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Article

The Impact of the Growing Substrate on Morphological and Biochemical Features of Salicornia europaea L.

by
Carmen Gabriela Constantin
1,
Mihaela Maria Zugravu
1,
Mihaela Georgescu
2,
Mugurași Florin Constantin
1,
Andrei Moț
1,
Maria Paraschiv
3,4 and
Aurora Dobrin
1,*
1
Research Center for Studies of Food Quality and Agricultural Products, University of Agronomic Sciences and Veterinary Medicine of Bucharest, 011464 București, Romania
2
Faculty of Horticulture, University of Agronomic Sciences and Veterinary Medicine of Bucharest, 011464 București, Romania
3
National Institute of R&D for Biological Sciences, 060031 București, Romania
4
Research Center for Advanced Materials, Products and Processes, University POLITEHNICA of Bucharest, 060042 Bucharest, Romania
*
Author to whom correspondence should be addressed.
Appl. Sci. 2023, 13(19), 10835; https://doi.org/10.3390/app131910835
Submission received: 23 August 2023 / Revised: 14 September 2023 / Accepted: 25 September 2023 / Published: 29 September 2023
(This article belongs to the Section Agricultural Science and Technology)
Browse Figures
Versions Notes

Abstract

:
Nowadays, intensive agriculture correlated with the impact of climate change has led to nutrient soil depletion and the salinization of agricultural lands, making them unsuitable for conventional agricultural crops, with a direct impact on the food industry. Therefore, it is necessary to find sustainable alternative solutions that satisfy the needs of both consumers and food production. One such solution may be represented by salt-tolerant species that can fulfill food requirements. One of the most promising salt-tolerant plant species that can be used is Salicornia europaea L. The present work was conducted in greenhouse conditions, and the adaptability of the species on different cultivation substrates was investigated by means of monitoring the plant indicators such as cuticle, epidermis, parenchyma, polyphenols content, and minerals. Moreover, the correlation between the polyphenol and mineral contents was highlighted. Therefore, three cultivation substrates with different levels of salinity/electrical conductivity were used. The reference (I) for biochemical indicators was represented by the plant grown in natural salinity conditions in the Southeast region of Romania. The results indicate that Salicornia europaea L. can be grown on different cultivation substrates other than salted soils, the plant showing the capacity to accumulate bioactive compounds similar to natively grown ones.

1. Introduction

With the prospect of evolving climate changes, many areas are facing shifts in rainfall patterns that, in combination with local climate extremes, induce alteration in soil productivity [1,2,3]. On the other hand, all over the world., the population is estimated to increase drastically, forcing scientists to find new alternative ways to produce food [4,5,6,7]. Sustainable agriculture is defined as an integrated system of production that meets food needs and improves the quality of life as a whole based on ecological and natural resource-saving principles [8,9]. In simple terms, sustainable agriculture must produce products and byproducts in a manner where the ecosystem’s health is preserved, as is its capability to provide services. Therefore, the goal is to produce food in a way that does not compromise the availability of resources for future generations [10,11,12,13].
At this time, agriculture is facing many constraints, among which is soil salinization, which threatens plant growth and production [14,15,16]. Therefore, grain production may become challenging in the context of urbanization and soil degradation [17,18]. The decrease in agricultural areas has led, in recent years, to an urgent need to consider the development of agriculture based on saline soils. A restriction to this agricultural approach is the low tolerance to salinity of agricultural crops and trees. On such saline soils, only the plants that are salt–resistant can produce significant yields [19]. Thus, due to the impact of continuous climate change, worldwide alternative sources and implicitly salt-tolerant crops are urgently required [18,20]. For this, halophyte plants naturally found in coastal salt marshes, inland dunes, and deserts may represent a perfect candidate [21]. They are adapted to harsh conditions and typically tolerate the presence of toxic ions, mainly in the form of sodium and chloride [22].
Mimicking nature, the use of halophytes or hyper-accumulators may also be a key approach to remediate the saline–alkaline land and contaminated sites [23,24]. Strategies for adapting halophytes to higher salinity levels enable their potential use for phytoremediation of brackish waters and saline soils [25]. Both annual and perennial halophyte species have the ability to accumulate significant concentrations of salt from saline soils [26].
Halophytes growing near seashores have been collected since ancient times as food for their medicinal qualities and high salt contents [27]. Their presence is necessary for the preservation of salt marshes, to enhance biomass accumulation on the soil, and to stimulate soil bioturbation and aggregation [28]. Another advantage of cultivating halophyte species is enhancing soil stability by decreasing groundwater levels [29].
One such plant is Salicornia europaea L., a member of the Amaranthaceae family. This is one of the most important halophytes, as it is able to use salt concentrations as high as full-strength seawater [19,28]. Its distribution area is located from the Arctic, Mediterranean, and Subtropical regions to South Africa [30].
Salicornia sp. accumulates salts and nutrients in its aerial parts [19,30] and is suitable for culinary, pharmaceutical, and cosmetic preparations. Due to its content of bioactive compounds [31], it is an important source of food [32,33] and is highly appreciated by consumers. The plant is used as food in different dishes (raw, cooked, or pickled), especially in northern European countries. According to the EU Novel Food Catalogue, Salicornia sp. was on the market as a food or food ingredient before 15 May 1997. Depending on the country of origin, it is known under different names: marsh samphire (EN), zeekraal (NL), soliród zielny (PL), suolayrtti (FI), harilik soolarohi (ET), deniz börülcesi (TR), slanorožec evropský (CZ), sziksófű (HU), salikornija (LV), vrsta osočnika (SL), and glasört (SE).
In Romania, it is found under the common name “brâncă” and can be found widely spread on saline soils, besides springs, ponds, and saline lakes in regions such as Tulcea county-Sărăturile Murighiol (protected area), Plopul, Oltenia (Jiu Corridor, Jiu-Danube Confluence, Ciuperceni-Desa, Ocnele Mari protected area), Valea Ilenei (Leţcani) nature reserve [34], Lacu Sărat area, Brăila county, and Turda Salt Mine. On the other hand, in Romania, the saline soils are located on lowlands, in depressionary areas with low natural drainage, and represent 4.2% of the arable land (about 614,000 ha) [35].
Therefore, given its ability to grow naturally in salinized areas and its large spectrum of bio compounds, the objective of this research work is to evaluate the anatomic and metabolic response of Salicornia europaea L. to the cultivation substrates in controlled conditions. Further work needs to be carried out to increase both its availability for human consumption and its popularity among farmers and the food industry.

2. Materials and Methods

2.1. Experimental Conditions

The choice of this species was based on the fact that in some countries, Salicornia europaea L. is edible and able to be cultivated on non-agricultural soils. The experiments were performed in the research greenhouse and the Research Center for Studies of Food Quality and Agricultural Products of the University of Agronomic Sciences and Veterinary Medicine of Bucharest. The experiments were carried out on three types of soils collected from Romania, as follows: Dâmbovița (S1), Brăila (S2), and Ialomița (S3) counties. The soil samples were collected from six sampling points at a depth of 0–20 cm. S1 was a sandy saline soil as a result of anthropic activities. S2 was a saline soil with a strong accumulation of salts in the upper layers, resulting from natural phenomena, and S3 was a meadow clay soil. Peat and perlite were used in a ratio of 3:1 for the reference soil (R).
The plants were obtained, starting from untreated seeds, Lot: SALIEUROP0119, provided by Alsagarden, France.

2.2. Biological Material

A number of 280 seeds were sown in modular seed trays in February on S1, S2, S3, and R. A number of 35 replicates for each cultivation substrate were transferred in 100% recycled polypropylene pots of 10 cm in diameter.
During the experiment, solar radiation, temperature, and relative humidity were recorded. The temperature values registered outside the greenhouse ranged from −1.4 °C in February to 31.6 °C in the middle of June. The light radiation values were between 18.3 W/m2 and 1559.1 W/m2 at the end of May. The inside temperature values in the greenhouse varied between 14.1 °C in February and 46.8 °C at the end of June. The recorded data showed that throughout the study period, the minimum and maximum values of relative humidity were 22% in February and 100% in April.
The watering regime was carried out with tap water. During February–March, the average volume of water used per day was 1 L/experimental variant; in the March–May period, it was 2.5 L/experimental variant, and in June, the average volume was 6 L/experimental variant equally distributed in the morning and evening. The aerial parts of the plants were harvested and subjected to extraction procedures for further analysis.
For biochemical assessment and cell morphology, the results provided by plants developed on S1, S2, S3, and R were compared to a native Salicornia (I or Salicornia I) plant grown spontaneously in a salinized area.

2.3. Sample Preparation for Optical Microscopy

Fresh samples from cross-sections on stems were made using a blade. The sections were placed in a Petri dish and covered with distilled water with one drop of ethanol (70%, vol) [36]. For microscope observation, an MC-7 optical microscope with digital Panasonic camera type DCM -L27 (DM 1000 LED, Leica Microsystems CMS GmbH, Wetzlar, Germany) was used.

2.4. Determination of pH and Electrical Conductivity (EC)

For pH measurements, an extraction ratio of 1: 2.5 plant/distilled water (m/v) was used. The samples were stirred for 1 h at 260 rpm and left to stand for 2 h. After settling, the pH was read directly into the prepared suspension sample.
The determination of EC values was performed according to the reference standard [37]. Thus, for EC of soil, the samples were dried at room temperature and sieved through a 2 mm sieve. Further, 10 g of soil was mixed with 50 mL of ultrapure water and stirred for 1 h at 260 rpm [38]. After filtration, the EC was measured directly into the prepared suspension sample using a Mettler Toledo SevenExcellence TM multiparameter (Mettler-Toledo Group, Schwerzenbach, Switzerland) and the obtained values are expressed in µS·cm−1.

2.5. Preparation of Plant Extracts for UV-VIS Analysis

For spectrophotometric determination, the extracts were prepared using smashed fresh plant and methanol 99.9% (Sigma-Aldrich Chemie GmbH, Steinheim, Germany) as solvent, in a ratio of 1:10 (m/v). The extract was cold centrifugated at 6000 rpm for 10 min. The supernatant was used for UV-VIS analysis.

2.6. Total Phenolic Content (TPC)

In order to determine the total phenolic content, Folin–Ciocâlteu method was adapted from [39,40]. For this, the following reagents were used: 20% Na2CO3 solution and Folin–Ciocâlteu reagent (2N, Sigma-Aldrich Chemie GmbH, Steinheim, Germany). The reading was performed at an absorbance of λ = 750 nm. The calculated results were based on a gallic acid calibration curve (R2 = 0.999) and were expressed as mg gallic acid (Carl Roth GmbH + Co. KG, Karlsruhe, Germany) equivalent (GAE) per mL extract.

2.7. Total Flavonoids Content (TFC)

The amount of total flavonoid content of plant extracts was determined using the adapted method described by [41]. The absorbance was measured at λ = 510 nm with a spectrophotometer. The calibration curve (R2 = 0.996) was obtained using rutin (Carl Roth GmbH + Co. KG, Karlsruhe, Germany). The results were expressed as rutin equivalents (RE) per ml extract.

2.8. Microwaves-Assisted Extraction (MAE)

The samples consisted of aerial parts of the plants. The cultivation substrate was removed with ultrapure water, and the plants were dried at room temperature. A total of 50 mg of dried sample was subjected to microwave digestion in an ETHOS UP Microwave Digestion System (Milestone Srl, Sorisole, Italy). For that, an adapted method [42] was applied, using a mixture of 4 mL of HNO3 (65%, Suprapur ®, Merck KGaA, Darmstadt, Germany) and 1 mL of H2O2 (30%, Suprapur®, Merck KGaA, Darmstadt, Germany). The extraction parameters were 1800 W, T1 20–200 °C for 30 min, and 1800 W, T2 110 °C, followed by 30 min of cooling. After digestion, the samples were brought to a final volume of 50 mL with ultrapure water.

2.9. The Elemental Analysis of Plant Samples

The elemental analysis was determined using ICP-MS (Agilent 7700× series) using a multielement calibration curve. The certified reference material was used as a calibration standard, lot: 2-34YJY2 (obtained from Agilent Technologies, Santa Clara, CA, USA). Triplicate analysis of all the samples was conducted in order to check the precision and accuracy of the data.

2.10. Statistical Analysis

The Bonferroni test, a general linear model, was used for the comparison of means for the content of bio compounds between groups, using Statistical Package for Social Science (SPSS version 21.0). Statistical processing was performed for a 95% probability. The results are expressed as the mean ± standard error of the mean (SEM).

3. Results

3.1. Results on pH and EC Determinations

The pH of soil is called a “master variable” due to its role in many chemical and biochemical processes. It indicates the degree of acidity or alkalinity. Between pH and biological, chemical, and physical properties of soil, there is a bidirectional relationship, which controls biological processes, and it is controlled by the leaching of cations such as Ca, Mg, K, and Na. The pH of soil depends on the ratio between H+ and OH−. H+ ions in soil can be a result of the dissolution of CO2 in soil’s moisture, humic residues, nitrification of NH4, and N uptake by plants. It can be said that soil pH has implications on nutrient availability for crops and other biochemical processes, whereas some biogeochemical processes can influence the pH evolution. Thus, crop productivity may be related to the pH value of the soil. Generally, the optimum pH interval for agricultural crops is between 5.5 and 7.5 [43].
In this work, the pH and EC of the cultivation substrates were determined before and after plant cultivation. It was found that in the growth and development of Salicornia europaea L., there were no significant differences among the cultivation variants. Also, there were no significant differences between the pH values before and after cultivation of Salicornia europaea L. (Figure 1).
After cultivation in the greenhouse experiment, the analysis of the samples showed that S1 had a pH of 7.65 ± 0.003 (mean ± standard error (SE)), S2 had one of 8.52 ± 0.06, S3 had one of 7.31 ± 0.005, and R had one of 5.29 ± 0.10. According to the United States Department of Agricultural National Resources Conservation Service, all soils were defined as slightly alkaline (>7.4), neutral (≥7.3), and very alkaline (>8.5), except for the reference soil (R), which was very acidic.
In general, agricultural crops are found on soils in the range of slightly acid–slightly alkaline. Within this interval, it is found that the bioavailability of nutrients is optimal and also influenced by several factors including the pH value [44].
The obtained EC values are presented in Figure 2. It can be observed that the cultivation of Salicornia europaea L. may influence the EC of the soil; for each tested substrate, the differences between the before and after cultivation values are significantly different. This may be due to the ability of the plant’s mechanism to tolerate salt and heavy metal toxicity, having, among other characteristics, a phytoextraction role. In the same way, Salicornia bigelovii [45], Salicornia brachiata, and Salicornia iranica have the same characteristics.
The presented results can be easily correlated with the variation of the Na content of the plant obtained on the cultivation substrates, as described below. Therefore, the mechanisms by which plants extract salt from saline soils and the consequences of this process on the soil–plant system are diverse. For instance, it was described that the main mechanisms for the role of plants in remedying salted soils are (1) the reduction of pH, which increases the solubility of CaCO3 and, therefore, makes Ca2+ available for the exchange of cations with Na+, and (2) the absorption by plants of dissolved salts and/or Na in particular [46].

3.2. Results of Spectrophotometric Analysis

In plants, polyphenol synthesis is generally stimulated in response to stress factors. Therefore, polyphenols might be considered bioindicators for plant development in conditions other than the native ones, having, moreover, high economic importance. However, increasing polyphenol content in stressed plants restricts their biomass production [47]. However, it is specific to the saline environment. The effect of cultivation substrates on the accumulation of total phenolic content in the Salicornia europaea L. plant is summarized in Figure 3. Spectrophotometric determination of the total phenolic content has been used as one of the fastest and simplest methods of quantification, even if there are interferences in absorbance at the same wavelength of substances such as proteins, nucleic acids, and amino acids [48].
The graphical representation was presented in the form of bars to highlight the difference between the cultivation substrates for the same species. Statistically, the results obtained are significantly different and were calculated for the probability of 0.05. Compared to the phenolic content of the plant grown in indigenous conditions (I = 118.08 µg GAE·mL−1 extract), the highest values of the total phenolic content were 92.18 µg GAE·mL−1 extract) recorded for the plant grown on the R cultivation substrate. The results show that the acidic cultivation substrate R (pH = 5.18) stimulated the accumulation of phenolic compounds. This tendency is according to other published data on pH affecting almost all biological and chemical processes in plants [49]. Considering the purpose of our study, the results showed the possibility of cultivating this species on acidic soils with the aim of capitalizing on plants rich in phenolic content.
Similar research was conducted by Grigore and Oprica [34] for Salicornia europaea from the Ilena Valley natural reserve, obtaining 1.04 mg GAE·g−1 dry weight. Furthermore, findings confirming the positive biological effects of the species were recorded by Sánchez-Gavilán et al. [31], who studied Salicornia patula Duval-Jouve from the Iberian Peninsula (Spain).
Moreover, the flavonoid content of Salicornia europaea L. determined for all cultivation variants is shown in Figure 4. With regard to this, other studies should be regarded, primarily Gupta’s book chapter [49] showcasing that Salicornia europaea contains quercetin, isoquercitrin, rutin, and isorhamnetin 4′-glucoside.
In general, the content of flavonoids differs from one halophyte species to another [38]. In this work, within the same species, multiple variations were identified. Thus, for variants S1, S2, and S3, there were no significant differences, the TFC values varying between 0.422 and 0.426 mg RE · mL−1 extract. Also, no significant differences were registered between the TFC of the indigenous plant (I) and the plant grown on acidic soil (R), the values being 0.604 and 0.589 mg RE · mL−1 extract, respectively. Significant differences were observed between S1, S2, and S3 extracts and those from Salicornia I and R.
It should be noted that in this study, the amount of flavonoids is higher than that of polyphenols, which may be due to the solubility of these biocompounds [50]. The obtained results are similar to those obtained by Sytar et al. [51], where the same type of solvent extraction was used. In support of the presented findings, from the chemical point of view, some tendencies were registered for pasta made from durum wheat supplemented with Salicornia europaea L. extract before and after digestion. Thus, it was found that the quantity of polyphenols and flavonoids in pasta supplemented with Salicornia europaea L. extract was higher than in the control samples [52].
Regarding this case study, the results showed the possibility of cultivating Salicornia europaea L. on substrates other than native ones. In this study, acidic substrates were specifically used.

3.3. Results on Elemental Quantification Using ICP-MS

Mineral nutrients are very important for human health, and their presence or absence has a direct impact on beneficial microorganisms. In plants, their presence increases plants’ disease resistance and enhances plant growth and development [53].
In our study, the mineral composition of Salicornia europaea L., depending on the cultivation substrates, is presented in Table 1. The analysis of the chemical composition of Salicornia europaea L. showed that Na content varies with the growing substrate, the differences being distinctly significant. High values of Na accumulation were obtained in the case of the aerial parts of Salicornia europaea L. grown on the substrates S2 and S1. Also, regarding Mg content, the concentration depended on the cultivation substrate. High values in Mg content were found in aerial parts harvested from the R and S2 substrates compared to the indigenous plant (I).
The value of K content is significantly different, with high values for the plant grown on acidic soil (R) (40.867 g·kg−1). What is interesting is that Salicornia europaea L., in its indigenous environment, has a lower K content. One explanation is related to the high Na+ concentrations in indigenous salinized soil where Salicornia I is grown. According to [49], high levels of Na+ inhibit the uptake of K+ ions, which is an essential element for the growth and development of plants, resulting in lower productivity.
Regarding Ca content, in the case of indigenous Salicornia europaea L., a concentration of 3.943 g/kg−1 was found. According to Thor K. [54], in an Arabidopsis experiment, the roots exhibit Ca2+ signals in response to K+ deficiency using the decoding complex that regulates the transport of K+. In this work, the highest values were observed in the case of the S3 cultivation substrate (non-saline, pH 7.45). Similar studies on S. bigelovii found significant amounts of minerals in stems: Na (1218.1 mg/100 g), Ca (158.8 mg/100 g), K (740.1 mg/100 g), and Mg (52.2 mg/100 g) [32]. It is important to mention that, generally, the adopted extraction and analysis procedure has an important role in the elemental analysis, so small differences obtained in quantification may be due to the method of extraction [55] and also to the sample preparation.

3.4. Correlation between Phenolic Compounds and Minerals

There are several elements known for their free radical scavenging properties. In this study, a moderate and strong correlation was observed between mineral content and phenolic compounds (Table 2).
A positive and high correlation was observed between Mg and total phenolic content (TPC) (r = 0.802, p = 0.05) and total flavonoid content (TFC) (r = 0.774, p = 0.05). Also, a strong and positive correlation was recorded between Na and Mg (r = 0.737, p = 0.05). A moderate correlation was found between Ca, TPC, and TFC, indicating that these minerals might be a part of the phenolic compounds and play important roles in the polyphenol accumulation in Salicornia plants. This study also corresponds with the research conducted by Thiruvengadam et al. [56], as we found a positive correlation between metal ions.
In the present study, a low and negative correlation was also observed between minerals such as K, TPC, and TFC. Low and negative correlation coefficients among mineral and polyphenol contents may be due to the influence of cultivation substrates.

3.5. Results Related to Cell Morphology

The cell morphology of Salicornia europaea L., the plant that naturally grows mainly in marshy areas, is presented in Table 3.
The images in Figure 5 show the morphology of the Salicornia europaea L. stem in different anatomical regions. The inner parts of the stem are closed by a single-layer structure called the epidermis, and on the outside, the epidermis is covered by a cuticle. Similar dimensions to the cuticle of the plant harvested from the native area were found for those cultivated on the substrate S2 and S1. As can be seen, the highest values of the cuticle were registered for the plants grown on the substrate S3. On the opposite side is the dimension of the cuticle of the plant grown on peat and perlite substrate (R) with a value of 0.151 µm. According to the study performed by [57], the role of the cuticle is related to the water loss limitation, pathogen and insect attacks, or attenuation of UV irradiation. Also, the structural and chemical response of the cuticle is related to biotic and abiotic stress factors and organ development stages. Therefore, at the cuticle level, it can be concluded that the cultivation substrate influences the cuticle thickness.
The palisade parenchyma is represented by cylindrical cells and is involved in water transport to the peripheral layers or air accumulation [32]. According to the measurements made in this study, it was observed that the cultivation substrates influence the size of the cell’s plies. The registered differences between cultivation substrates S1, S2, and S3 and those used in I and R might be related to the first mechanisms developed by the plants to manage the high Na+ concentrations that take place at this level [58,59].
Then, on the outside of the palisade tissue, we found the epidermis, where stomata structures are found. At the level of the epidermis, significant differences were registered for cultivation variants S1 and S2 compared to I and R. The highest thickness was observed for the epidermis of the plant grown on S1 (2.394 µm).
The obtained results follow the same model according to which anatomical changes like the thickness and stomatal distribution are induced by increased salinity. The increase in the epidermal thickness could be an adaptation mechanism of Salicornia europaea L. to maintain the water content and provide additional space for the sequestration of Na+ [60]. There are several special structures developed by halophytes, such as the epidermal bladder. Their role is to accumulate excessive Na+, ensuring the survival of the plant [61].

3.6. Study Limitations

There are several limitations that this study does not address, and future studies should be developed. Firstly, regarding the growth and development of Salicornia europaea L., it would be useful for the producers to have results on both plant growth parameters for each cultivation substrate and the productivity obtained for each cultivation variant. Secondly, performance characteristics such as dry weight or fresh weight and plant height should also be addressed. Thirdly, since elements such as zinc, manganese, and copper are essential for plants, being involved in a number of biochemical reactions, their quantification would be preferable. Lastly, heavy metals should also be taken into account in future studies. In particular, zinc is a cofactor of chloroplast b carbonic anhydrase (b-CA), which catalyzes the conversion of HCO3− and CO2 and supplies RuBisCo with CO2 in Calvin Cycle. Moreover, Zn is involved in photosynthesis, Mn is part of several processes such as photosynthesis, while Cu is important in the electron transport chain and is also involved in the activity of Cu/Zn-superoxide dismutase (Cu/Zn-SOD), inactivating reactive oxygen species [62].

4. Conclusions

Overall, our findings greatly increase our understanding of how S. europaea reacts in response to the cultivation substrate, allowing the identification of possible appropriate future agricultural practices. Specifically, it was shown that Salicornia europaea L., although a salt-loving plant, is rather unpretentious and can be successfully cultivated on non- and slightly saline soils, as well as in greenhouses watered with tap water. Cell morphology analysis was efficient in evaluating the impact of the cultivation substrate on anatomical modification in the cuticle, epidermis, and parenchyma. Depending on the substrate, the plant accumulates phenolic compounds, with high values in the case of cultivation on peat substrate (acidic soil). Based on the obtained results, Salicornia, being rich in minerals (Ca in S3, Na and Mg in S2, and K in peat substrate), may be used successfully in food production. The minerals were found to be high and moderately correlated with polyphenols and flavonoid content, especially for Ca and Mg.
Ultimately, although further studies are required, these preliminary results support the idea that Salicornia cultivation, in another substrate than a saline substrate, accumulates bioactive compounds similar to natively grown ones, providing an important source of minerals and polyphenols.

Author Contributions

All authors contributed equally to this work as follows: C.G.C. designed the experiments and performed analytical measurements. A.D. performed statistical analysis and conclusions. M.G. performed morphological measurements. M.M.Z. performed the spectrophotometric analysis. A.M. performed the ICP-MS analysis. M.P. and C.G.C. prepared the manuscript and the interpretation. M.F.C. established and maintained the experimental lots. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Romanian National Research Program PNIII, Subprogram 3.2 International and European Cooperation—Horizon 2020, financing contract no. 44/2018 and Integrated system of bioremediation—biorefinering using halophyte species—code: ERANET FACCE-SURPLUS-HaloSYS, and the publication fee was funded by CNFIS-FDI-2023-F-0715.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data are contained within the article.

Acknowledgments

All the determinations (physical, chemical, microscopic, etc.) were found with the support of the Research Center for Studies of Food Quality and Agricultural Products as the infrastructure of the University of Agronomic Sciences and Veterinary Medicine of Bucharest, Romania.

Conflicts of Interest

The authors declare no conflict of interest.

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Applsci 13 10835 g001
Figure 1. The impact of Salicornia europaea L. cultivation on the pH variation. Values followed by the same letter(s) do not differ significantly at p = 0.05.
Figure 1. The impact of Salicornia europaea L. cultivation on the pH variation. Values followed by the same letter(s) do not differ significantly at p = 0.05.
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Figure 2. The impact of Salicornia europaea L. cultivation on EC variation. Values followed by the same letter(s) do not differ significantly at p = 0.05.
Figure 2. The impact of Salicornia europaea L. cultivation on EC variation. Values followed by the same letter(s) do not differ significantly at p = 0.05.
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Figure 3. TPC—total phenolic content in Salicornia europaea L. grown on different substrates. Values followed by the same letter(s) do not differ significantly at p = 0.05.
Figure 3. TPC—total phenolic content in Salicornia europaea L. grown on different substrates. Values followed by the same letter(s) do not differ significantly at p = 0.05.
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Figure 4. TFC—total flavonoid content in Salicornia europaea L. grown on different substrates. Values followed by the same letter(s) do not differ significantly at p = 0.05.
Figure 4. TFC—total flavonoid content in Salicornia europaea L. grown on different substrates. Values followed by the same letter(s) do not differ significantly at p = 0.05.
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Figure 5. Gallery of microscopy images of Salicornia europaea L. fleshy segment sections from the middle region of the plant. (A) Image of segment section: cuticle (cut), epidermis (ep), and palisade tissue (pt); (B) measurements on I variant; (C) measurements on S1 variant; (D) measurements on S2 variant; (E) measurements on S3 variant; and (F) measurements on R variant.
Figure 5. Gallery of microscopy images of Salicornia europaea L. fleshy segment sections from the middle region of the plant. (A) Image of segment section: cuticle (cut), epidermis (ep), and palisade tissue (pt); (B) measurements on I variant; (C) measurements on S1 variant; (D) measurements on S2 variant; (E) measurements on S3 variant; and (F) measurements on R variant.
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Table 1. Elemental analysis results for Salicornia europaea L. grown in different conditions.
Table 1. Elemental analysis results for Salicornia europaea L. grown in different conditions.
Cultivation SubstrateInitially
pH Values		Na g/kgMg g/kgK g/kgCa g/kg
S17.8 ± 0.017 72.166 ± 0.405 c6.874 ± 0.119 c19.038 ± 0.133 c36.359 ± 0.526 b
S28.81 ± 0.03 156 ± 0.479 b11.734 ± 0.016 b15.400 ± 0.061 d8.057 ± 0.307 d
S37.45 ± 0.0354.487 ± 0.302 d 7.388 ± 0.052 c23.389 ± 0.089 b46.207 ± 0.461 a
I8.81 ± 0.06170.336 ± 1.566 a15.039 ± 0.133 a7.685 ± 0.022 e3.943 ± 0.438 e
Peat and perlite (R)5.18 ± 0.0345.962 ± 0.292 e11.329 ± 0.124 b40.867 ± 0.229 a25.520 ± 0.346 c
Within each column, values followed by a common letter are not significantly different (p ≤ 0.05).
Table 2. Pearson’s correlation coefficients of the phenolic compounds and minerals.
Table 2. Pearson’s correlation coefficients of the phenolic compounds and minerals.
TPCTFCNaMgKCa
TPC1
TFC0.9691
Na0.2980.1941
Mg0.8020.7740.7371
K−0.0190.162−0.816−0.3061
Ca−0.523−0.516−0.880−0.9150.4651
p < 0.05.
Table 3. Morphological characteristics of Salicornia europaea L.
Table 3. Morphological characteristics of Salicornia europaea L.
SubstrateCuticle (µm)Epidermis (µm)Parenchyma (µm)
I0.297 ± 0.014 b1.707 ± 0.090 c6.565 ± 0.566 c
S10.278 ± 0.016 b2.394 ± 0.331 a7.675 ± 0.423 b
S20.240 ± 0.008 b2.023 ± 0.121 b8.584 ± 0.599 a
S30.533 ± 0.058 a1.657 ± 0.099 c8.694 ± 0.677 a
Peat and perlite (R)0.151 ± 0.053 c1.783 ± 0.162 c5.226 ± 0.412 d
Within each column, values followed by a common letter are not significantly different (p ≤ 0.05).
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Constantin, C.G.; Zugravu, M.M.; Georgescu, M.; Constantin, M.F.; Moț, A.; Paraschiv, M.; Dobrin, A. The Impact of the Growing Substrate on Morphological and Biochemical Features of Salicornia europaea L. Appl. Sci. 2023, 13, 10835. https://doi.org/10.3390/app131910835

AMA Style

Constantin CG, Zugravu MM, Georgescu M, Constantin MF, Moț A, Paraschiv M, Dobrin A. The Impact of the Growing Substrate on Morphological and Biochemical Features of Salicornia europaea L. Applied Sciences. 2023; 13(19):10835. https://doi.org/10.3390/app131910835

Chicago/Turabian Style

Constantin, Carmen Gabriela, Mihaela Maria Zugravu, Mihaela Georgescu, Mugurași Florin Constantin, Andrei Moț, Maria Paraschiv, and Aurora Dobrin. 2023. "The Impact of the Growing Substrate on Morphological and Biochemical Features of Salicornia europaea L." Applied Sciences 13, no. 19: 10835. https://doi.org/10.3390/app131910835

APA Style

Constantin, C. G., Zugravu, M. M., Georgescu, M., Constantin, M. F., Moț, A., Paraschiv, M., & Dobrin, A. (2023). The Impact of the Growing Substrate on Morphological and Biochemical Features of Salicornia europaea L. Applied Sciences, 13(19), 10835. https://doi.org/10.3390/app131910835

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