al., 2020). Conversely, NTP treatment decreased K, Mg, and Mn concentrations, mostly in white flowers. These alterations could highlight a possible effect of NTP treatment on the bioavailability of certain elements within the nutrient solution, espe-cially those that are administered by chelated fertilizers, as in the case of Mn. Additionally, an influence of NTP treatment on mineral element assimilation cannot be excluded. Other authors observed higher syner-gisms between the accumulation of K, Mg, and Mn in relation to Zn in tomato fruits (Dannehl et al., 2014). However, the almost complete lack in the literature about the effect of NTP on ornamental plant production does not allow further discussion of this aspect, therefore studies on the interaction between NTP and plant nutrition and irrigation are neces-sary. Nitrates are rarely investigated in the characterization of edible flowers while these molecules are harmful for human beings if present in excess in the daily diet (Santamaria, 2006). Both red and white begonia varieties showed level of nitrates below the thresholds established, for example, for leafy vegetables in Europe (EFSA, 2008; European Com-mission, 2011) and NTP and Si treatments did not increase these molecules.

5. Conclusion

Red begonia flowers showed enhanced nutraceutical proprieties, but they were a lower number per plant compared with white flowers. Several biochemical aspects have been evaluated to assess the possible influence of Si and NTP treatments on the nutritional and nutraceutical profile of begonia. Silicon treatment increased anthocyanin content without affecting flower yield and number, highlighting its suitability in agronomical practices for improving edible flower productions. More-over, it also increased Si flower content that can be beneficial for human beings as well. The above findings concerned the strategic role of fer-tigation practices in the biofortification of edible plants. Besides the literature, in our experimental conditions, NTP treatment did not show desirable effects on yield improvement and nutraceutical flower pro-prieties but influenced the nutritional profile by increasing Zn and Si



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contents in edible flowers. The combination of Si and NTP had negative effects on some nutraceutical proprieties of red flowers thereby revealing a lack of synergy between these treatments for functional food production. The protective role of NTP treatment under biotic stress occurrences remains to be deepened while also considering its role in substituting chemical inputs on food crops. Moreover, given the current necessity to explore new post-harvest technologies for edible flower production, the role of NTP and Si in increasing the shelf-life of blooms should be investigated.

Author contributions

Work conceptualization and hypothesis, DM, SC and LP; methodol-ogy, DM, SC and ST; greenhouse experiment management, sampling and data acquisition, SC, BDM and AO; laboratory analysis, MG, GC, IM, BDM, ST; data elaboration and statistics, ST, DM; writing-original draft preparation ST, DM; manuscript final revision and editing, ST, DM, SC, IM, LP, GC, MG; project administration and funding acquisition, DM and LP; supervision and coordination, DM and SC. All authors have read and agreed to the final version of the manuscript.

Declaration of competing interest

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

Acknowledgments

This research was partly funded by the INTERREG-ALCOTRA UE 2014–2020 Project “ANTEA” Attivita innovative per lo sviluppo della filiera transfrontaliera del fiore edule (n. 1139), grant number CUP C12F17000080003. This research was also partly supported by the POR- FESR project High-Tech House Garden (HT-HG), funded by the Tuscany Region (Italy) under “Bandi POR FESR 2014–2020, Bando 2” (Decree n. 5906, 20 November 2015).

The authors wish to thank Azienda Agricola Carmazzi, Torre del Lago Puccini, Lucca, Italy, for supplying begonia plants.

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