Variation of Elemental Composition of Leaves in Nitraria schoberi L. and N. sibirica Pall. Depending on Edaphic Growth Conditions

Halophytes are a diverse group of plants with high salt tolerance. Due to their tolerance of salinity and of low availability of nutrients, these plants hold promise for the development of agriculture in extreme environments and can be used for the restoration of saline soils and for phytoremediation (Agudelo et al., 2021). To manage adaptations of valuable cultivated halophytes, it is necessary to understand the mechanisms of salinity tolerance formation, including osmotic regulation, succulence, ion transport and uptake, antioxidant systems, maintenance of redox and energy status, and incorporation and/or excretion of salts (Lokhande and Suprasanna, 2012).

It is known that mineral composition of plants is determined both by soil/geochemical growth conditions and by characteristics of mineral metabolism characteristic of various taxa (Broadley et al., 2004; Watanabe et al., 2007). There are complex relations between salinity and the absorption of nutritional minerals (elements) by plants, as shown in some studies on the effect of salt stress on the absorption of macro- and microelements in laboratory experiments (Eom et al., 2007; Lotfi et al., 2009). An increase and a decrease in concentrations of macro- and microelements under salt stress have been demonstrated in plants, in addition to the absence of such an influence of salt stress (Bekmirzaev et al., 2021).

Owing to their physiological characteristics, halophytes are concentrator plants and are capable of accumulating a substantial amount of easily soluble salts in their tissues (Prokopyev, 2001); this property makes them promising plant species for phytoremediation (Ahmadi et al., 2022). Control over the content of microelements in plants is also necessary because many halophytes are a source of biologically active compounds and can serve as valuable nutritional and medicinal raw materials (Agudelo et al., 2021).

The genus Nitraria L. (Nitrariacea) includes 11 species of shrubby euhalophytes occurring in steppe and desert regions of Asia Minor, Central and Middle Asia, Southeast Europe, North Africa, and Australia on various types of saline soils, often along banks of bitter-salty water bodies (Li et al., 2012; Yang et al., 2012; Banaev et al., 2023a, 2023b). Steppe and semidesert areas where Nitraria species grow are characterized by sulfate and soda landscapes with anomalous levels of Cu, Zn, B, Mo, Mn, Co, F, and Li in soils (Taisaev, 1994).

Nitraria is a promising medicinal, reclamation, and fruit crop (Khan and Qaiser, 2006; Banaev et al., 2014). Currently, the most active research on Nitraria species is being conducted in countries where the problem of salinization and desertification is serious: Australia, Algeria, Egypt, Israel, Kuwait, and China. In recent years, interest in this genus grew considerably, including the identification of the cytotoxic effect of leaf extracts (Boubaker et al., 2015) and their antiviral activity, in particular against influenza A viruses of subtypes H5N1 and H3N2 (Zheleznichenko et al., 2018; Kurskaya et al., 2022). Potential usefulness of N. sibirica Pall. and N. schoberi L. for medicinal purposes has been demonstrated, and ecological-geographical and taxonomic features of the profile and levels of phenolic compounds have been identified in leaves of these plants (Banaev et al., 2015; Voronkova et al., 2017); some patterns of occurrence of these species depending on habitat salinity have been revealed (Khudjaev and Banaev, 2012).

The purpose of the present work was to identify ecological and biochemical features of N. schoberi and N. sibirica in various habitats of Siberia via investigation into the variation of elemental composition in a soil–plant system.

The study on the variation of levels of macro- and microelements in soil and leaves of plants in natural populations of N. schoberi and N. sibirica was conducted in the 2010–2014 period in Siberia within the Kulunda Plain, the Ob Plateau, and intermountain basins in the Altai–Sayan infolded region (Chuya, Minusinsk, Turano-Uyuk, Ulug-Khem, and Uvs-Nuur basins); three populations of N. schoberi and nine populations of N. sibirica were analyzed (Table 1).

The chemical elements (K, Na, Ca, Mg, Fe, Mn, Zn, Cu, Ni, Li, Sr, and Cd) in each soil–plant system were studied by the method of conjugate selection and analysis of soil and plant samples (leaves). Each sample was a pool of 10 plants from each population. Soil samples were taken from the mineral nutrition zone (0–30 cm) of these plants, and a pooled sample was compiled likewise to determine elemental, chemical, and salt composition. Leaves were collected from plants in the generative age state (g), mainly at the stage of fruit ripening. In population N. schoberi_Bagan, for comparative analysis, additional samples were taken from plants in the virginal age state (v) and from adult plants that were a poor general condition (gs). In population N. schoberi_Malinovoe, samples were taken from two plots (Malinovoe_1 and Malinovoe_2) having different degrees of salinity. Furthermore, in population N. sibirica_Balansor, samples were collected along the contour of the lake basin: on the shore of the lake: Balansor_1, in the middle part of the slope: Balansor_2, and in the upper part of the slope: Balansor_3. In population N. sibirica_Balansor, leaves were collected from generative plants at the budding stage.

The soils were diagnosed by standard methods (Klassifikatsiya i diagnostika…, 2004). In an aqueous extract from soils (soil/distilled water ratio of 1 : 5), concentrations of cations (K, Na, Ca, and Mg) and anions (\({\text{HCO}}_{3}^{ - }\), \({\text{SO}}_{4}^{{2 - }}\), and Cl⁻) were determined. Cations were quantified by the atomic absorption technique on a Kvant-2mt atomic absorption spectrometer (Russia). \({\text{HCO}}_{3}^{ - }\) ions were quantified by titration with an H₂SO₄ solution having a concentration of 0.02 mol/dm³. Cl⁻ ions were quantified by the Mohr argentometric method (titration of the Cl⁻ ion in the aqueous extract with a solution of AgNO₃ having a concentration of 0.02 mol/dm³). \({\text{SO}}_{4}^{{2 - }}\) ions were quantitated by the gravimetric method after their precipitation from the aqueous extract by means of a 10% solution of BaCl₂. The CaCO₃ content was determined on a KM-04 calcimeter (Russia) after treatment of a soil sample with a HCl solution (1 : 3). pH of the aqueous suspension (soil/distilled water ratio 1.0 : 2.5) was determined by the potentiometric technique on an ITAN pH meter/ionomer (Russia) with an ESK-10601 combined glass electrode (Russia). The number of particles smaller than 0.01 mm (physical clay) was determined by the pipette method (GOST 12536-2014, 2019). The organic-matter content was quantified by a photometric approach that is based on the oxidation of soil organic matter by K₂Cr₂O₇ in H₂SO₄ with subsequent quantitation of trivalent Cr, which is equivalent to the amount of organic matter in the soil, on a PE-5400UF spectrophotometer (Russia) at a wavelength of 590 nm.

Mobile forms of elements were extracted from soils with CH₃COONH₄ buffer having рН 4.8 (soil/buffer ratio 1 : 10), and their concentrations were measured on the Kvant-2mt atomic absorption spectrometer (Russia). Levels of chemical elements (K, Na, Ca, Mg, Fe, Mn, Zn, Cu, Ni, Li, Sr, Cd, and Pb) in the leaves of nitre bushes were determined by the atomic absorption method after ashing of the plants in a SNOL 8,2/1100 muffle furnace (Russia) at 525°C with subsequent preparation of an ash solution via treatment of the resulting ash with a mixture of concentrated HNO₃ and 30% H₂O₂.

The intensity of biological absorption of elements by plant leaves was assessed with the help of the coefficient of biogeochemical mobility (B_x) calculated as the ratio of an element’s concentration in plant dry matter to the concentration of the mobile form of the element in the soil (Perelman and Kasimov, 1999).

The studied habitats of N. schoberi and N. sibirica were found to have high heterogeneity of physical and chemical properties of soils (Fig. 1, Tables 2 and 3). Soils of the Nitraria habitats in intermountain basins of the Altai–Sayan infolded region differed from soils in areas of the Kulunda Plain by heavier granulometric composition and, accordingly, a higher concentration of physical clay. In all analyzed populations of nitre bushes, the soil was alkaline: pH varied from 7.6 (slightly alkaline) to 9.8 (very alkaline). Total salt ranged from 0.07 to 3.23%. In terms of the type of soil salinity, the soils were of chloride, sulfate–chloride, chloride–sulfate, sulfate, and soda–sulfate types. In the habitats of N. schoberi and N. sibirica, predominant cations were Na and Ca; among anions, in populations of N. schoberi, Cl⁻ predominated, and in populations of N. sibirica, \({\text{SO}}_{4}^{{2 - }}\) was dominant. The ranges of variation of these parameters were very wide in the habitats of both species.

Soils of the studied habitats of N. schoberi are characterized by a lower concentration of CaCO₃ (1.0–3.8%) and physical clay (6–19%) as compared with the soils in the habitats of N. sibirica: 1.2–18.2% and 15–40%, respectively. When both species grow in one habitat, soils under N. schoberi contain less CaCO₃ (2.5%) than do soils under N. sibirica (3.6%) (Fig. 2).

Linear relations were revealed between physical properties of soils and levels of individual elements needed for plant nutrition. With an increase in the physical-clay content of soils, levels of mobile Na and of Cu (p ≤ 0.01), Ca and Mn (p ≤ 0.05) as well as of Cd (p ≤ 0.001) increased. In the soils under N. sibirica populations Kosh-Agach, Tobeler, Ulug-Kol, Hadyn, and Shara-Nur, high concentrations of CaCO₃ were noted, which positively correlated with levels of mobile Ca, of Li, Sr, and Ni (p ≤ 0.001). A strong positive association was found between total salt and the concentration (in it) of water-soluble Na, Ca, Mg, and Cl⁻ and of the mobile form of Na (p ≤ 0.001). For instance, in the soil of population N. sibirica_Tobeler, the highest concentration of mobile Na (14.5 g/kg) was noticed, as was the highest level of total salt (among the investigated populations of nitre bushes): 3.23%. The situation was similar in the habitats of N. schoberi: along with the highest total salt (0.5%) at locality Malinovoe_1, the highest concentration of mobile Na (2.3 g/kg) in the soil was observed there. With an increase in the level of water-soluble Na cations in the soil, concentrations of water-soluble forms of Ca, Mg, Cl⁻, and \({\text{SO}}_{4}^{{2 - }}\) increased, as did levels of mobile forms of Mg and Cu (p ≤ 0.01). It is worth noting strong positive interdependence of such substances as Na, Mg, Ca, Cl⁻, and \({\text{SO}}_{4}^{{2 - }}\).

The investigated species showed a wide range of variation of levels of the analyzed macro- and microelements in leaves (Table 4). Among vitally important (essential) elements, Fe (27 to 361 mg/kg) and Mn (9 to 264 mg/kg) featured the greatest variation.

Linear positive relations were detected between the level of mobile or water-soluble Na in the soil and the extent of accumulation of Ca, Mg, Zn, Cu, and Cd in leaves of N. schoberi and N. sibirica plants. With increasing soil salinity, a higher concentration of Ca, Mg, Zn, Cd, and Sr was observed in the leaves (Table 5).

On soils with a high carbonate content, levels of Ca and Ni in plants were significantly higher. For example, in the leaves of N. sibirica_Shara-Nur plants, the greatest extent of accumulation of Ca (19.9 g/kg) and Ni (8.2 mg/kg) was registered, while in soils at this site the highest concentrations of CaCO₃ (18.2%) were found. Levels of Mg, Cu, and Mn in leaves of nitre bushes were positively associated with the physical-clay content of soils. On heavy loamy soils, in N. sibirica_Gornyak plants, the greatest extent of accumulation of Mg (11.6 g/kg) was noted, and the highest concentrations of Cu and Mn in leaves (32.8 and 264 mg/kg, respectively) were detected in population N. sibirica_Hadyn. On highly saline soils, the concentration of Zn in the plant leaves significantly increased with increasing concentrations of Na, Ca, Mg, and total salt in the soils. The concentration of Ni in plant leaves was positively associated with an increase in the levels of mobile forms of Ca, Sr, Ni, and Li in soils. The concentration of Cu in leaves of nitre bushes went up with increasing levels of mobile forms of Na, Ca, and Cu in soils.

Physiologically important ratios of the levels of macro- and microelements in the leaves of the analyzed nitre bush species (K/Na and K/Ca, associated with the transport of mineral-nutrition elements in plant organs, as well as Cu/Zn, associated with enzyme synthesis) manifested very wide of variation (Table 6). Ratios Ca/Mg and Ca/Na proved to be stabler; in the leaves of both species, the Ca/Na ratio was within 0.12–0.33, while Ca/Mg was within 1.15–2.34.

Quantification of uptake of macro- and microelements by N. schoberi and N. sibirica suggested that for all analyzed elements, B_x is >1.0 (Fig. 3a). Both species very actively take up macroelements K and Na, and in N. sibirica, the accumulation coefficient is 3 and 5 times lower, respectively, than that in N. schoberi. Among microelements, Fe, Cu, and Zn are taken up most intensively by the two species. The accumulation coefficient of Fe, Cu, and Zn for N. schoberi leaves is lower than that of N. sibirica leaves by 6-, 2-, and 1.5-fold, respectively.

In the plant leaves, significant interspecific differences were revealed in the content of the main elements needed for mineral nutrition (Figs. 3b–3d). In N. sibirica leaves, concentrations of K, Mg, and Zn were 1.3–1.5 times higher than those in the leaves of N. schoberi, whereas concentrations of Ca, Fe, Mn, and Cu were 1.8–1.9 times higher and Sr concentration 2.5 times higher. At the same time, both species are capable of accumulating similar (very high) concentrations of Na in leaves (N. schoberi: up to 83.8 g/kg and N. sibirica: up to 77.2 g/kg) (Table 4).

In population N. schoberi_Bagan, it was found that young plants are located closer to water’s edge on soils with higher salinity (total salt concentration was 5.5 times higher) and higher levels of Na, Fe, and Mn (7.5-, 2.9-, and 1.7-fold, respectively) as compared to habitats of adult plants (Fig. 4). Plants in the virginal age state accumulated K and Na in leaves 7 times more than adult generative plants did, while Mg and Ca were accumulated 3–5 times more (Fig. 5). Analysis of adult plants that were in a poor general condition indicated significantly higher concentrations of Mg and Na (8- and 10-fold, respectively) in the leaves of these plants as well as lower ratios K/Na, Ca/Mg, and Ca/Na (2-, 3-, and 4-fold, respectively) as compared to healthy plants. Apparently, an imbalance between these macroelements had an adverse effect on the health of these plants.

In population N. sibirica_Balansor, the highest salinity was observed on the shore of the lake (Balansor_1) and in the middle of the slope (Balansor_2) (Table 7). On the shore of the lake, the level of mobile forms of Fe and Mn in the soil was higher (Fig. 6). With increasing distance from the lake, as soil salinity declined and levels of mobile forms of Na, Ca, Mg, Zn, Sr, Li, and Cd in soil diminished, there was a tendency for the concentrations of these elements to decrease (∼1.5-fold) and for levels of K, Fe, and Mn in leaves of N. sibirica plants to rise (Figs. 7a–7c). Besides, with increasing soil salinity, a decrease in physiologically important ratios Fe/Mn, Cu/Zn, K/Ca, and K/Na by 1.6–2.4-fold was observed in the leaves of N. sibirica plants (Fig. 7d).

Our examination of soils in the habitats of the two species of the genus Nitraria showed that N. schoberi is more often found on lighter soils with lower salinity as compared to soils in the habitats of N. sibirica, consistently with data presented in a study by Petrov (1964). According to the results of analyses in Central Asia and Kazakhstan, that author characterized N. schoberi as a psammophytic halophyte growing on slightly saline sands, whereas N. sibirica is more often found on meadow-type saline soils. Krupennikov (1944) reports that in Naurzum Nature Reserve (Kazakhstan), N. schoberi occurs on soils of various mechanical compositions, including those with a high carbonate content. Nonetheless, this plant prefers lighter soils and achieves the best development on silted saline sands. That author stated that nitre bushes, just as other halophytes, are calciphiles and basiphiles. In a paper by Mojiri and Jalalian (2011), it was demonstrated that increased percentage concentrations of Na, HCO₃, and physical clay in the soil of habitats of N. schoberi (Isfahan province, Iran) negatively affected physiological parameters of plants, while an elevated CaCO₃ concentration had a positive influence. At the same time, the percentage concentration of gypsum (CaSO₄) did not have a significant impact on the physiological parameters of these plants.

In Siberia, N. schoberi and N. sibirica plants grow on different types of soils of various granulometric compositions and degrees of salinity. N. sibirica can grow on soils with wider variation of Na concentration as compared to N. schoberi. This difference may be due to the fact that the studied populations of N. sibirica are confined to soils with a high CaCO₃ content. It is known that on carbonate soils, the toxic effect of high Na concentrations on plants is attenuated (Orlov, 1992; Jafari et al., 2006). In the soil solution, Na cations can be displaced from the soil absorption complex and replaced by Ca. The method of gypsuming of alkaline soils proposed by Giedroyts (1955) is based on this reaction.

It has previously been established experimentally that an increase in the concentration of NaCl in the soil solution causes an increase in the Ca level and a decrease in Fe concentration in the soil (Bekmirzaev et al., 2021). On carbonate soils, the high concentration of CaCO₃ has positive linear relations (characteristic of these soils) with elements Ca, Li, and Sr. Ni is also often associated with these soils and accumulates in appreciable quantities in plant leaves. We noticed similar patterns in the soils of natural habitats of nitre bushes.

Currently, there is little information about changes in elemental composition of plants in natural populations of Nitraria species, especially correlations with concentrations of elements in the soil. Amanova et al. (2023) investigated levels of elements in the soil of habitats of N. schoberi in the Southern Aral Sea region (Uzbekistan) as well as in various organs of this species (roots, leaves, fruits, and seeds). In those N. schoberi plants, more than 30 elements were identified, including radioactive and rare-earth ones. A large number of research articles are focused on experimental analyses of shifts in levels of macro- and microelements within plant organs under salt stress. In most of these studies, only one or a few elements, such as Na, K, and/or Fe, are quantified (Chen et al., 2005; Nazar et al., 2011; Yousfi et al., 2007). An increase in concentrations of Na and Cl in the roots, stems, and leaves of various plant species, including N. sibirica and N. tangutorum Bobr., has been detected with increasing salinity (Sheng et al., 2012). It was found there that, depending on tolerance to the degree of salinity, certain taxa demonstrate different responses to an increase in the concentration of salts in the soil. With higher salinity of soil, there is a greater extent of accumulation of K and Ca along with preservation of the Na/K ratio in plant organs of the most tolerant species, in particular Solidago cutleri Fernald (Eom et al., 2007) and Portulaca oleracea L. (Bekmirzaev et al., 2021). At increasing concentration of salts, the most resistant varieties of Juglans regia L. also accumulate K and Ca (Lotfi et al., 2009). A study on mechanisms of salt tolerance in various Arabidopsis thaliana (L.) Heynh. genotypes indicates that in plants of this species carrying the AtHKT1;1 gene, levels of K, P, S, and Mn go up more than in other genotypes under salt stress, and Na concentration diminishes significantly (Hill et al., 2013).

Our findings about the variation of mineral composition of leaves in N. schoberi and N. sibirica plants depending on soil conditions are not fully consistent with laboratory studies about the influence of salinity levels on concentrations of macro- and microelements in the leaves of halophytes. It is believed that salt stress not only limits the uptake of macroelements but also affects the absorption of microelements, in particular their concentration decreases significantly with increasing concentrations of Na salts (Kirmizi and Bell, 2012; Kopittke, 2012; Shabala et al., 2010). In a laboratory experiment, under salt stress applied to N. sibirica, a decrease in levels of Ca, Cu, Fe, Mg, and K and elevation of Na concentration was found in roots, stems and leaves; the accumulation of Na and the diminished levels of the other elements caused osmotic stress and affected metabolism (Li et al., 2017). According to our observations in localities with a higher total salt content of the soil, the extent of accumulation of Ca, Mg, Zn, Cd, and Sr in plant leaves is greater. A higher level of mobile Na in the soil positively correlated with concentrations of Ca, Zn, and Cu in the leaves. It is possible that under natural conditions, in soil, there are interactions (between elements) that attenuate the toxic effect of salts; an example of such interactions is the mutual influences between Na and Ca already noted above.

A ratio of elements is more informative regarding physiological status of a plant organism, as compared to their individual concentrations. A key feature of plant resistance to salt stress is the K/Na ratio (Tester and Davenport, 2003; Shabala and Cuin, 2008). The mechanism ensuring K/Na homeostasis in N. sibirica organs after treatment with NaCl was demonstrated in the study by Tang et al. (2018a). They found that in seedlings of N. sibirica, under salt stress (elevated concentration of NaCl in the substrate), the Na content of roots, stems, and leaves rises significantly, while the Na content of the leaves is up to 3 times higher than that of the roots. It is thought that the high salt tolerance of halophytes, including N. sibirica, is due to Na transport in a vacuole preventing its adverse effects (Huanyong et al., 2017; Ma et al., 2023).

In an experiment, in seedlings of N. sibirica, the K/Na ratio in organs diminished with increasing concentration of NaCl; at 400 mmol/L NaCl, this ratio was less than 1.0 in leaves (Tang et al., 2018b). We obtained ambiguous results on the relation between the degree of soil salinity and the K/Na ratio in leaves of nitre bushes. A tendency for a reduced K/Na ratio was observed only in some saline habitats of N. sibirica, for example, N. sibirica_Gornyak and N. sibirica_Rubtsovsk (K/Na = 0.11–0.12). Meanwhile, in population N. sibirica_Balansor, our comparison of this parameter with the salinity profile indicated its dependence on the salinity degree.

Adaptation to excess salinity is reflected in alterations at morphological, physiological, and anatomical levels in plants (Zhang et al., 2013; Boughalleb et al., 2009). Among woody plants, nitre bushes are considered “record holders” on salt tolerance because they can withstand high levels of Cl, SO₄, Na, and total salt in upper soil horizons (Kremenskoy, 1953). Amanova et al. (2023) revealed high concentrations of Ca, Cl, K, and Na in organs of N. schoberi. In this context, concentrations of Ca, K, and Na were noticeably lower in the roots of these plants than in the soil, while levels of K, Na, and Cl in the leaves were significantly (2-, 5-, and >10-fold, respectively) greater than those in the soil. We also documented significant accumulation of K and Na in leaves of N. schoberi and N. sibirica.

According to data from Krupennikov (1944), during the vegetative season, N. schoberi significantly accumulates Cl in the leaves. Furthermore, regardless of concentrations of sulfates and chlorides in the habitat soil, the salt content and the ratio of SO₄ to Cl ions in the leaves are similar among N. schoberi plants. Therefore, in nitre bushes, there is a (known for halophytes) ability to regulate ratios of ions. Our results confirm this conclusion. For example, the level of Na can differ by orders of magnitude among habitat soils of N. schoberi and N. sibirica, while the concentration of this element in leaves usually varies by no more than 1.5-fold among nitre bushes (50–80 g/kg). I.A. Krupennikov classifies N. schoberi as a chloride halophyte by pointing out that the Ca/(Na + K) ratio in N. schoberi leaves is 0.11 and is always lower than that in soil. According to our data, Ca/(Na + K) in N. schoberi leaves also averages 0.11, whereas in N. sibirica, it is slightly higher: 0.19.

By means of the K/Ca concentration ratio in a plant, the type of mineral metabolism is determined by researchers: the oxalate type corresponds to K/Ca > 10, the calciotrophic type to K/Ca ≤ 1, and the potassium type to K/Ca > 1 (Horak and Kinzel, 1971). In most of the studied habitats of nitre bushes, at different soil salinity levels, the K/Ca ratio in plant leaves has varied from 1.0 to 3.4, which makes it possible to classify N. sibirica and N. schoberi as plants of the potassium type of mineral metabolism. In some populations of these species in our work, the K/Ca ratio was less than 1.0 (N. schoberi_Malinovoe_2, N. sibirica_Gornyak, N. sibirica_Rubtsovsk, and N. sibirica_Hadyn). The soils of these habitats are characterized by heavier granulometric composition; the physical-clay content significantly (p ≤ 0.01) correlated with the K/Ca ratio in plant leaves, indicating a possible disturbance of mineral nutrition of plants under these edaphic conditions.

A necessary condition for normal plant development is a Fe/Mn ratio of 1.5–2.5 (Kabata-Pendias, 2011). According to our findings, a low Fe/Mn ratio is featured by plants in populations N. sibirica_Rubtsovsk (0.4), N. sibirica_Ulug-Kol (0.35), N. sibirica_Gornyak (0.3), and N. schoberi_Malinovoe (0.5), implying a disturbance in the supply of Fe to the leaves. The highest Fe/Mn ratio was exhibited by plants in population N. schoberi_Bagan (6.4). High concentrations of Fe can be toxic to plants.

The ratio of Cu to Zn levels determines whether the supply of these physiologically important elements is at a ratio appropriate for the processes of enzyme synthesis and is more strictly controlled by biological and physicochemical mechanisms of absorption and concentration of elements (Arzhanova and Elpatyevsky, 1990; Bityutsky, 2020). As a rule, in higher plants, the Cu/Zn ratio features a relatively constant value and, according to our earlier data, varies in the range of 0.1–0.5 among different species, with extreme values typical for habitats in zones of geochemical anomalies (Boyarskikh and Siromlya, 2022). Correlations between the Cu/Zn ratio and antioxidant activity of extracts have also been reported (Hodžić et al., 2013). In the leaves of nitre bushes in our work, the Cu/Zn ratio varied widely: 0.26–2.0 (in N. schoberi) and 0.13–2.15 (in N. sibirica). A significant increase in the Cu/Zn ratio occurred due to more intense accumulation of Cu by plants in populations N. schoberi_Malinovoe (1.4–2.0), N. sibirica_Hadyn (2.15), and N. sibirica_Ulug-Kol (1.9).

The two studied Nitraria species, just as other halophytes, are concentrator plants: the coefficient of biogeochemical mobility (B_x) is above unity. Our analysis of B_x uncovered different intensities of accumulation of certain macro- and microelements by leaves in the Nitraria species, thus confirming the previously reported selectivity of absorption of individual chemical elements from soil by plants, which is genetically determined in different species (Dobrovolsky, 2009). For the two Nitraria species examined here, the highest B_x values are characteristic of macroelements K and Na and microelements Fe, Zn, and Cu. Plants of N. schoberi more intensively accumulate K, Na, Ca, Mg, and Li, while B_x of essential microelements Fe, Mn, Zn, and Cu in this species is significantly lower as compared to N. sibirica. Earlier, Ma et al. (2023) showed that enhanced capacity for K retention and for Fe uptake in N. sibirica plants is crucial for cellular homeostasis and chlorophyll synthesis, respectively.

It is known that certain concentrations of microelements in plants can have toxic effects on animals (Kriterii otsenki…, 1992). According to biogeochemical criteria, maximal permissible levels in plant cuttings and plant-based feed are as follows: Ni, 5 mg/kg of air-dry mass; Cu, 20; and Zn and Fe, 100. In population N. sibirica_Shara-Nur, this limit was exceeded in terms of Ni (8.2 mg/kg) in plant leaves; in populations N. sibirica_Tobeler, N. sibirica_Turan, and N. sibirica_Hadyn, the limit was exceeded in terms of Сu (23, 28, and 33 mg/kg, respectively); in populations N. sibirica_Tobeler, N. sibirica_Turan, N. sibirica_Balansor, and N. sibirica_Hadyn, there was a significant (more than threefold) excess of Fe (114, 141, 197, and 361 mg/kg, respectively). These results must be taken into account when collecting and using plant materials for the preparation of herbal extracts because ~50% of the content of microelements (contained in plants) gets transferred into infusions and decoctions (Gravel et al., 2012; Siromlya, 2014).

The soil and elemental analyses of N. schoberi and N. sibirica populations allowed to reveal specific features of the habitats of these species in Siberia. N. sibirica grows on soils that are more saline and heavier in terms of granulometric composition (usually loams) with high concentrations of carbonates and physical clay. N. schoberi is usually found on light soils: sand or sandy loam. In all the analyzed populations of nitre bushes, soil pH proved to be alkaline: from 7.6 (slightly alkaline) to 9.8 (very alkaline). Total-salt concentration ranged from 0.07 to 3.23%. Soil salinity was of chloride, sulfate–chloride, chloride–sulfate, sulfate, and soda–sulfate types. In the habitats of N. schoberi and N. sibirica, predominant cations were Na and Ca; in N. schoberi populations, Cl⁻ was the predominant anion, and in N. sibirica populations, it was \({\text{SO}}_{4}^{{2 - }}\). A strong positive association was detected between total salt and levels of Ca, Zn, Sr, Mg, and Cd in the leaves of nitre bushes. At the same time, in the leaves of N. sibirica, the concentration of K, Ca, Mg, Fe, Sr, Mn, Zn, and Cu was 1.5–3 times higher than that in the leaves of N. schoberi. It was revealed that both species are capable of accumulating very high concentrations of Na in the leaves, on average 50–80 g/kg, regardless of the level of this element in the soil.

The studied Nitraria species, just as other halophytes, are concentrator plants: the coefficient of biogeochemical mobility (B_x) is above unity. The highest B_x values were found to be typical for macroelements K and Na and microelements Fe, Zn, and Cu. N. schoberi leaves accumulate K, Na, Ca, Mg, and Li more intensively, while B_x of essential microelements Fe, Mn, Zn, and Cu is significantly lower in this species compared to N. sibirica.