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TAMARIX SPECIES AS A SECONDARY SELENIUM ACCUMULATORS: THE IMPORTANCE IN HUMAN NUTRITION AND MEDICINE

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ABSTRACT.
Many species of the Tamaricaceae family are medicinal plants capable to accumulate high levels of macro- and micro- elements. To evaluate the ability of these plants to accumulate selenium (Se) in temperate climate and Southern areas of Russia several Tamaricaceae representatives (Tamarix ramosissima, T. tetrandra, T. litwinowii, T. hohenackeri, and Myricaria bracteata) were investigated. The highest Se levels (1276–6235 µg kg-1 d.w.) were registered in T. tetrandra from the Crimean southern sea shore (Karadag and Yalta), in T. ramosissima from the Baskunchak Nature Reserve (Astrakhan region, 1015 µg kg-1 d.w.), and Myricaria (Ossetia, 676 mcg kg-1 d.w.), contrary to the Tsitsin Main Botanic Garden collection (T. ramosissima, T. litwinowii, T. hohenackeri) grown on Se deficient soils (soil Se was equal to 240 µg kg-1 d.w.; plant Se concentrations 44–55 µg kg-1 d.w.). The results confirm the belonging of Tamarix species to the group of secondary selenium accumulators and indicate high significance of T. tetrandra and T. ramosissima from the Crimean peninsula and Astrakhan region in the human Se status optimization due to not only high Se levels but also to high antioxidant activity (86–135 mg GAE g-1 d.w.) and polyphenol content (14.5–31.4 mg GAE g-1 d.w).  Half of the Se RDA level (35 µg day-1) may be provided by the consumption of 5 g of the Tamarix leaves from the Karadag Nature Reserve, 30 g – from Yalta, 35 g – from the Baskuncgak Nature Reserve and 60 g of Myricaria bractiata leaves from Ossetia. The results confirm the pharmacological importance of Tamarix leaves from the southern regions of Russia due to the significant content of biologically available Se and natural antioxidants.

KEYWORDS:  T. tetrandra, T. ramosissima, Myricaria bractiata, T. litwinowii, T. hohenackeri, selenium, antioxidant status, environment.

For citation: Golubkina N., Golubev F., Lapchenko V., Lapchenko H., Naumenko T., Bagrikova N., Pirogov N., Pavlova I., Murariu O.C., Caruso G. Tamarix species as a secondary selenium accumulators: the importance in human nutrition and medicine. Trace elemets in medicine. 2025;26(4):25-34. DOI: 10.19112/2413-6174-2025-26-4-25-34

INTRODUCTION
Human Se deficiency is widespread in many regions around the world affecting about 1 billion people (Jones et al., 2017), which causes the immunity and the antioxidant status decrease, brain activity and reproduction problems, reduces antiviral protection, cardiovascular and oncological diseases, and shortening life expectancy (Genchi et al., 2023; Bai et al., 2025). The problem of the human Se deficiency has worsened during the last years due to the increase of the oxidative stress caused by the intensive environmental pollution, global warming, increase of solar activity, wars, import rejection of cereals rich in Se from endemic regions of the world, and a significant decrease of welfare of nations. Exclusive utilization of domestic wheat in Russia since 2016 with Se levels 3-7 times lower than wheat of USA, Canada and Australia (Golubkina, Alfthan, 1999) caused a dramatic decrease of the human Se status in the country with serum Se decrease 1.25 times in Moscow region and to almost twice in Se deficient Khabarovsk land reaching the critical levels of 45 µg L-1 (Kovalsky et al., 2019). 

Among different approaches to combat the problem of Se deficiency, such as utilization of Se fertilizers (Alfthan et al., 2015), Se biofortification of vegetables and leafy crops (Sarwar, 2020; Skrypnik et al., 2024; Golubkina et al., 2024), utilization of Secontaining premixes in animal breeding and poultry (Sirai et al., 2018), the development of new Biologically Active Supplements containing Se (Sun et al., 2023), synthesis of Se containing amino acids – mimetics of glutathione peroxidase (Poluboyarinov et al., 2022), and utilization of wild plant species with significant Se accumulation ability the latter seems to be especially interesting due to high content of other natural antioxidants, and extremely low cost for the production of the appropriate product.

Despite several attempts to identify new Se accumulators (Golubkina et al., 2020) little is known about the suitability of Tamaricaceae representatives as a source of Se in human nutrition.

Tamarix (tamarisk) genus of the Tamaricaceae family includes 78 species with relatively high adaptability and quick growth recording vast distribution of the plants both in subtropical and temperate areas of the world with different levels of water availability, salinity levels and mean temperature variations (Christenhusz, Byng, 2016). These plants belong to halophyte representatives with a unique property to excrete salt excess via special leaf glands and to develop deep roots of up to 30 m, providing plant survival in severe conditions of high salinity and water deficit (Sookbirsingh, 2010; Sedlakova-Kadukova et al., 2008; Samadi et al., 2013). Though Tamarix shows wide spectrum of utilization as an ornamental (Guerrero et al, 2016), and an anti-erosion plant stabilizing sand dunes (Han et al., 2013), a plant suitable for phytoremediation of soils polluted with heavy metals (Sedlakova-Kadukova et al., 2008; Fawzy et al., 2006), a valuable remedy in traditional medicine, and a component of spices and potables (Guerrero et al., 2016; Bahramsoltani et al.,  
2020), it is considered to be an aggressive weed capable to decrease bioavailability due to intensive allopathic properties (Meinhardt et al., 2015). 

Being considered an aggressive weed in USA and several other countries of the world (Mein-hardt et al., 2015) Tamarix displays at the same time unique medicinal properties highly valued in traditional medicine as an anti-diabetic, anti-carcino-genic, bactericidal, wound healing, anti-infectional, anti-inflammatory, liver, and spleen protection remedy (Abdelgawad, 2017; Chen et al., 2017; Li et al., 2024). It should be specially mentioned that all parts of plant (leaves, bark, roots, flowers) record significant antioxidant and biological activity connected primary with high levels of polyphenols (Bahramsoltani et al., 2020).

Up to date, the ability of Tamarix to accumulate high levels of macro- and micro- elements was investigated regarding the possibility of phytoremediation of the territories polluted with heavy metals and radionuclides (Sedlakova-Kadukova et al., 2008). The ability of Tamarix to accumulate high levels of Se has been documented for Kazakhstan plants grown in semi-desert conditions regardless of their species identity (Suska-Malawska et al., 2019). This fact supposes the possibility of Tamarix utilization in programs of the human Se status optimization. 

The attractiveness of such an approach lies in quick Tamarix growth and the well-known synergism of Se with natural antioxidants, among which polyphenols are the main biologically active components in this genus plants (Bencherif et al., 2020). Nevertheless, up to date, no data exist concerning Se accumulation levels in Tamarix grown both in temperate climate and the Southern part of Russia and about the prospects of such plant utilization as a source of dietary Se and antioxidants. T. ramosissima, T. tetrandra, T. hohenackeri, T. gracilis, and T. gallica are the main Tamatix species of the southern regions of Russia while T. ramosissima, T. hohenackeri, and T. linwinowii compose a Tamatix collection of the Tsitsin Main Botanic Garden in Moscow (Kostina et al., 2020). 

The present investigation aimed: (i) to evaluate the ability of Tamarix species (T. ramosissima, H. hohenacheri, and T. litwinowii) to accumulate Se in temperate zone (Moscow), (ii) indicate the values of Tamartix Se accumulation at the Crimean peninsula 
(T. tetrandra), Astrakhan region (T. ramosissima), and of Myricaria bracteata in Ossetia, and (iii) reveal the levels of plant antioxidant status in these conditions.
 
MATERIAL AND METHODS 
Sample Preparation 
Research was carried out to assess Se and antioxidant status in Tamarix species: T. ramosissima Ledeb., T. hohenackeri Bunge, and T. litwinowii Gorschk. grown in the Tsitsin Main Botanic Garden of Moscow, T. ramosissima from Astrakhan region (the semi-desert area; Baskunchak Nature Reserve) (Figure 1, см. в  в приложенном pdf-файле), T. tetrandra Pall. ex M. Bieb from the Crimean Peninsula, and of Myricaria bracteata Royle (Tamaricaceae family) from the Northern Caucasus (Table 1; Figure 1, см. в  в приложенном pdf-файле).

Leaves of the Tamarix species analyzed were gathered from plants grown in August 2023-2024. The objects of the investigation and geographical coordinates of sampling places are presented in Table 1. The leaves were dried to constant weight at room temperature and after additional homogenization of probes the obtained powders were used for the determination of Se, the total antioxidant activity (AOA), and polyphenol (TP) content. Utilization of dried leaf samples provided the opportunity to use representative probes which is extremely important due to small sample weight used in the analysis.

Selenium 
Plant Se was analyzed using the microfluorimetric method according to Alfthan (Alfthan, 1984). Dried homogenized samples were digested via heating with a mixture of nitric and perchloric acids, subsequently, selenate (Se+6) was reduced to selenite (Se+4) with a solution of 6 N HCl, and a complex between Se+4 and 2,3-diaminonaphtalene (piazoselenol) in the presence of 1.25 % EDTA solution was used for the quantitative Se assessment. 

The calculation of the Se concentration was done by recording the piazoselenol fluorescence value in hexane at 519 nm λ emission and 376 nm λ excitation. Each determination was performed in triplicate. The precision of the results was verified using the Mitsuba reference standard of Sefortified stem powder in each determination, with a Se concentration of 1865 µg kg−1 (Federal Scientific Vegetable Center). The detection limit of the method was 0.8 ng per probe.

Preparation of Ethanolic Extracts
Half a gram of dry homogenized leaf powder was extracted with 20 mL of 70% ethanol at 80 °C over 1 h. The mixture was cooled down and quantitatively transferred to a volumetric flask, and the volume was adjusted to 25 mL. The mixture was filtered through a filter paper and used further for the determination of polyphenols and total antioxidant activity.

Total Polyphenols (TP)
Total polyphenols were determined in 70% ethanol extracts of dried samples using the Folin–Ciocâlteu colorimetric method as previously described (Golubkina et al., 2020a). Half a gram of dry homogenates was extracted with 20 mL of 70% ethanol/water at 80 ◦C for 1 h. The mixture was cooled down and quantitatively transferred to a volumetric flask, and the volume was adjusted to 25 mL. The latter mixture was filtered through a filter paper, and 1 mL of the resulting solution was transferred to a 25 mL volumetric flask, to which 2.5 mL of saturated Na2CO3 solution and 0.25 mL of diluted (1:1) Folin–Ciocâlteu reagent were added. After adjusting the volume to 25 mL with distilled water the solutions were kept at room temperature for 1 h., and the concentration of polyphenols was calculated according to the absorption of the reaction mixture at 730 nm. As an external standard, 0.02% gallic acid was used. The results were expressed as mg of gallic acid equivalent per g of dry weight (mg GAE g-1 d.w).

Antioxidant Activity (AOA) 
The antioxidant activity of Tamarix leaves and bark was assessed on 70% ethanolic extracts of dry samples using a redox titration method (Golubkina et al, 2020a). The values were expressed in mg gallic acid equivalents per g of dry weight (mg GAE g-1 d.w.). 

Statistical Analysis 
The presented results are the mean values of three replicates of each sample. The data were processed by the analysis of variance (ANOVA) and the Principal Component Analysis (PCA) and mean separations were performed through Duncan’s multiple range test, with reference to the 0.05 probability level, using the SPSS software version 28.  

RESULTS AND DISCUSSION
Selenium Accumulation
The comparison of Se accumulation levels by Tamarix leaves from the Tsitsin Main Botanic Garden of Moscow with other Tamarix species from the Southern regions of Russia: semi-desert of Baskunchak Nature Reserve, Mediterranean zone of Yalta  
and Karadag, and with Myricaria bracteata of Caucasus Ossetia indicated significant relationship between the Se accumulation and the place of habitat and showed species differences in the ability to accumulate Se (Figure 2, см. в  в приложенном pdf-файле). Indeed, among T. ramosissima, T. hohenackeri, and T. litwinowii grown in the Tsitsin Main Botanic Garden of Moscow with Se concentration range of 0.044–0.055 mg kg-1 d.w., T. ramosissima demonstrated the lowest Se level while in conditions of high soil salinity at the territory of Bogdinsko-Baskunchak Nature Reserve this plant provided 25 times higher leaf Se concentrations. Contrary, Se was not detected in T. ramosissima of Uzbekistan (Valizhonova, 2023) which may relate to the extremely high temperature during leaf drying (600 oC) resulting in dramatic losses of volatile Se.

The above-mentioned results were in accordance with the literature data about a broad Se concentration range recorded for T. ramosissima grown in USA from less than 0.100 up to 1.89 mg kg-1 d.w. (Sorensen et al., 2009). Furthermore, the latter authors demonstrated that at an average of 1.250 mg Se kg-1 d.w., Setreated T. ramosissima had as much Se as hyperaccumulator plants (plants that accumulate > 1.000 mg Se kg-1 f.w.) (Reeves, Baker, 2002), which suggests high Tamarix plasticity and adaptability.

On the other hand, not only the value of soil bioavailable Se affect the accumulation of the element in plant tissues. Indeed, the intensity of solar radiation effect on the levels of Se accumulation may vary considerably depending on the environmental conditions, and species differences (Germ et al., 2005). Different investigations suggest that increased solar radiation can lead to higher Se accumulation in certain plant species, particularly under Serich condition, though the amount of soil bioavailable Se effect dominates. 

Among different Tamarix species, T. ramossisima is the most studied due to its wide distribution worldwide (Sultanova et al., 2001). Contrary, Se accumulation by T. hohenackeri, T. litwinowii, and Myricaria bracteata has never been described previously. In any case, the results prove high dependence of plant Se concentrations on geochemical peculiarities. In this respect, the Crimean and the Baskunchak Nature Reserve Tamarix species seem to be the most powerful sources of Se capable to accumulate from 0.6 to 6.0 mg Se kg-1 d.w. contrary to the species grown in Moscow region with relatively low content of the element in soils (about 240 µg kg-1 d.w.) and in Tamarix leaves (Figure 2, см. в  в приложенном pdf-файле).

Thus, among the tested Tamarix species from the southern regions, T. tetrandra showed Se concentration up to 6235 µg kg-1 d.w. at the territory of ancient volcano (Karadag) which was 5 times higher compared to the Se levels in leaves of T. tetrandra grown in Yalta. In Serbia T. tetrandra plants were able to accumulate up to 16 mg Se kg-1 d.w. of leaves in conditions of the restoration of chronosequence fly ash deposits (Kostic et al., 2022).

The revealed differences in Se accumulation entails that Tamarix plants belong to a group of Se indicators or secondary accumulators (White, 2016), capable to accumulate high levels of this microelement in regions with high soil selenium content. In this respect 50% of Se RDA may be compensated by the consumption of 5 g of the Tamarix leaves from Karadag, 30 g from Yalta, 35 g from Baskunchak and 60 g of the Myricaria bracteata leaves from 
Ossetia.

As far as the Crimea is concerned, the extremely high variability in the content of Se may be connected with the uneven distribution of elements in the mountainous areas. Thus, the previous results on the effect of habitat on this parameter in Allium ursinum of the Chechen republic, where Se content was in the range of 41–1775 µg kg-1 d.w. (10 settlements) (Amagova et al., 2020), indicates the differences reaching 43 times! For T. ramosissima the differences were equal to 23.3 times, and 4.9 times for T. tetrandra. Analogically, great variations in the Se content in the Tamarix species of Kazakhstan reached 15 and the Se concentrations in plant leaves were in the range of 0.42–6.31 mg kg-1 d.w. with M±SD equal to 2.19±1.64 mg kg-1 d.w. (the CV value was 74.9%). In this respect, plants of the Se indicator group may be used in the monitoring of the Se status in the environment. In USA the registered Se concentration range in T. ramosissima was equal to (<0.136–1.809 mg kg-1 d.w.)(Sorensen et al., 2009).

Parameters of Antioxidant Status
The significance of high Se levels in leaves of Tamarix from the southern regions of Russia is strengthened by the high antioxidant status of both leaves and bark of Tamarix species (Figure 3, см. в  в приложенном pdf-файле), as it is well known that Se demonstrates a synergism with natural antioxidants (Ikram et al., 2024).

The results presented on Figure 7 indicate high levels of the total antioxidant activity and the polyphenol content in leaves of all Tamarix species 
tested regardless of the place of habitat which was in accordance with the Tamarix antioxidant status evaluation for plants grown in Kazakhstan.  According to literature data, 50% acetone extract showed 5.84–6.9% of phenolic acids in Kazakhstan Tamarix hohenackeri stems and leaves and 6.32–6.81% for T. ramosissima with the corresponding 2.76–3.51% of flavonoids (Bikbulatova, Korul’kina, 2001). Investigation of Karpova et al (Karpova et al, 2025) demonstrated high polyphenol content also in Miricaria species. According to this study, Myricaria extracts contain flavonoid aglicones, ellagic acid and its derivatives. High polyphenol content was indicated previously in T. ramossisima grown in Kazakhstan with tamarixetin (3,3,5,7-tetrahydroxy-4-methoxyflavone) as the main leaf flavonoid (Sultanova et al., 2001).

In this respect, it is important mentioning that Tamarix litwinowii Gorschk antioxidant status has been described in the present work for the first time. 

CONCLUSIONS 
The revealed differences in the Se accumulation by 5 Tamaricaceae representatives tested indicate high utilization prospects of plants grown in the southern regions of Russia as a valuable source of dietary selenium and natural antioxi-dants. High tolerance of Tamarix and Myricaria to elevated concentrations of the element in the environment supposes the possibility of Se bio-fortification of plants grown in moderate climate with low soil Se which might become the basis of new functional food production valuable both in human nutrition and the maintenance of human health.

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Information about the authors:

Nadezhda A. Golubkina – Dr.Sc. (Agric.), Chief Research Scientist, Analytical Laboratory Department 
E-mail:  segolubkina45@gmail.com; https://orcid.org/0000-0003-1803-9168

Fedor V. Golubev –Ph.D. (Biol.), Research Scientist, Laboratory of Environmental Biogeochemistry 
E-mail: f.v.golubev@mail.ru; https://orcid.org/0000-0001-7401-5705; SPIN-код: 6311–8229 

Vladimir A. Lapchenko – Research Scientist, Department of Biodiversity Study and Environmental Monitoring
E-mail: ozon.karadag@gmail.com  

Helene V. Lapchenko – Engineer, Department of Biodiversity Study and Environmental Monitoring
E-mail: elenalapchenko@gmail.com

Tatiana S. Naumenko – Ph.D. (Agric.), Leading Research Scientist, Laboratory of Aromatic, 
Medicinal and Essential Oil Plants
E-mail: tanya_yalta@inbox.ru; https://orcid.org/0000-0003-1220-4927  

Natalia A. Bagrikova – Dr.Sc. (Biol.), Chief Research Scientist, Department of Natural Ecosystems
E-mail:  nbagrik@mail.ru; https://orcid.org/0000-0002-2305-4146 

Nikolay G. Pirogov – Deputy Director for Research
E-mail: npirogov2017@yandex.ru

Irina V. Pavlova – Research Scientist, Natural Flora Laboratory
E-mail: irpavlova@list.ru

Otilia Cristina Murariu – Professor, Faculty of Food Technology
E-mail: otilia.murariu@iuls.ro; https://orcid.org/0000-0002-9612-6198 

Gianluca Caruso – Professor, Department of Agricultural Sciences 
E-mail: gcaruso@unina.it; https://orcid.org/0000-0001-6981-852X 

Conflict of interest 
The authors declare no obvious and potential conflicts of interest related to the publication of this article.

Funding
The investigation was achieved according to the agreements between Federal Scientific Vegetable Center, 
Bogdinsko-Baskunchak Nature Reserve, and T.I. Vyazemsky Karadag Scientific Station, and within the state assignment 
of the Vernadsky Institute of Geochemistry and Analytical Chemistry of the Russian Academy of Sciences, 
and T.I. Vyazemsky Karadag Scientific Station theme № 124030100098-0 ‘Investigation of biotic 
and abiotic ecosystem components in different climatic conditions’ and did not receive any special funding.

Author Contributions 
Conceptualization: N. Golubkina, F. Golubev, and G. Caruso; investigation: N. Golubkina, F. Golubev, T. Naumenko, H. Lapchenko, and V. Lapchenko; methodology: N. Bagrikova; formal analysis: O. Murariu and V. Lapchenko; data curation: N. Pirogov and V. Lap-chenko; validation: N. Golubkina, I. Pavlova, O. Murariu, and G. Caruso; writing original draft: N. Golubkina, I. Pavlova; writing, re-view and editing: N. Golubkina, F. Golubev, and G. Caruso. 
All authors have read and agreed to the published version of the manuscript.