The effect of drought stress on the antioxidant activity of water (ААА) and methanol (ААМ) extracts, expressed in %, and the total content of polyphenols (TРС), expressed in mg equivalent of gallic acid (mg/g TW) in the leaves of Amaranthus species.
Abstract
The Federal Research Center of Vegetable Growing has developed the cultivars Valentina (Amaranthus tricolor L.) and Krepysh (Amaranthus cruentus L.), which are successfully grown in several regions of Russia. The dry periods observed in recent years have a negative impact on the development of plants. The red-colored vegetable cultivar demonstrated a higher level of adaptability to drought than the green-colored grain cultivar. It was found that only in the leaves of cv. Valentina multiple spiked crystals consisting of four elements were formed, the predominant proportion belonged to Ca (38.59), then P (0.48), Mg (0.25), and K (0.16) followed, weight%, respectively. Under the conditions of moisture deficiency, the antioxidant activity of water and ethanol extracts in the leaves of both types of amaranth increased from 1.5 to 2.5 times. It was established that under drought conditions, the carbohydrate metabolism and the synthesis of secondary metabolites change. The leaves of the new cultivar of amaranth Valentina are a promising and reproducible source of antioxidants and can be used to create phytobiological preparations. The increased level of the main macro- and microelements—Ca, K, P, Mg, Mo, S and Cl in the seeds of cv. Valentina and Krepysh makes these cultivars promising for use in the food industry.
Keywords
- amaranth
- leaves
- photosynthetic pigments
- low-molecular-weight metabolites
- ash composition of seeds
1. Introduction
Among abiotic stresses, drought is widely spread and strengthens from year to year all over the world. The stressful influence of drought conditions causes changes in morphological, physiological, and metabolical processes of plants that decrease the productivity and the quality of agricultural crops after all [1]. Molecular indicator of water stress is, first of all, speeded accumulation of active forms of oxygen that leads to the development of water stress, the change of chlorophylls structure, the decrease of photosynthetic pigments and metabolites, and the damage of plants cells [2, 3, 4, 5]. Phenolic compounds and flavonoids are the most important and widely spread secondary products of plants. These metabolites enlarge enzymic antioxidant system and possess essential potential to decrease and prevent the cell damage [6]. Mineral elements are not only used as structural components, but also play an important role in the enzymes activity, osmotic pressure control for the cells’ turgor and growth, take part in acid-base and water-salt metabolism [7, 8, 9]. Increased stability to drought mostly depends on the mineral composition of the plants [10, 11].
The most important and actual problem of genetic-breeding research studies is to determine the crops that are stable to drought. Metabolomic approach is a new direction of molecular-genetic research studies to identify the changes in plants under the influence of adverse environmental factors and to assess their nutritional value. Though, nowadays, the use of this approach remains a little used and poorly studied direction of breeding.
The fundamental knowledge about the characteristics of the leaves, seeds, and flour is crucial for the promotion of the crop for use in the food industry. The
2. Studies results
2.1 Studies place, objects, and methods
A vegetative experiment was conducted with amaranth species
The pots were filled with a mixture of peat and sand (5:1) with a drainage layer at the bottom. In the pots with the control samples, the humidity of the substrate for the plants was maintained at the level of 45–50%. Soil moisture was determined using soil moisture meter MC-7828 SOIL. All the plants were grown for 2 months in well-watered conditions in natural light (Figure 1). The average day/night temperature, relative humidity, and the day length during the experimental period were 17.2°C/11.7°C, 64%, and 17 h, respectively. After 2 months of growth, the degree of stress from drought was determined according to the moisture content in the soil. The watering of the experimental plants was stopped until the signs of wilting. The duration of the soil drought period was 7 days. The plants were examined when the soil moisture dropped till 20–25%.
The biochemical research studies were held in the Laboratory of Physiology and Biochemistry of FHRCBAN.
The understudied parameters included the laboratory studies of the leaves (microscopy of cross sections of the leaf blade, photosynthetic pigments content, antioxidant activity, phenolic compounds sum, ash composition seeds, and quality content of the leaves’ main metabolites). The leaves’ microscopy and ash composition were determined on analytical REM JEOL JSM-6010 LA (JEOL Ltd., Japan). Photosynthetic pigments Chl a and b and total carotenoids (Car) were studied on spectrophotometer Helios Υ UV–vis (USA) in accordance with the method [12]. Total phenolic amount was determined with Folin–Ciocalteu reagent in accordance with the method [13] and tоtal antioxidant capacity, the scavenging activity for the 2, 2-dipheny l-1-picrylhydrazyl (DPPH) radical was determined in accordance with the method [14].
Metabolites quality composition contained in leaf extracts was analyzed on JEOL JMS-Q1050GC (JEOL Ltd., Japan) via the method of gas chromate-mass-spectrometry in accordance with the method [15].
2.2 Biomineralization of amaranth leaves
An important morphological feature of
The local energy dispersive spectrometry (EDS) analysis showed that the inclusions contained four elements. The main element was Ca (5.9–8.3 mass %); K (0.34–0.38 mass%); Mg and P—0.03–0.07 mass %. The combination of scanning electron microscopy (SEM) and EDS was a convenient method for determining the microstructure in the cross section of the leaves of
Calcium is involved in regulating metabolic processes, plant growth and development [23]. Under drought stress, Ca is an integral part of the recovery process after stress exposure, regulating the plasma membrane enzyme adenosinetriphosphatase, which is required to pump back nutrients lost during cell damage [24].
2.3 Effects of drought on influence on photosynthetic pigments synthesis
The content analysis of chlorophylls and carotenoids in the amaranth leaves showed that some changes were associated with drought (Figure 4). An increase of Chl a, b and Car was observed in the leaves of drought-affected amaranth species. In the leaves of
A high correlation was found between Chl a and Car (r = 0.985) and Chl b and Car (r = 0.977) in the leaves of
2.4 Effects of drought on influence on antioxidant activity and phenol compounds sum accumulation
The ability of amaranth leaf extracts to absorb DPPH + free radicals, which is used as a measure of total antioxidant activity (TAA), and total phenol content (TPC) are shown in Table 1. The antioxidant activity of the water extracts of
Samples | Determined indicators | ||
---|---|---|---|
AAA | AAM | TPS | |
24.11 ± 1.87 7.75 | 16.26 ± 0.65 0.43 | 2.28 ± 0.37 16.06 | |
66.82 ± 1.36 2.03 | 27.08 ± 0.87 3.24 | 6.61 ± 0.56 8.59 | |
1.35 ± 0.21 14.93 | 16.08 ± 0.24 1.53 | 1.15 ± 0.07 6.09 | |
7.71 ± 1.01 13.56 | 26.05 ± 0.56 2.15 | 3.19 ± 0.45 14.18 |
Hence, the leaf mass of
2.5 The influence of drought on the contents of metabolites in the leaves of A. tricolor L. (cv. Valentina) и A. cruentus L. (cv. Krepysh)
Forty-three secondary metabolites were totally determined in ethanol extracts of amaranth leaves. Forty-two substances were identified in the leaves of
N | Тmin | Metabolite | Peak height, % of scale cv.Valentina cv,Krepysh | Biological characteristic | |
---|---|---|---|---|---|
1 | 10:20 | Lactic acid | 15–8 | 0.3–0.2 | Antimicrobial 93 |
2 | 10:23 | Butanoic scid | 1.4–0.5 | 1.2–0.3 | Organic acid |
3 | 10:27 | Clycolic acid | 5–15 | 5–7 | Organic acid |
4 | 10:28 | Oxalic acid | 10–15 | 8–5 | Organic acid |
5 | 10:42 | Pyruvic acid | 0.2–0.2 | 0.3–1.2 | Antimicrobial 118 |
6 | 10:49 | 2-Butanedioic acid | 0.2–1.5 | 0.1–7 | Organic acid |
7 | 11:00 | L-Alanine | 1.5–4 | 1.2–1.8 | Amino acid |
8 | 11:29 | Monoethyl malonic acid | 8–10 | 5–10 | Organic acid |
9 | 12:16 | Glyoxylic acid | — | 2.5–3 | Antimicrobial 78 |
10 | 13:23 | Acetamide | 0.8–0 | — | Antimicrobial 40 |
11 | 13:43 | Glycerol | 8–60 | 8–70 | Antimicrobial 77 |
12 | 14.04 | Succinic acid | 11–15 | 3–4 | Organic acid |
13 | 14:23 | Glyceric acid | 40–13 | 13–7 | Organic acid |
14 | 15:03 | Glycine | 0.4–3 | 0.2–1.5 | Amino acid |
15 | 15:24 | 2-Oxopentanoic acid | 2–3.2 | 8–10 | Organic acid |
16 | 15:29 | Malonic acid | 6–7 | 2–3 | Organic acid |
17 | 16:27 | Malic acid | 14–27 | 8–19 | Antimicrobial 96 |
18 | 16:40 | L-5-Oxoproline | 1.5–2 | 1.2–2 | Amino acid derivative |
19 | 16:48 | L-Proline | 5–20 | 4–11 | Amino acid |
20 | 17:30 | 2.3.4.-Trihydroxybutiric acid | 22–43 | — | Organic acid |
21 | 17:54 | 1. 2-Ketoglutaric acid | 0.2–0.4 | — | Keto acid |
22 | 18:14 | Arabinoic acid | 0.3–0.25 | 0.3–0.3 | Organic acid |
23 | 18:16 | Ketosuccinic acid | 11–8 | — | Organic acid |
24 | 18.24 | Lauric acid | 0.2–0.4 | 0.1 | Saturated fatty acid |
25 | 19:33 | Vanillic acid | 2–2.5 | — | Phenolic acid |
26 | 19:37 | Benzoic acid | 3–4.1 | 0.5–1.6 | Antimicrobial 60 |
27 | 16.46 | Fumaric acid | 0.1–0.5 | — | Organic acid |
28 | 16:58 | Serine | 2.5–11 | 3–8 | Amino acid |
29 | 25:00 | 2-Propenoic acid | 0.1–0.3 | — | Organic acid |
30 | 20:08 | Adenine | 1–4 | 1–2.5 | Amino acid |
31 | 20:21 | Citric acid | 15–40 | 8–15 | Organic acid |
32 | 21:48 | Cinnamic acid | 2.5–2.8 | 1.2–1.0 | Phenolic acid |
33 | 22:24 | Myristic acid | 4–13 | 4–10 | Saturated fatty acid |
34 | 22:26 | Acrylic acid | 8–10 | 6–10 | Antimicrobial 44 |
35 | 22:30 | Palmitic Acid | 0.1 | 0.05–0.1 | Saturated fatty acid |
36 | 22:46 | Tartaric acid | 4–62 | 3–15 | Antimicrobial 126 |
37 | 22:48 | Caffeic acid | 1.2–28 | 0.2–0.8 | Phenolic acid |
38 | 23:17 | Apigenin | 0.4–1.2 | — | Glycosides |
39 | 23:31 | Myo-inositol | 10–40 | 11–15 | Sucar acid |
40 | 24:19 | Stearic acid | 1–1.4 | — | Saturated fatty acid |
41 | 34:14 | Mannonic acid | 10–70 | 8–30 | Organic acid |
2.6 The ash residue comparative composition of A. tricolor L. (Valentina cultivar) and A. cruentus L. (Krepysh cultivar) amaranth seeds
The content (in mass %) of 11 main elements that make up the mineral part of amaranth seeds was studied (Table 3). The ash composition of the seeds varies significantly. The descending series of the elements accumulation is the following:
Mineral Elements | ||||||
---|---|---|---|---|---|---|
min-max | V,% | min-max | V,% | |||
K | 8.94 ± 0.20 | 7.78–9.07 | 13.35 | 15.78 ± 0.19 | 11.71–13.32 | 17.75 |
P | 9.67 ± 0.08 | 8.49–9.98 | 8.82 | 14.38 ± 0.15 | 13.29–14.87 | 27.78 |
Ca | 17.83 ± 0.08 | 16.71–18.08 | 13.39 | 11.54 ± 0.12 | 9.76–14.37 | 29.85 |
Mo | 2.54 ± 0.04 | 2.12–3.35 | 17.62 | 3.43 ± 0.04 | 3.21–4.86 | 45.16 |
Mg | 7.33 ± 0.42 | 6.31–8.89 | 13.09 | 5.76 ± 0.22 | 4.06–6.06 | 38.21 |
S | 1.84 ± 0.20 | 1.08–2.35 | 19.45 | 2.23 ± 1.04 | 1.49–2.41 | 38.60 |
Si | 0.48 ± 0.07 | 0.41–0.64 | 20.68 | 0.21 ± 0.08 | 0.17–0.37 | 22.97 |
Mn | 0.17 ± 0.11 | 0.12–0.21 | 27.81 | 0.19 ± 0.08 | 0.10–0.29 | 54.20 |
Fe | 0.23 ± 0.04 | 0.18–0.36 | 36.38 | 0.23 ± 0.03 | 0.13–0.39 | 58.40 |
Zn | 0.21 ± 0.06 | 0.17–0.34 | 30.35 | 0.26 ± 0.08 | 0.17–0.24 | 29.45 |
Se | 0.41 ± 0.06 | 0.37–0.54 | 29.45 | 0.35 ± 0.06 | 0.27–0.44 | 31.18 |
∑ | 49.65 | 54,36 |
At the same time, the main proportion of ash elements in the seeds of
Ca is the main ash element in the seeds of
The content of Mg and Mo in the seeds of
S is a biogenic element in the composition of proteins and glutathione, has antioxidant activity, provides the process of energy transfer in the cell by transferring electrons, participates in the transfer and fixation of methyl groups, the formation of covalent, hydrogen, and mercaptide bonds, provides the transfer of genetic information. Mn is a cofactor and activator of many enzymes (pyruvate kinase, decarboxylase, siperoxide dismutase), participates in the synthesis of glycoproteins and proteoglycans, has antioxidant activity.
In active centers (hemoproteins and iron-sulfur proteins), Fe determines the structure and activity of space and participates in redox reactions. Organic Fe is a necessary compound for the human body. This element is part of catalytic centers of many redox enzymes. Zn stabilizes the structure of molecules, plays an important role in the metabolism of DNA and RNA, in protein synthesis and cell division, in the processes of signaling within the cell [41, 42, 43].
Si is not only the basis of the framework element of tissues, but also controls a number of biological and chemical processes in a living organism, increases the resistance of a living organism to the effects of biogenic and abiogenic stressors, is a necessary trace element that is part of active centers in the form of selenocysteine animoacystide [44]. The concentration of Si in
The minerals found in amaranth seeds are important for meeting human dietary needs and can make a significant contribution to recommended diets.
2.7 Biologically active components of the studied cultivars of Amaranthus L.
The previous studies of the extracts from cv. Valentina fresh leaves detected the following physiologically active substances with antioxidant activity: Amarantin—1.5 mg/g, Ascorbic acid—150–170 mg/100 g, simple phenols and phenolcarboxylic acids, Chlorogenic, Ferulic, Gallic acids, and Arbutin—2.05, 0.01, 1.51, and 473 mg/g, respectively. All metabolites are biologically active substances [45]. Phenolic acids and Betacyanin (Amarantin) are characterized by antibacterial [46, 47, 48], antimycotic, anti-inflammatory, and wound-healing properties. Ferulic acid has radioprotective properties, glycosylated hydroquinone Arbutin exhibits antioxidant activity [48]. The pigment Amarantin is a multifunctional pigment of red-colored amaranth leaves. Amarantin is a nitrogenous heterocyclic compound that has a strong physiological effect on living organisms. The study of the biochemical properties of Amarantin extracted from the leaves of the red-colored cv. Valentina revealed the following physiological activities: antibacterial, antimycotic, antioxidant, antitumor. The extracts from fresh and dried leaves of cv. Valentina stimulated the growing activity of vegetable seeds, which allows its extracts to be used in phytobiology for stimulation of seeds and sprouts (in the concentration of 10-4, 10-5 M) [49]. The mechanism of antioxidant activity of Amarantin is associated with its ability to neutralize the superoxide radical and inhibit lipid peroxidation. This allows the leaves to be used to obtain Amarantin extract as a dietary supplement and a phytopreparation.
Under the conditions of drought and high solar radiation, the content of Amarantin in the leaves of cv. Valentina decreases to 40%. The received data indicate that Amarantin performs an important protective function of the photosynthetic apparatus in the plant [50, 51]. The advantage of Amarantin as a water-soluble antioxidant is its rapid synthesis (within 4 hours) after the cessation of drought. The data obtained by us and investigated in the literature data indicate an important role of Amarantin in photosynthetic, metabolic, and protective reactions of an amaranth plant.
Consequently, the data found in literary sources and the results received by us prove that
3. Conclusions
In the present study, the representatives of species C4 (amaranth)
The leaves of
The present study showed that the
Acknowledgments
The reported study was funded by RFBR and BRFBR, project number 20-516-00012. The reported study was also funded by BRFFR-project number B20R-298.
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