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Biological properties of selected Amaranthaceae halophytic species: A review

Abstract

The family Amaranthaceae contains a large number of halophytic species. The aim of this paper is to present a review of biologically significant halophytes in the flora of Serbia belonging to this family. This review includes a description of the following 18 species: Atriplex littoralis L., A. rosea L., A. halimus L., Bassia sedoides Pall., B. scoparia (L.) A.J.Scott., B. prostrata (L.) Beck., Beta trigyna W. et K., Camphorosma annua Pall., C. monspeliaca L., Chenopodium ambrosioides L., Ch. polyspermum L., Ch. vulvaria L., Ch. hybridum L., Ch. album L., Ch. rubrum L., Salicornia europaea L., Suaeda maritima (L.) Dum., Salsola soda L. These species are sources of biologically active substances and have a good potential for multi-purpose applications. Most extracts of these species have been found to exhibit biological activities such as antioxidant, anticancer, antibacterial, antifungal, antiinflammatory and others. The aim of this review is to describe these species including their morphology, distribution, phytochemistry, as well as their use for medicinal and food purposes.

Keywords:
Amaranthaceae; Morphology; Essential oils; Secondary metabolites; Medicinal application

INTRODUCTION

Family Amaranthaceae

Halophytes grow in habitats with an increased concentration of salt in the substrate to which they have adapted in order to survive in saline habitats. One of these adaptive capacities lies in the synthesis of compounds that belong to the group of secondary metabolites. Increased production of secondary metabolites, with pronounced biological activities in halophytes, has received additional attention due to the rapid increase in demand for natural bioactive substances (Stanković et al., 2019Stanković M, Jakovljević D, Stojadinov M, Stevanović ZD. Halophyte species as a source of secondary metabolites with antioxidant activity. Ecophysiology, abiotic stress responses and utilization of halophytes. Springer, Singapore. 2019;289-312.). The plant species belonging to the Amaranthaceae family represent important potential sources of pharmacological substances. Biological activity of these substances has been proven in numerous scientific studies (Ksouri et al., 2011Ksouri R, Ksouri WM, Jallali I, Debez A, Magné C, Hiroko I, et al. Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Crit Rev Biotechnol. 2011;32(4):289-326.; Arya et al., 2019Arya SS, Devi S, Ram K, Kumar S, Kumar N, Mann A, et al. Halophytes: The plants of therapeutic medicine. In: Hasanuzzaman M, Nahar K, Öztürk M, editors. Ecophysiology, abiotic stress responses and utilization of halophytes. Springer; 2019. Cap. 13: p. 271-287.). These plants have been used for their antibacterial, antioxidant, antifungal, and many other biological effects (Stanković, 2019Stanković J. Halophytic plant species - isolation and characterization of secondary metabolites. [Dissertation]. Belgrade: University of Belgrade, Faculty of Chemistry; 2019. (In Serbian); Stevanović et al., 2019).

The Amaranthaceae family includes the formerly called Chenopodiaceae family and contains about 178 genera and 2052 species based on the data provided by ‘The Plant List’ (http://www.theplantlist.org/1.1/browse/A/Amaranthaceae/ accessed 2021-06-25). In previous classifications, the family Amaranthaceae was placed in the order Caryophyllales and included genera and species that were formerly treated as Chenopodiaceae (Christenhusz, Byng, 2016Christenhusz MJM, Byng JW. The number of known plants species in the world and its annual increase. Phytotaxa. 2016;261:201-217.). However, in some publications the name Chenopodiaceae is still used (Gelin, Mosyakin, Clemants, 2003Gelin Z, Mosyakin LS, Clemants ES. Chenopodiaceae. Flora of China. 2003;5:351-414.; Kadereit, Hohmann, Kadereit, 2006Kadereit G, Hohmann S, Kadereit JW. A synopsis of Chenopodiaceae subfam. Betoideae and notes on the taxonomy of Beta. Willdenowia. 2006;9-19.; Tundis et al., 2009Tundis R, Menichini F, Conforti F, Loizzo MR, Bonesi M, Statti G, et al. A potential role of alkaloid extracts from Salsola species (Chenopodiaceae) in the treatment of Alzheimer’s disease. J Enzyme Inhib Med Chem. 2009;24(3):818-824.; Voznesenskaya et al., 2013Voznesenskaya EV, Koteyeva NK, Akhani H, Roalson EH, Edwards GE. Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis. J Exp Bot. 2013;64(12):3583-3604.; Chikhi et al., 2014Chikhi I, Allali H, El Amine M, Medjdoub H, Tabti B. Antidiabetic activity of aqueous leaf extract of Atriplex halimus L. (Chenopodiaceae) in streptozotocin-induced diabetic rats. Asian Pac J Trop Med. 2014;4(3):181-184.).

Plants of this family inhabit arid areas, deserts, coastal and salt habitats. They are widespread in Africa, Asia, Europe, and North and South America (Gelin, Mosyakin, Clemants, 2003Gelin Z, Mosyakin LS, Clemants ES. Chenopodiaceae. Flora of China. 2003;5:351-414.).

Species belonging to this family are mostly herbaceous and annuals, biennials or perennials. Some of them have a succulent structure. They have alternating or opposite leaves. In some species, the leaves are opposite at the base of the stem, whereas they are alternating in the central part. The flowers can be unisexual or bisexual, three-part or five-part and arranged in cluster blooms. The leaves of flower sheath are often protected, more or less succulent. They have 1 to 5 anthers, and the pistil consists of 2 to 5 fertilizing leaves. The fruit is dry and in some genera it opens, while in others remains closed (Gelin, Mosyakin, Clemants, 2003Gelin Z, Mosyakin LS, Clemants ES. Chenopodiaceae. Flora of China. 2003;5:351-414.).

Species belonging to this family are mostly herbaceous and annuals (Atriplex rosea, Bassia sedoides, Chenopodium ambrosioides, Ch. polyspermum, Ch. hybridum, Ch. album, Ch. rubrum, Kochia scoparia, Salicornia europaea, Suaeda maritima, Salsola soda), biennials (A. littoralis, Camphorosma annua) or perennials (Beta trigyna, C. monspeliaca, K. prostrata). Some of them have a succulent structure (A. littoralis, B. sedoides, C. annua, Ch. rubrum, S. europaea, S. maritima, S. soda). They have alternating (B. sedoides, B. trigyna, species of the genera Camphorosma, Chenopodium, Kochia) or opposite leaves (S. europaea, S. soda). In some species, the leaves are opposite at the base of the stem, while in the central part they are alternating (species of the genus Atriplex, S. maritima). The flowers can be unisexual (species of the genus Atriplex) or bisexual (B. trigyna, B. sedoides, species of the genus Camphorosma, Chenopodium, Kochia and species S. europaea, S. maritima, S. soda), three-part or five-part and arranged in cluster blooms. The leaves of the flower sheath are often protected, more or less succulent. They have 1 to 5 anthers, and the pistil consists of 2 to 5 fertilizing leaves. The fruit is dry and in some genera it opens, while in others remains closed.

This review paper will describe some of the most important genera with species belonging to the family Amaranthaceae, namely the genera Atriplex, Bassia, Beta, Camphorosma, Chenopodium, Salicornia, Suaeda and Salsola.

Genus Atriplex

Atriplex littoralis L. is a biennial plant that can reach a height up to 80 cm. It is upright and branched, with green or reddish shoots. The leaves are alternate, succulent, linear, without visible lateral nerves, and with sharply serrated edges. Flower glomerulus is arranged in a leafless inflorescence. The bracts of female flowers are up to 55 mm long, egg-shaped and succulent at the beginning, and later they are dry. The seed has a lateral germinal root. The species is present on a wet sandy, clay or rocky substrate, in an open halophytic vegetation. It mainly grows on solonchak and less often on solonjec. It is widespread in Europe, southwestern and Central Asia (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

A. littoralis has the ability to absorb ions from saline soil and isolate them in the saline glands on the leaf surface. This feature has great importance because it enables this plant to be used for the revegetation of saline or dry/semi-dry soil. The species is used to clone genes responsible for drought and salt tolerance and their introduction into cultivated crops in order to achieve higher resistance of these plants to the mentioned conditions (Benzarti et al., 2013Benzarti M, Ben Rejeb K, Debez A, Abdelly C. Environmental and economical opportunities for the valorisation of the genus Atriplex: New Insights. In: Hakeem K, Ahmad P Ozturk M, editors. Crop improvement: New approaches and modern techniques. Springer; 2013. Cap. 16: p. 441-457.).

By examining the total phenolic content and antioxidant activity of methanolic extracts of its aerial parts, this plant proved to have a high content of phenolic compounds and flavonoids (Table I), as well as a high antioxidant effect (Stevanović et al., 2014Stevanović ZD, Janacković P, Stanković M. Are there still neglected medicinal plants beyond official and traditional consideration? J Arid Environ . 2014;26-32.).

TABLE I
Secondary metabolites of presented halophytic Amaranthaceae species

This plant is a source of secondary metabolites exhibiting various effects such as antimicrobial, antiviral, anticancer, and antioxidant effects (Gođevac et al., 2015Gođevac D, Stanković J, Novaković M, Anđelković B, Dajić- Stevanović Z, Petrović M, et al. Phenolic compounds from Atriplex littoralis and their radiation-mitigating activity. J Nat Prod . 2015;78(9):2198-2204.).

Atriplex rosea L. is an annual plant that reaches a height of 20 to 70 cm. The stem is cylindrical and densely shelled. The leaves are whitish, rarely green and serrated along the rim, with a narrowed base. The lower ones are on a short stalk and rhombic, and the upper ones are sitting and deltoid. The flowers are clustered in a terminal or axillary inflorescence. The bracts are ovoid, unevenly toothed and 4 to 12 mm long. The seeds are shiny and blackish. It is a cosmopolitan species that grows along roadsides, around settlements on dry and saline sites (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

The individuals of this plant species were grown on soil treated with various heavy metals (Cu, Ni, Pb and Zn). The results showed that the exposure of plants to different levels of metals reduced the production of dry matter and influenced the gradual reduction of growth after treatment (Kachout et al., 2009Kachout S, Mansoura AB, Jaffel K, Leclerc JC, Rejeb MN, Ouerghi Z. The effect of salinity on the growth of the halophyte Atriplex hortensis (Chenopodiaceae). App Ecol Environ Res. 2009;7(4):319-332.). Plant growth was inhibited when the species was exposed to high concentrations of these elements. A. rosea can be used in phytostabilization of contaminated soil the reason being that it has a high ability to tolerate the presence of heavy metals in the substrate (Kachout et al., 2015Kachout S, Benmansoura A, Ennajah A, Leclerc JC, Ouerghi Z, Karray Bouraoui N. Effects of metal toxicity on growth and pigment contents of annual halophyte (A. hortensis and A. rosea). Int J Environ Res. 2015;9(2).).

This species is used in nutrition. Its leaves are used to make traditional dishes in some areas of Turkey (Dogan et al., 2015Dogan Y, Nedelcheva A, Łuczaj Ł, Drăgulescu C, Stefkov G, Maglajlić A, et al. Of the importance of a leaf: the ethnobotany of sarma in Turkey and the Balkans. J Ethnobiol Ethnomedicine. 2015;11(1):1-15.).

Atriplex halimus L. is an upright perennial shrub that branches from the base. It can reach a height up to 3 m. The bark is gray-white, and the leaves are 10- 30 mm long and 5-20 mm wide. The leaves can have different shapes, and they taper to a base with a short stalk. During hot and dry summers, it happens that its leaves fall off, even though it is an evergreen plant. Based on differences in morphology, Le Houérou (1992Le Houérou HN. The role of saltbushes (Atriplex spp.) in arid land rehabilitation in the Mediterranean Basin: a review. Agrofor Syst. 1992;18(2):107-148.) divided this species into two subspecies: halimus (var. typica Aellen, var. genuina Maire et Weill.) and schweinfurthii (Boiss.) Le Houérou (var. glaucoidea L. Chevall, var. ramosissima L. Chevall, var. argutidens Bornm). The subspecies halimus is lower, with more upright habitus and shorter fruiting branches, while the upper branches are slightly twisted. The subspecies schweinfurthii has leafless fruiting branches of a reddish hue. The leaves have different sizes, shapes and colors ranging from greenish to grayish. The leaves of the subspecies halimus are more or less lanceolate. The young are greenish, while the older ones are silver-gray (Walker et al., 2014Walker DJ, Lutts S, Sánchez-García M, Correal E. Atriplex halimus L.: Its biology and uses. J Arid Environ . 2014;100:111-121.). It grows in arid or semi-arid areas, with the subspecies schweinfurthii occurring mainly in arid and/or salt areas, and the subspecies halimus in semi-arid areas, without the presence of salt in the substrate (western Mediterranean basin and Macaronesia). It can grow at altitudes up to 1200 m, although it has a moderate tolerance to cold. It occurs in open, sunny places, as well as on neutral or alkaline soils. It thrives better on loam than on sandy or clay soils (Le Houérou, 1992Le Houérou HN. The role of saltbushes (Atriplex spp.) in arid land rehabilitation in the Mediterranean Basin: a review. Agrofor Syst. 1992;18(2):107-148.). It mainly forms part of halophilic communities on saline soils.

It is spread throughout Macaronesia, then the Mediterranean basin, all the way to western Asia. Its range includes southern Portugal, France, southern and eastern Spain, Italy, Greece, Malta, Turkey, Cyprus, Israel, Syria, Lebanon, Jordan, Tunisia, Morocco, Algeria, Libya, Egypt and Saudi Arabia (Gu et al., 2011Gu W, Müller G, Schlein Y, Novak RJ, Beier JC. Natural plant sugar sources of Anopheles mosquitoes strongly impact malaria transmission potential. PloS one. 2011;6(1):e15996.).

A. halimus has a high biomass with a relatively low metal translocation to the upper surface of the soil. It has manifested the efficiency to adopt metals. Due to its high biomass production and relatively high root metal content, this plant can be successfully used in phytoremediation, and especially in phytostabilization (Amer et al., 2013Amer N, Al Chami Z, Al Bitar L, Mondelli D, Dumontet S. Evaluation of Atriplex halimus, Medicago lupulina and Portulaca oleracea for phytoremediation of Ni, Pb, and Zn. Int J Phytorem. 2013;15(5):498-512.).

In addition to alkaloid compounds, fatty acids, sterols and amino acids, some flavonols, flavanones, flavones and isoflavone glycosides have also been identified. All of these compounds have medical and physiological activity (Emam, 2011Emam SS. Bioactive constituents of Atriplex halimus plant. J Nat Prod. 2011;4:25-41.).

An aqueous leaf extract of this species has a beneficial impact on reducing elevated blood glucose levels and hepatitis levels in diabetic rats (Chikhi et al., 2014Chikhi I, Allali H, El Amine M, Medjdoub H, Tabti B. Antidiabetic activity of aqueous leaf extract of Atriplex halimus L. (Chenopodiaceae) in streptozotocin-induced diabetic rats. Asian Pac J Trop Med. 2014;4(3):181-184.). By analyzing the antioxidant properties of the main secondary metabolites (Table I) of leaves and stems, it was concluded that methanolic extracts of leaves have a content of total phenolic compounds higher than methanolic extracts of stems. Flavonoids from the leaves have a higher ability to donate hydrogen for iron chelation and higher antioxidant activity (Benhammou, Bekkara, Panovska, 2009Benhammou N, Bekkara FA, Panovska TK. Antioxidant activity of methanolic extracts and some bioactive compounds of Atriplex halimus. C R Chim. 2009;12(12):1259-1266.).

A. halimus has a deep root system that in dry zones plays a role in soil stabilization and reduces erosion. The shoot is rich in protein, and therefore represents an important fodder species, especially for goats and sheep (Walker et al., 2014Walker DJ, Lutts S, Sánchez-García M, Correal E. Atriplex halimus L.: Its biology and uses. J Arid Environ . 2014;100:111-121.).

Genus Bassia

Bassia sedoides Pall. is an annual upright xerohalophytic species (Voznesenskaya et al., 2013Voznesenskaya EV, Koteyeva NK, Akhani H, Roalson EH, Edwards GE. Structural and physiological analyses in Salsoleae (Chenopodiaceae) indicate multiple transitions among C3, intermediate, and C4 photosynthesis. J Exp Bot. 2013;64(12):3583-3604.). It has a succulent leaf structure that is typical for halophytes growing in Europe (Grigore, Ivanescu, Toma, 2014Grigore MN, Ivanescu L, Toma C. Halophytes: an integrative anatomical study. Springer. Cham. Switzerland; 2014.). The leaves are simple, alternate and have very thick and long hairs on the surface (Safiallah et al., 2017Safiallah S, Hamdi SMM, Grigore MN, Jalili S. Micromorphology and leaf ecological anatomy of Bassia halophyte species (Amaranthaceae) from Iran. Acta Biol Szeged. 2017;61(1):85-93.). The roots and the stem are succulent (Hasanuzzaman, Shabala, Fujita, 2019Hasanuzzaman M, Shabala S, Fujita M. (Eds.). Halophytes and climate change: adaptive mechanisms and potential uses. 2019; CABI.). It has small flowers with a prickly perianth gathered in spikes. The embryo is five-pointed (5 anthers) and curved. The seeds are oval (Safiallah et al., 2017Safiallah S, Hamdi SMM, Grigore MN, Jalili S. Micromorphology and leaf ecological anatomy of Bassia halophyte species (Amaranthaceae) from Iran. Acta Biol Szeged. 2017;61(1):85-93.). This is a euchalophyte that inhabits dry salt marshes on a highly saline light base. It is widespread in Dobrogea, Crimea, the Caucasus, in Central Asia and in the east to western Mongolia and China (Stevanović, 1999Stevanović V. Crvena knjiga Flore Srbije. Beograd, Ministarstvo za životnu sredinu Republike Srbije, I tom; 1999.).

In B. sedoides, the amount of Na+ and K+ ions in the root is independent of the amount of salt in the soil. Flavonoids and K+ ions were also recorded in large amounts indicating high productivity and adaptation to saline soil (Rakhmankulova, Shuyskaya, Shcherbakov, 2015Rakhmankulova ZF, Shuyskaya EV, Shcherbakov AV. Content of proline and flavonoids in the shoots of halophytes inhabiting the South Urals; Russ J Plant Physiol . 2015;62(1):71-79.).

Bassia scoparia (L.) A.J.Scott (syn. Kochia scoparia (L) Schrad.) is an annual plant with a shrubby life form. It reaches a height of 1 to 2 m. The branches are straight, green or reddish, hairy or smooth. The flowers are small, up to 3 mm in diameter, and the seeds are oval and have a length of 1.5-2 mm. The seeds are brown with yellow spots or dark red to brown (Friesen et al., 2009Friesen LF, Beckie HJ, Warwick SI, Van Acker RC. The biology of Canadian weeds. 138. Kochia scoparia (L.) Schrad. Can J Plant Sci. 2009;89(1):141-167.). B. scoparia is a weed that grows along canal banks, roadsides, field edges, and salt marshes. It is a common weed in ruderal arid and semiarid areas, as well as in field production systems in North America. It is widely present in crop systems due to its abilities such as germination at low temperatures, drought tolerance, high temperature and salinity, and rapid growth. It is a native species in Europe and Asia, but it was introduced to the United States as an ornamental species in the early 20th century, being naturalized in the central and western parts (Welsh et al., 1978Welsh SL, Atwood ND, Goodrich S, Higgins LC. Utah flora: Fabaceae (Leguminosae). Great Basin Nat. 1978;9:1-894.; Friesen et al., 2009Friesen LF, Beckie HJ, Warwick SI, Van Acker RC. The biology of Canadian weeds. 138. Kochia scoparia (L.) Schrad. Can J Plant Sci. 2009;89(1):141-167.).

Studies have confirmed that B. scoparia has an allelopathic effect on some species. It was determined that in laboratory conditions it negatively affected the growth and development of soybean, sorghum, cotton, sugar beet and sunflower (Nair et al., 2021Nair J, Lima PMT, Abdalla AL, Molnar LJ, Wang Y, McAllister TA, et al. Kochia (Bassia scoparia) harvest date impacts nutrient composition, in vitro degradability, and feed value more than pre-harvest herbicide treatment or herbicide resistance traits. Anim Feed Sci Technol. 2021;115079.). An aqueous extracts inhibited the growth of seedlings of Bouteloua gracilis (Friesen et al., 2009Friesen LF, Beckie HJ, Warwick SI, Van Acker RC. The biology of Canadian weeds. 138. Kochia scoparia (L.) Schrad. Can J Plant Sci. 2009;89(1):141-167.) and had a negative effect on germination and growth of seedlings of Linum usitatissimum (Zhao et al., 2010Zhao L, Niu J, Li C, Ma P, Dang Z. Allelopathy of aqueous extracts of Kochia scoparia on flaxseed. Acta Prataculturae Sin. 2010;19(2):190-195.). It also negatively affected maize germination (Nawaz et al., 2013Nawaz H, Hussain N, Yasmeen A, Alam S, Nasrullah HM. Screening Faisalabad flora for allelopathic potential. J Sci Res. 2013;25(1):01-23.).

An exudate of B. scoparia seeds extracted in water inhibited fungus Colletotrichum graminicola. After exposure to exudate, hyphae formation was inhibited indicating that this species with persistent seeds may be useful in controlling the plant pathogen (Houlihan, Conlin, Chee-Sanford, 2019Houlihan AJ, Conlin P, Chee-Sanford JC. Water-soluble exudates from seeds of Kochia scoparia exhibit antifungal activity against Colletotrichum graminicola. PLoS One . 2019;14(6):e0218104.). The n-hexane fraction had an antibacterial effect on methicillin-resistant Staphylocccus aureus (Joung et al., 2012Joung DK, Kim YH, Yang DW, So GW, Lee KH, Kwon DY, et al. Antibacterial and synergistic effects of Kochia scoparia extracts against methicillin-resistant Staphylococcus aureus. Afr J Microbiol Res. 2012;6(10);2455-2461.).

The leaves have insecticidal properties and have an acaricidal effect on three types of mites (Tetranychus sp., Acari, Tetranychidae) (Shi et al., 2006Shi GL, Zhao LL, Liu SQ, Cao H, Clarke SR, Sun JH. Acaricidal activities of extracts of Kochia scoparia against Tetranychus urticae, Tetranychus cinnabarinus, and Tetranychus viennensis (Acari: Tetranychidae). J Econ Entomol. 2006;99:858-863.). Chloroform extract from seeds showed strong activity on the nutrition of the larva Plutella xylostella. It was found to be able to have both selective and complete impact (Zhao et al., 2008Zhao L, Du J, Liu SQ, Cao H. Antifeeding effects of Plutella xylostella L. by extracts of the seed of Kochia Scoparia (L.) Schrad.[J]. J Shanxi Agr Sci. 2008; 10.).

The whole plant and seeds have been found to contain phytoecdysteroids which have potential medical significance. The main phytoecdysteroids in the seed are 20-hydroxyecdysone and polypodine B (5β,20-dihydroxyecdysone), but significant amounts of unidentified others were also detected. A similar mixture of phytoecdysteroids was observed in all plant extracts including a large amount of apolar conjugate ecdysone not identified in the seed (Dinan, 1994Dinan L. Phytoecdysteroids in Kochia scoparia (burning bush). J Chromatogr A. 1994;658(1):69-76.).

Flavonoids extracted from B. scoparia exhibited antioxidant activity and had the power to remove free radicals (Hao et al., 2012Hao Z, Hua Y, Xin Z, Honghai S, Fei Z, Weihong Li. Antioxidant activities of flavonoids extraction from Kochia scoparia. Chem Ind Times. 2012;26(7):30-32.). It is known that this species have cardiotonic, tonic, hypotensive and stimulating properties (Akopian et al., 2020Akopian JA, Ghukasyan AG, Shomurodov HF, Adilov BA. On some medicinal plants of Chenopodiaceae family in the floras of Armenia and Uzbekistan. Electron J Nat Sci. 2020;34(1):12-17.). It can be used in bioremediation of soils containing cesium and hydrocarbons (Friesen et al., 2009Friesen LF, Beckie HJ, Warwick SI, Van Acker RC. The biology of Canadian weeds. 138. Kochia scoparia (L.) Schrad. Can J Plant Sci. 2009;89(1):141-167.).

A study in Thailand showed that this plant caused allergic reactions to pollen in humans, where 14% out of 100 patients reported to have allergic rhinitis in response to it (Pumhirum, Towiwat, Mahakit, 1997Pumhirum P, Towiwat P, Mahakit P. Aeroallergen sensitivity of Thai patients with allergic rhinitis. Asian Pac J Allergy Immunol. 1997;15:183-185.).

B. scoparia is used as animal feed because it has a similar nutritional value as alfalfa (Medicago sativa), but it can be poisonous to livestock if ingested in large quantities. The death of sheep, cows and horses has been reported. Toxic substances are saponins and alkaloids, oxalates and nitrates (Friesen et al., 2009Friesen LF, Beckie HJ, Warwick SI, Van Acker RC. The biology of Canadian weeds. 138. Kochia scoparia (L.) Schrad. Can J Plant Sci. 2009;89(1):141-167.).

Bassia prostrata (L.) Beck - (syn. Kochia prostrata (L.) Schrad.) is a perennial, semi-shrubby plant with a cylindrical root. It has many above-ground shoots up to 60 cm, which are hairy or later more or less smooth. The stem is woody and bears thick and thin branches from the base. The leaves are alternate or in vertebrae, up to 1 mm wide. They are conical, pointed or narrowly linear. The inflorescence is composed of apical and lateral, loose or compact spikes. The glomeruli are composed of 3 to 5 flowers. The seeds are up to 2 mm long and dark gray. It grows on alkaline soil, on steppes. It is resistant to wind and drought. It is widespread in the Southern Europe, Asia and North Africa (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

In addition to the alkaloids harmen and harmin, B. prostrata contains organic acids, flavonoids, and saponins (Akopian et al., 2020Akopian JA, Ghukasyan AG, Shomurodov HF, Adilov BA. On some medicinal plants of Chenopodiaceae family in the floras of Armenia and Uzbekistan. Electron J Nat Sci. 2020;34(1):12-17.). The content of proline and flavonoids, which have a protective role and participate in adaptation to habitat conditions, was determined in the shoots of this plant. Since a high content of proline and flavonoids, especially naringin and rutin, was identified, this species was concluded to be well adapted to salinity conditions (Rakhmankulova, Shuyskaya, Shcherbakov, 2015Rakhmankulova ZF, Shuyskaya EV, Shcherbakov AV. Content of proline and flavonoids in the shoots of halophytes inhabiting the South Urals; Russ J Plant Physiol . 2015;62(1):71-79.).

This plant is considered to be good for grazing and is used on the Asian continent to feed sheep, goats, camels and horses. It is a good source of protein and carotene, without the risk of poisoning caused by tannins or oxalates, as in B. scoparia (Davis, 1979Davis AM. Forage quality of Kochia prostrata compared with three browse species. Agron J. 1979;71:822-824.).

B. prostrata had a crude protein content that was higher than the minimum content required to maintain the activity of microorganisms in ruminant rumen. These results suggest that this species can be a significant source of feed, especially in critical dry periods of certain areas (Ramazan et al., 2021Ramazan ACAR, Fatma İNAL, Koyun NK, Kahraman O, Özbilgin A. The feed values of three forage Kochia phenotypes at different growth periods. Bahri Dağdaş Bitk Araşt Derg. 2021;10(1):57-63.). It is known to be used as an anthelmintic (Akopian et al., 2020Akopian JA, Ghukasyan AG, Shomurodov HF, Adilov BA. On some medicinal plants of Chenopodiaceae family in the floras of Armenia and Uzbekistan. Electron J Nat Sci. 2020;34(1):12-17.).

Genus Beta

Beta trigyna W. et K. is the perennial plant growing from 50 to 90 cm in height. The lower leaves are broad and ovate, narrowed into a petiole. The leaves of the perigon are hairy, yellow-white, 5-7 mm long, thickened and initially shrunken (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.). The flower has an outer spiral containing five perigons, a spiral having five anthers connected in a ring, and a pistil with three carpels. The perigon resembles a corolla and can be whitish, yellowish or reddish (Kadereit, Hohmann, Kadereit, 2006Kadereit G, Hohmann S, Kadereit JW. A synopsis of Chenopodiaceae subfam. Betoideae and notes on the taxonomy of Beta. Willdenowia. 2006;9-19.). It is present on steppes, sea shores, arable land and can be found along roads. It grows on acidic, neutral and basic soils, but also on saline, moist soils. This is a weed, less often a ruderal plant. It is widespread in Southeast Europe and Asia Minor (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.). The center of distribution of this species is in Turkey, Russia, Georgia and Armenia. It occurs around the Black Sea and the Caspian Sea, as well as in Persia, Crimea and Southern Ukraine. It spreads to the east in Hungary, Romania, Slavonia and some parts of the Balkans, as well as in Macedonia. It has been found to occur naturally in Iran, while no specimens have been recorded in Japan (Srivastava et al., 1991Srivastava HM, Yi-Chu Sun, Nasser Arjmand M, Masutani T. Beta genetic resources activity in Asia; International Beta genetic network; 1991.).

B. trigyna is used in traditional medicine for asthma and bronchitis, and its use in the nutrition was previously noted (Ezer, Arisan, 2006Ezer N, Arisan ÖM. Folk medicines in Merzifon (Amasya, Turkey). Turk J Bot. 2006;30(3):223-230.). It is also used in Turkey in the diet of the local population, especially in the area of Agri. It has a good CI (The Cultural Importance index) value and is considered as nutritionally and economically important species. Only shoots and leaves whose preparation requires cooking are consumed (Kadioglu et al., 2020Kadioglu Z, Cukadar K, Kalkan NN, Vurgun H, Kaya O. Wild edible plant species used in the Ağrı province, eastern Turkey. An Jard Bot Madr. 2020;77(2):e098.).

Genus Camphorosma

Camphorosma annua Pall. is a therophyte with the ground habitus. Flower branches can be 5 to 40 cm long. The leaves are succulent, hairy and with a thick cuticle. It germinates in the period from the end of February or the beginning of March and flowers in June (Murakeözy et al., 1999Murakeözy ÉP, Nagy Z, Tuba Z. Proline accumulation pattern in species of an inland salme habitat. Z Naturforsch C. 1999;54(9-10):718-722.; Murakeözy, Nagy, Tuba, 2003Murakeözy ÉP, Nagy Z, Duhazé C, Bouchereau A, Tuba Z. Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J Plant Physiol. 2003;160(4):395-401.). This species is present in the Pontopannonian floristic area and mainly in Southeast Europe. It grows on continental saline places that are thermophilic and sunny. The presence of C. annua is an indicator of dry and saline habitats with a hard mechanical composition (Janjatović et al., 1992Janjatović V, Knezevic A, Andjelic M, Merkulov L. Eco- morphological characteristics of Camphorosma annua Pall. (Chenopodiaceae). Biology series; 1992.). This plant is characteristic for the sodicidal type of solonchaks with the highest salt content (Murakeözy et al., 1999Murakeözy ÉP, Nagy Z, Tuba Z. Proline accumulation pattern in species of an inland salme habitat. Z Naturforsch C. 1999;54(9-10):718-722.). It is suited to a highly alkaline substrate dominated by chloride (Janjatović et al., 1992Janjatović V, Knezevic A, Andjelic M, Merkulov L. Eco- morphological characteristics of Camphorosma annua Pall. (Chenopodiaceae). Biology series; 1992.). It has been found in alkaline habitats such as alkaline steppe, open alkaline grassland and alkaline meadow (Riba et al., 2020Riba M, Kiss-Szikszai A, Gonda S, Parizsa P, Deák B, Török P, et al. Chemotyping of terrestrial Nostoc-like isolates from alkali grassland areas by non-targeted peptide analysis. Algal Res. 2020;46:101798.). C. annua is bound to saline soil and it is not able to germinate below a certain level of salinity. Due to this fact it is classified as an obligate halophyte suffering even periodic flooding with salt water that would destroy most other plants (Josifović, 1980Josifović, M. Flora of SR Serbia III, Belgrade: SANU, 1980. (in Serbian)). C. annua is a plant with a large ecological spectrum so it can grow in other saline habitats (salty sand or populated areas), as well as in less saline areas. This is the reason why Grigore and Toma (2010Grigore MN, Toma C. A proposal for a new halophytes classification, based on integrative anatomy observations. Oltenia Stud Comun Ştiinţele Nat. (Oltenia J Stud Nat Sci). 2010;26:45-50.) called this species “a reversible” halophyte. C. annua is a pioneer species in the succession of steppe habitats. It successfully resists high salt concentrations forming almost monotypic vegetation (Josifović, 1980Josifović, M. Flora of SR Serbia III, Belgrade: SANU, 1980. (in Serbian)). It is the dominant species in Camphorosmetum annuae community being especially widespread on solonetzes. This community occurs on bare depressions with the highest salinity and such areas can be considered the most extreme for vegetation in lowland conditions. These are mainly areas with scarce vegetation cover that make up a small number of species (Levente, Codrin, 2014Levente CR, Codrin G. Aspect regarding the halophilous vegetation from the Ierului Plain. Analele Universității din Oradea, Fascicula: Ecotoxicologie, Zootehnie și Tehnologii de Industrie Alimentară. 2014;13(B):283-288.).

The specific habitat conditions of this species growth have influenced the creation of a large number of anatomical adaptations such as succulent leaves, thick cuticles, concave stoma, developed palisade and tissue for water storage (Janjatović et al., 1992Janjatović V, Knezevic A, Andjelic M, Merkulov L. Eco- morphological characteristics of Camphorosma annua Pall. (Chenopodiaceae). Biology series; 1992.). Also, some other specific anatomical features may appear, such as successive cambium, Kranz anatomy, and hair follicles (Grigore, Toma, 2010Grigore MN, Toma C. A proposal for a new halophytes classification, based on integrative anatomy observations. Oltenia Stud Comun Ştiinţele Nat. (Oltenia J Stud Nat Sci). 2010;26:45-50.).

The osmolites have a role in maintaining the vital osmotic concentration in halophytes. When plants are exposed to a higher concentration of salt, the level of osmolyte is subjected to change. Seasonal changes in osmolytes of halophytic plant leaves were also investigated in C. annua. It was determined that this species accumulates glycine, betaine and pinitol in leaves, mostly during the spring months. The concentration of these osmolytes is lower in the summer months. An increased production of pinitol was found in the species Limonium gmelini during the summer months, but not in C. annua, and this finding can be attributed to a larger vacuolar space (Murakeözy, Nagy, Tuba, 2003Murakeözy ÉP, Nagy Z, Duhazé C, Bouchereau A, Tuba Z. Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J Plant Physiol. 2003;160(4):395-401.).

Osmolites betaine and pinitol were found by examining seasonal changes in the concentration of osmolytes in C. annua leaf tissues (Murakeözy, Nagy, Tuba, 2003Murakeözy ÉP, Nagy Z, Duhazé C, Bouchereau A, Tuba Z. Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J Plant Physiol. 2003;160(4):395-401.). This species usually accumulates small amounts of proline, but a relatively large amount of this amino acid was found in this species in March (Murakeözy et al., 1999Murakeözy ÉP, Nagy Z, Tuba Z. Proline accumulation pattern in species of an inland salme habitat. Z Naturforsch C. 1999;54(9-10):718-722.), when the main constraints on plant development were low temperatures, hypoxic conditions, and high salt concentrations (Murakeözy, Nagy, Tuba 2003Murakeözy ÉP, Nagy Z, Duhazé C, Bouchereau A, Tuba Z. Seasonal changes in the levels of compatible osmolytes in three halophytic species of inland saline vegetation in Hungary. J Plant Physiol. 2003;160(4):395-401.).

Among the organic anions present in C. annua, malate, citrate, and oxalate were observed to bear quantitative significance (Albert, Popp, 1977Albert R, Popp M. Chemical composition of halophytes from the Neusiedler Lake region in Austria. Oecologia. 1977;27(2):157-170.).

Camphorosma monspeliaca L. (Figure 1) is a perennial shrub that can reach a height up to 60 cm (Moghimi, 2006Moghimi J. Introducing the important range species for range management. Arvan Publishing. New York. 2006; 669.). The leaves have hairs on the surface. The lower ones are linear, and the upper ones are shorter and triangular (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.). The stem and leaves have an intense camphor-like odor. The flowers are hermaphroditic and pollinated by insects (Thomas, 1992Thomas GS. Ornamental shrubs, climbers and bamboos. France Lincoln. 1992; pp 592.). This is a plant characteristic of steppe zones and solonetz-type soil (Goryaev, Korablev, 2020Goryaev IA, Korablev AP. Halophytic vegetation in the west caspian lowland. Contemp Probl Ecol. 2020;13(5):514-521.). It prefers well-drained soil and is suitable for light sandy and medium loamy soils. It can tolerate drought and grow on highly alkaline saline soils (Genders, 2001Genders R. Scented Flora of the World. Robert Hale Ltd. 2001; pp: 560.; Moghimi, 2006Moghimi J. Introducing the important range species for range management. Arvan Publishing. New York. 2006; 669.). In addition to saline habitats, C. monspeliaca can be detected on unsalted and alkaline soils with low content of organic matter and gypsum. The texture of these soils may consist of clay, loamy and calcareous soils (Gharibvand et al., 2011Gharibvand HAK, Tilaki GAD, Mesdaghi M, Sardari M. Ecological characteristics of Camphorosma monspeliaca in Doto-Tangsayad habitat, Chaharmahal va Bakhtiari Province (Iran). Iran J Range Desert Res. 2011;17(4):632-645.). This species is present in the Mediterranean area (Hasanuzzaman, Shabala, Fujita, 2019Hasanuzzaman M, Shabala S, Fujita M. (Eds.). Halophytes and climate change: adaptive mechanisms and potential uses. 2019; CABI.). It occurs as a dominant species in the community of Camphorosmetum monspeliaceae (Goryaev, Korablev, 2020Goryaev IA, Korablev AP. Halophytic vegetation in the west caspian lowland. Contemp Probl Ecol. 2020;13(5):514-521.), but also as a part of the Puccinellion convolutae in the southern Balkans (southern Serbia, the Republic of Northern Macedonia and Bulgaria) (Eliáš et al., 2013Eliáš JrP, Sopotlieva D, Dítě D, Hájková P, Apostolova I, Senko D, et al. Vegetation diversity of salt-rich grasslands in Southeast Europe. Appl Veg Sci. 2013;16(3):521-537.; Stevanović et al., 2016Stevanović ZD, Aćić S, Luković M, Zlatković I, Vasin J, Topisirović G, et al. Classification of continental halophytic grassland vegetation of southeastern Europe. Phytocoenologia. 2016;46(3):317-331.).

FIGURE 1
Camphorosma monspeliaca L.

C. monspeliaca contains alkaloids, organic acids, saponins, flavonoids, coumarins, betaine, steroids, oils, vitamins B1, B2, C1, E, carotene and others. It is used in folk medicine to treat various diseases. It is known to be used as a diaphoretic and diuretic (Akopian et al., 2020Akopian JA, Ghukasyan AG, Shomurodov HF, Adilov BA. On some medicinal plants of Chenopodiaceae family in the floras of Armenia and Uzbekistan. Electron J Nat Sci. 2020;34(1):12-17.).

This plant is important as a food source for camels, sheep and goats. It contains essential oils with camphor giving it a strong scent. It is used in folk medicine due to its antiasthmatic and diuretic properties (Tajali et al., 2007Tajali AA, Amin G, Chaichi MR, Zahedi G. Habitat influence on essential oil of Camphorosma monspeliaca L. in Iran. Asian J Plant Sci. ISO 690; 2007.), but also as a diaphoretic, expectorant and stimulant (Usher, 1974Usher G. A dictionary of plants used by man. Constable. 1974; 619.). Significant phenol content was confirmed (Table I), as well as an antioxidant activity of this species (Stanković et al., 2015Stanković MS, Petrović M, Gođevac D, Stevanović ZD. Screening inland halophytes from the central Balkan for their antioxidant activity in relation to total phenolic compounds and flavonoids: Are there any prospective medicinal plants?. J Arid Environ. 2015;120:26-32.).

Under stressful conditions, this species accumulates the amino acid proline, the concentration of which depends on the intensity of stress (Öncel, 1988Öncel I. The proline accumulation of some halophytes in the vicinites of the salt lake. Commun Fac Sci Univ Ank Serie C. 1988;6:219-225.).

Genus Chenopodium

Chenopodium ambrosioides L. is an annual or perennial plant that can reach a height up to 1 m (López de Guimaraes, Neyra Llanos, Romero Acevedo, 2001López De Guimaraes D, Neyra Llanos RS, Romero Acevedo JH. Ascariasis: comparison of the therapeutic efficacy between paico and albendazole in children from Huaraz. Revista de gastroenterologia del Peru: organo oficial de la Sociedad de Gastroenterologia del Peru. 2001;21(3):212-219.). It is aromatic and has a strong odor (Kumar et al., 2007Kumar R, Mishra AK, Dubey NK, Tripathi YB. Evaluation of Chenopodium ambrosioides oil as a potential source of antifungal, antiaflatoxigenic and antioxidant activity. Int J Food Microbiol. 2007;115(2):159-164.). The stem is bent, with leaves having a length of 4 cm and a width of 1 cm (Gadano et al., 2006Gadano AB, Gurni AA, Carballo MA. Argentine folk medicine: genotoxic effects of Chenopodiaceae family. J Ethnopharmacol. 2006;103(2):246-251.; Jamali et al., 2006Jamali A, Kouhila M, Mohamed LA, Jaouhari JT, Idlimam A, Abdenouri N. Sorption isotherms of Chenopodium ambrosioides leaves at three temperatures. J Food Eng. 2006;72(1):77-84.). The leaves are serrated and lanceolate. The flowers are greenish or purple (Mishra, et al., 2002Mishra A, Dubey NK, Singh S, Chaturvedi CM. Biological activities of essential oil of Chenopodium ambrosioides against storage pests and its effect on puberty attainment in Japanese quail. Natl Acad Sci Lett. 2002;25(5-6):174-177.; Lans et al., 2006Lans C, Turner N, Brauer G, Lourenco G, Georges K. Ethnoveterinary medicines used for horses in Trinidad and in British Columbia, Canada. J Ethnobiol Ethnomed. 2006;2(1):1-20.). They are collected in thick brooms and each has 5 calyx leaves. The seed is up to 0.8 mm long and black (Gadano et al., 2006Gadano AB, Gurni AA, Carballo MA. Argentine folk medicine: genotoxic effects of Chenopodiaceae family. J Ethnopharmacol. 2006;103(2):246-251.; Jamali et al., 2006Jamali A, Kouhila M, Mohamed LA, Jaouhari JT, Idlimam A, Abdenouri N. Sorption isotherms of Chenopodium ambrosioides leaves at three temperatures. J Food Eng. 2006;72(1):77-84.). It is native in Central and South America and considered as invasive due to its ability to adapt to different conditions. It has successfully spread to other continents hence being a cosmopolitan species (Lorenzi, Matos, 2002Lorenzi HE, Matos FJ. Plantas medicinais no Brasil: Nativas e exóticas. Nova Odessa: Instituto Plantarum. 2002; 512 p.).

Some previous studies indicate that this species affects the growth of some plants, ie. it has an allelopathic effect. Extracts of Ch. ambrosioides were tested for germination and hormone growth inhibition on Amaranthus hypochondriacus and it was concluded that the essential oil of Ch. ambrosioides inhibited the germination of A. hypochondriacus. Based on this deduction, the usage of Ch. ambrosioides as an allelopathic agent for pest control in agroecosystems could be considered (Jimenez-Osornio, Kumamoto, Wasser, 1996Jimenez-Osornio J, Kumamoto J, Wasser C. Allelopathic activity of Chenopodium ambrosioides L. Biochem Syst Ecol. 1996;24(3):195-205.).

Infusion showed higher antioxidant activity, while methanol extract was the only one to exhibit antitumor effects. Toxicity in tumor cells was not observed for either infusion or extract. Ch. ambrosioides was confirmed to be a good source of natural antioxidants (Table I) with potential application in industry (Barros et al., 2013Barros L, Pereiraa E, Calhelhaab RC, Dueñasc M, Carvalhoa A, Santos-Buelgac C, et al. Bioactivity and chemical characterization in hydrophilic and lipophilic compounds of Chenopodium ambrosioides L. J Funct Foods. 2013;5(3):1732-1740.). It was found that extracts of this species showed strong fumigant activity on the corn borer Sitophilus zeamais. The essential oil of this species and its main active component, ascaridol, could be investigated as a fumigant with natural potential (Chu, Hu, Long Liu, 2011Chu S, Hu JF, Long Liu Z. Composition of essential oil of Chinese Chenopodium ambrosioides and insecticidal activity against maize weevil, Sitophilus zeamais. Pest Manag Sci. 2011;67(6):714-718.). Essential oil and its main components (ascaridol, carvacrol and caryophyllene oxide) exhibited a leishmanicidal effect on the parasite Leishmania amazonensis. All tested substances had strong inhibitory activities on promastigote and amastigote forms, and ascaridol exhibited the best activity (Monzote et al., 2014Monzote L, García M, Pastor J, Gil L, Scull R, Maes L, et al. Essential oil from Chenopodium ambrosioides and main components: activity against Leishmania, their mitochondria and other microorganisms. Exp Parasitol. 2014;136:20-26.).

According to the WHO, this plant is considered as one of the most commonly used medicinal plants in the world (Lorenzi, Matos, 2002Lorenzi HE, Matos FJ. Plantas medicinais no Brasil: Nativas e exóticas. Nova Odessa: Instituto Plantarum. 2002; 512 p.). It is used in folk medicine in the form of teas and infusions for inflammatory problems, contusions and lung infections, as well as an antifungal agent (Trivellato Grassi et al., 2013Trivellato Grassi L, Malheirosa A, Meyre-Silvaa C, Silva ZB. From popular use to pharmacological validation: A study of the anti-inflammatory, anti-nociceptive and healing effects of Chenopodium ambrosioides extract. J Ethnopharmacol . 2013;145(1):127-138.). Chekem et al. (2010Chekem MSG, Lunga PK, Tamokou JDD, Kuiate JR, Tane P, Vilarem G, et al. Antifungal properties of Chenopodium ambrosioides essential oil against candida species. Pharmaceuticals. 2010;3(9):2900-2909.) recorded the antifungal effect of Ch. ambrosioides essential oil. In vitro method showed that the activity was dependent on concentration, while in vitro method demonstrated that the antifungal activity was not dose dependent. All of the three tested doses had an effect after 12 days. The analysis of the bactericidal activity showed that Ch. ambrosioides had an active effect in vitro on Helicobacter pylori, an antibiotic- resistant bacterial species (Liu et al., 2012Liu W, Liu Y, Zhang XZ, Li N, Cheng H. In vitro bactericidal activity of Jinghua Weikang Capsule and its individual herb Chenopodium ambrosioides L. against antibiotic-resistant Helicobacter pylori. Chin J Integr Med. 2012;19(1):54-57.).

Powders and essential oil obtained from the dried leaves of this plant were tested in laboratory conditions and they were established to have the ability to protect grains from damage done by six insect pests: Callosobruchus chinensis, C. maculatus, Acanthoscelides obtectus, Sitophilus granarius, S. zeamais and Prostephanus truncatus (Tapondjou et al., 2002Tapondjou LA, Adlerb C, Boudaa H, Fontemc DA. Efficacy of powder and essential oil from Chenopodium ambrosioides leaves as post-harvest grain protectants against six-stored product beetles. J. Stored Prod Res. 2002;38(4):395-402.). The essential oil of the leaves of Ch. ambrosioides was tested against the aflatoxigenic strain of the fungus Aspergillus flavus. The oil inhibited mycelial growth to 100 μg/mL. It also showed a broad fungitoxic spectrum against Aspergillus niger, A. fumigatus, Botryodiplodia theobromae, Fusarium oxysporum, Sclerotium rolfsii, Macrophomina phaseolina, Cladosporium cladosporioides, Helminthosporium oryzae and Pythium debaryanum. During in vivo research, the essential oil protected wheat from various storage fungi for one year time frame. It also exhibited strong antioxidant activity. All these observations indicate the possible exploitation of the oil of this plant as a potential botanical fungitoxicant (Kumar et al., 2007Kumar R, Mishra AK, Dubey NK, Tripathi YB. Evaluation of Chenopodium ambrosioides oil as a potential source of antifungal, antiaflatoxigenic and antioxidant activity. Int J Food Microbiol. 2007;115(2):159-164.).

Chenopodium polyspermum L. is an annual plant reaching the height from 20 to 80 cm. The shoots are smooth and branched. At the beginning of the growth, it is close to the ground, and later it is upright. The older plant eventually becomes reddish by the time. The leaves are also smooth, ovate and not serrated. It has inflorescences in the axils of the leaves and at the top of the branches. They have the shape of oblong clusters. It blooms in summer (Fuentes-Bazan, Pertti, Thomas, 2012Fuentes-Bazan S, Uotila P, Borsch T. A novel phylogeny- based generic classification for Chenopodium sensu lato, and a tribal rearrangement of Chenopodioideae (Chenopodiaceae). Willdenowia - Annals of the Botanic Garden and Botanical Museum Berlin-Dahlem. 2012;42(1):5-24. DOI: 10.3372/wi.42.42101
https://doi.org/10.3372/wi.42.42101...
). Ch. polyspermum is a weed species present from the lowlands to mountainous areas and grows in wet cultivated or uncultivated areas (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.). It is common in coastal places (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.). It also occurs in ruderal habitats, fields and gardens where sandy soil is present (Pokorná et al., 2018Pokorná A, Kočár P, Novak J, Šálková T, Žáčková P, Komarkova V, et al. Ancient and early medieval man- made habitats in Czech Republic: colonization history and vegetation changes. Preslia. 2018;90(3):171-193.). Soils with a high content of nitrates, nitrogen and phosphorus are suitable for this plant (Woźnica et al., 2016Woźnica P, Urbisz A, Urbisz A, Franiel I. Tram tracks as specific anthropogenic habitats for the growth of plants. PeerJ Preprints. 2016;4:e2606v1.). It is widespread in Europe and Asia (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

Ch. polyspermum has a rich content of flavonoids (Table I) (Vysochina, 2010Vysochina GI. Flavonoids of the Chenopodium L. genus of world flora. Russ. J Bioorganic Chem. 2010;36(7):787-792.) and it is characterized by the presence of the flavonoid rutin (Uslu et al., 2020Uslu N, Acar R, Seymen M, Dursun N, Türkmen Ö, Özcan MM. The effect of sowing dates on total phenol, antioxidant activity and phenolic compounds of orache garden leaves harvested from plants growing garden house and field conditions. J Agroaliment Processes Technol. 2020;26(4):347-352.). Quercetin and rutin were identified in leaves and flowers, while procyanidin and epicatechin were identified only in flowers (Dadáková et al., 2013Dadáková E, Vrchotová N, Tříska J, Děkanová Z. Content of phenolic substances in the selected species of the Chenopodiaceae family. J Agrobiol. 2013;30(2):127-135.).

Limonene and ascaridol were found to be the two most abundant compounds of leaf essential oil. Safrole, saponin, ascaridol, camphor, histamine, cinnamon, methyl salicylate and trimethylamine were also identified (Dembitsky, Shkrob, Hanus, 2008Dembitsky V, Shkrob I, Hanus LO. Ascaridole and related peroxides from the genus Chenopodium. Biomed Pap Med fac Univ Palacky Olomouc. 2008;152(2): 209-215.). The presence of oxalic acid and hydrocyanic acid was determined as well. Due to the presence of these compounds, Ch. polyspermum causes hemolytic and renal toxicity when consumed by human (Acık et al., 2012Acık DY, Yilmaz M, Sahin HH, Sayıner Z, Koruk I, Tiryaki O, et al. Management of Chenopodium polyspermum toxicity with plasma exchange and hemodialysis. J Clin Apher. 2012;27(5):278-281.).

Ch. polyspermum has antimicrobial, antiviral, antifungal, anthelmintic, and trypanocidal action; it possesses neoplastic and immunomodulatory properties and exhibits antioxidant activity. Due to these pharmacological properties, it has application in alternative medicine (Acık et al., 2012Acık DY, Yilmaz M, Sahin HH, Sayıner Z, Koruk I, Tiryaki O, et al. Management of Chenopodium polyspermum toxicity with plasma exchange and hemodialysis. J Clin Apher. 2012;27(5):278-281.).

Chenopodium vulvaria L. is an annual plant which can reach a height from 5 to 40 cm. It is sticky and gray- green (Medwecka et al., 2012). The lower branches are flat and often spread on the surface. The lower leaves are ovate or broadly rhombic. They are wedge-shaped at the base and may have a slight depression at the widest part. The flowers are small and inconspicuous. They are collected in false spikes or brooms. The fruit is a spherical or slightly flattened achenia. The seeds are black and kidney-shaped (Mochnacký, 2012Mochnacký S. Occurrence and distribution of Chenopodium vulvaria L. in Košice city, Slovakia. J Bot. 2012;22(2):191-195.). Ch. vulvaria is recognizable by its unpleasant odor similar to the smell of rotten fish. This plant mainly grows in places exposed to anthropogenic influence (Groom, 2015Groom QJ. Piecing together the biogeographic history of Chenopodium vulvaria L. using botanical literature and collections. Peer J. 2015;3:723.). It grows in ruderal environments, near city paths, buildings and walls. It is an integral part of the phytobiodiversity of urban ecosystems (Mochnacký, 2012Mochnacký S. Occurrence and distribution of Chenopodium vulvaria L. in Košice city, Slovakia. J Bot. 2012;22(2):191-195.). Ch. vulvaria is often found in eutrophic and coastal habitats and its number in such habitats is increasing in northern Europe (Van Landuyt et al., 2008Van Landuyt W, Vanhecke L, Hoste I, Hendrickx F, Bauwens D. Changes in the distribution area of vascular plants in Flanders (northern Belgium): eutrophication as a major driving force. Biodivers Conserv. 2008;17(12):3045-3060.; Groom, 2013Groom QJ. Some poleward movement of British native vascular plants is occurring, but the fingerprint of climate change is not evident. Peer J. 2013;1:e77.). This species grows naturally in Europe and Asia (Mochnacký, 2012Mochnacký S. Occurrence and distribution of Chenopodium vulvaria L. in Košice city, Slovakia. J Bot. 2012;22(2):191-195.). In the west, it is widespread in the countries bordering the Mediterranean, and in the east it is present as far as Afghanistan and Mongolia (Jalas, Suominen, 1988Jalas J, Suominen J. Atlas Florae Europaeae: Volume 1: Distribution of Vascular Plants in Europe (Vol. 1). Cambridge University Press. 1988.). It has been introduced to North America, Northern Patagonia, Chile, Australia, and New Zealand (Mochnacký, 2012Mochnacký S. Occurrence and distribution of Chenopodium vulvaria L. in Košice city, Slovakia. J Bot. 2012;22(2):191-195.).

It is known that the volatile oil of Ch. vulvaria can be used as a bacteriostatic, bactericidal and antioxidant product. It can be obtained by steam distillation or supercritical CO2 extraction. It has the effect of inhibiting bacteria such as Staphylococcus sp., Streptococcus sp., Enterobacter sp., Salmonella sp., Shigella sp., Pseudomonas sp., Bacillus sp., Escherichia sp., as well as fungi such as Candida sp., Cryptococcus sp., Aspergillus sp., Trichophyta epidermophyton sp., etc. Also, the diphenyl-picryl- phenylhydrazine (DPPH) method shows that the essential oil has a high antioxidant activity and can be widely used in the food, medicine, cosmetics and health care products industry. People with a tendency to rheumatism, arthritis and gout should be careful since the usage of this plant can worsen their condition (Chao et al., 2002Chao L, Ling V, Zhikin L, Mengia L, Zhukun M. Method for preparing Chenopodium vulvaria volatile oil and application of Ch. vulvaria volatile oil. 2002. https://patents.google.com/patent/CN102618386A/en
https://patents.google.com/patent/CN1026...
).

Chenopodium hybridum L. is an annual plant with an upright stem. It reaches a height of 1 m. At first, the stem is a little rough, and later completely smooth. All leaves are green, pointed at the top. The lower leaves are large, round at the base, and the upper ones are smaller. The flowers are light green, up to 2 mm long. There are 5 anthers, and the fruit is 1.5-2 mm wide and with sharp ends. The seeds are shiny and black. It is characteristic of arable land and avoids open, very sunny places. It is widespread in Eurasia and North America (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.). In vitro analysis of ethanolic extracts has shown that some species of the genus Chenopodium can suppress cancer cells. Unfortunately, these properties are often accompanied by high toxicity to skin fibroblasts. The extract of Ch. album caused inhibition of about 95% of accumulating ovarian and endometrial cancer cells. These data are similar to those obtained for Ch. hybridum. However, the toxicity of both of these extracts on skin fibroblasts was also high. Cell mortality after 72 h was 90%. Ch. hybridum exhibited cytotoxic activity against ovarian cancer cells (55%). Moreover, 30% activity of Ch. hybridum extracts on human lung cancer cells was also recorded with probable cytopathic effects on skin fibroblasts (Nowak et al., 2016Nowak R, Szewczyk K, Gawlik-Dziki U, Rzymowska J, Komsta L. Antioxidative and cytotoxic potential of some Chenopodium L. species growing in Poland. Saudi J Biol Sci. 2016;23(1):15-23.).

Extracts of this plant exhibited multidirectional biological activity, such as anticancer and antioxidant abilities, as a result of which this species can be used as an easily accessible source of natural antioxidants, as well as for the production of food supplements and in the pharmaceutical industry (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.).

A high phenol content was found in the aerial parts and seeds. Extracts of these parts of the plant showed a significant antiproliferative effect on the TOV-112 cell line (Nowak et al., 2016Nowak R, Szewczyk K, Gawlik-Dziki U, Rzymowska J, Komsta L. Antioxidative and cytotoxic potential of some Chenopodium L. species growing in Poland. Saudi J Biol Sci. 2016;23(1):15-23.).

Chenopodium album L. is herbaceous and an annual species growing up to 1 m in height. The stem is grayish, with upright or raised branches. The leaves are alternate. The lower leaves have the greatest width, the middle ones are elongated with sharp ends, and the upper ones are narrow and pointed. This is a monoecious plant. The flowers are clustered in glomerulus. The perianth basically shrinks and almost closes the ripe fruit. It has five anthers and two stamps. The pericarp is smooth. The seeds are mostly round and black. Flowering lasts from late May to October. Pollination is done by wind. The species grows on substrates varying from strongly acidic to alkaline. It prefers well-drained conditions and is found on chernozem, podzol or gley soils. It is found in open habitats exposed to anthropogenic influence and grows in association with other weed species (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

Ch. album is a good source of functional nutrients and has healing properties. It has a high functional potential in addition to basic nutritional benefits. It is used in the diet in order to provide minerals, fiber, vitamins and essential fatty acids, improving the sensory and functional value of food. It can be incorporated into various extruded food products to make them more nutritious and healthier. Adding leaves of this species to products can improve chemical and nutritional parameters (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.).

Ch. album shows a zone of inhibition against Staphylococcus aureus, Bacillus subtilis, Streptococcus faecalis, Pseudomonas aeruginosa, Salmonella typhi, Vibrio colerae, Shigella disenteriae, Escherichia coli, Penicillium notatum, Aspergillus niger and against Candida albicans. Ch. album prevents cell growth progression and increases cell toxicity in breast cancer cell lines. The findings highlight the potential of this plant to become a clinically used bioagent with ability to suppress the development of breast cancer malignancy (Khoobchandani et al., 2009Khoobchandani M, Ojeswi BK, Sharma B, Mohan M. Chenopodium album prevents progression of cell growth and enhances cell toxicity in human breast cancer cell lines. Oxid Med Cell Longev. 2009;2(3):160-165.).

Ch. album is traditionally used for blood purification and as a sedative. It exhibits hepatoprotective and antiscorbutic activities. Pharmacological studies have revealed that the plant has antihelmintic properties, the ability to immobilize sperm and has a role in contraception. The antipruritic and antinociceptive effect was also confirmed (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.). This plant is also acknowledged to be used as a cardiotonic, digestive, diuretic and laxative drug. Its action has been proved against dyspepsia, bloating, pharyngopathy and splenopathy. The leaf powder is made to suppress irritation, and the leaf juice is used to treat burns. The use of this plant has also been documented in the treatment of liver disorders and blindness. It is also used as animal feed. The leaves are rich in potassium and vitamin C (Sarma, Sarma, Sarma, 2008Sarma H, Sarma AM, Sarma CM. Traditional knowledge of weeds: a study of herbal medicines and vegetables used by the Assamese people [India]. Herba Pol. 2008;54(2):80-88.).

Commercial exploitation of Ch. album in many regions of the world is still far from reality. Its active ingredients can be isolated and further evaluated for the development of useful drugs (Table I) since the established antioxidant and antibacterial activities have additionally confirmed its biological value. The studies should stimulate the use of Ch. album in areas where it can be grown (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.).

Chenopodium rubrum L. has an upright and smooth stem of green or reddish color. It is an annual, herbaceous plant which can reach a height up to 50 cm. The stem and leaves are succulent and the leaves are rhombic or triangular. Flower glomeruli are small and arranged in clusters being gathered into compact or loose complex inflorescences. The leaf sheath is composed of 5 free leaves at the apical flowers and 3 fused leaves at the lateral ones. It has 2 to 5 anthers and 2 stamps. The seeds are black. This plant is found in open vegetation, on the shores of saline or unsalted waters. It is widespread in Europe, Asia and North America (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

A high phenol content was found in aerial parts and seeds. The extracts of the aerial part of Ch. rubrum showed a good antioxidant effect (Nowak et al., 2016Nowak R, Szewczyk K, Gawlik-Dziki U, Rzymowska J, Komsta L. Antioxidative and cytotoxic potential of some Chenopodium L. species growing in Poland. Saudi J Biol Sci. 2016;23(1):15-23.). Methanolic extracts were reported to exhibit high antioxidant potential through various tests (Mynarski et al., 2018Mynarski A, Pietrzak W, Galanty A, Dawiec E, Nowak R, Podolak I. Phenolic acid LC/MS profile of Chenopodium rubrum and evaluation of cytotoxic activity. Nat Prod Commun. 2018;13(7):855-857.).

In methanolic extracts of different parts of this plant, eleven phenolic acids were identified. The most common were p-coumaric, ferulic and salicylic acid. The highest concentration of phenolic acids was in the leaves and roots (Mynarski et al., 2018Mynarski A, Pietrzak W, Galanty A, Dawiec E, Nowak R, Podolak I. Phenolic acid LC/MS profile of Chenopodium rubrum and evaluation of cytotoxic activity. Nat Prod Commun. 2018;13(7):855-857.).

The toxicity of oxidized phytosterols of this plant was analyzed on the type of roundworm (Tenebrio molitor) (Meyer et al., 1998Meyer W, Jungnickel H, Jandke M, Dettner K, Spiteller G. On the cytotoxity of oxidized phytosterols isolated from photoautotrophic cell cultures of Chenopodium rubrum tested on meal-worms Tenebrio molitor. Phytochemistry. 1998;47(5):789-797.). By testing the cytotoxic effect, the seed extract showed activity against malignant melanoma of the VM 793 cell line. The extracts were reported to have cytotoxic effects on cell lines such as TOV112D, HT-15, HT-27, IMR-32 and A-549 (Mynarski et al., 2018Mynarski A, Pietrzak W, Galanty A, Dawiec E, Nowak R, Podolak I. Phenolic acid LC/MS profile of Chenopodium rubrum and evaluation of cytotoxic activity. Nat Prod Commun. 2018;13(7):855-857.).

This plant is considered to be good for grazing and is used on the Asian continent to feed sheep, goats, camels and horses. It is a good source of protein and carotene, without the risk of poisoning caused by tannins or oxalates, as in Bassia scoparia (Davis, 1979Davis AM. Forage quality of Kochia prostrata compared with three browse species. Agron J. 1979;71:822-824.).

Genus Salicornia

Salicornia europaea L. (Figure 2) is an annual halophytic species (Piernik et al., 2017Piernik A, Hrynkiewicz K, Wojciechowska A, Szymańska S, Lis MI, Muscolo A. Effect of halotolerant endophytic bacteria isolated from Salicornia europaea L. on the growth of fodder beet (Beta vulgaris L.) under salt stress. Arch Agron Soil Sci. 2017;63(10):1404-1418.) that has a succulent structure and a leafless stem (Davy, Bishop, Costa, 2001Davy AJ, Bishop GF, Costa CSB. Salicornia L. (Salicornia pusilla J. woods, S. ramosissima J. woods, S. europaea L., S. obscura PW ball & tutin, S. nitens PW ball & tutin, S. fragilis PW ball & tutin and S. dolichostachya moss). J Ecol. 2001;89(4):681-707.). The stem consists of a series of cylindrical internodes evenly branching out. The internodes consist of the central marrow and the external photosynthetic cortex surrounding it. Those at the base generally reject the external cortex and undergo secondary thickening and lignification (Ellison, Niklas, Shumway, 1993Ellison AM, Niklas KJ, Shumway S. Xylem vascular anatomy and water transport of Salicornia europaea. Aquat Bot. 1993;45(4):325-339.). Under conditions of increased salinity, many genes involved in lignin biosynthesis and the lignification process are regulated in this species. This is consistent with reports claiming that reduced cellulose synthesis induces lignification (Fan et al., 2013Fan P, Nie L, Jiang P, Feng J, Lv S, Chen X, et al. Transcriptome analysis of Salicornia europaea under saline conditions revealed the adaptive primary metabolic pathways as early events to facilitate salt adaptation. PLoS One. 2013;8(11): e80595.).

FIGURE 2
Salicornia europaea L.

S. europea is present in habitats exposed to salt. These can be shores, tidal streams, salt lakes, and salt water springs (Piernik et al., 2017Piernik A, Hrynkiewicz K, Wojciechowska A, Szymańska S, Lis MI, Muscolo A. Effect of halotolerant endophytic bacteria isolated from Salicornia europaea L. on the growth of fodder beet (Beta vulgaris L.) under salt stress. Arch Agron Soil Sci. 2017;63(10):1404-1418.). It can be found on the Atlantic coasts in Western and Northern Europe, on the shores of the Baltic, the Mediterranean, the Black Sea and the Caspian Sea, as well as on the continental salt habitats of the Iberian Peninsula, Pannonian and Wallachian lowlands and on the steppes of Ukraine and Russia (Stevanović, 1999Stevanović V. Crvena knjiga Flore Srbije. Beograd, Ministarstvo za životnu sredinu Republike Srbije, I tom; 1999.).

This is one of the most resistant (Davy, Bishop, Costa, 2001Davy AJ, Bishop GF, Costa CSB. Salicornia L. (Salicornia pusilla J. woods, S. ramosissima J. woods, S. europaea L., S. obscura PW ball & tutin, S. nitens PW ball & tutin, S. fragilis PW ball & tutin and S. dolichostachya moss). J Ecol. 2001;89(4):681-707.) and the most salt-tolerant plants (it can tolerate concentrations greater than 1M NaCl) (Rozema, Schat, 2013Rozema J, Schat H. Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environ Exp Bot. 2013;92:83-95.; Zare-Maivan et al., 2015Zare-Maivan H, Daviran M, Ghanati F, Sharifi M. Salicornia europaea L. maintains its physiological integrity under high salinity stress in retreated sections of the Urmia Lake, Iran J Persian Gulf. 2015;6(22):79-89.). It requires an appropriate concentration of NaCl for normal growth and development. It accumulates high concentrations of inorganic ions in cell vacuoles, mainly sodium and chloride, thereby managing to maintain a low water potential in its tissues (Davy, Bishop, Costa, 2001Davy AJ, Bishop GF, Costa CSB. Salicornia L. (Salicornia pusilla J. woods, S. ramosissima J. woods, S. europaea L., S. obscura PW ball & tutin, S. nitens PW ball & tutin, S. fragilis PW ball & tutin and S. dolichostachya moss). J Ecol. 2001;89(4):681-707.). In addition to the bladder and glands, it is able to accumulate significant amounts of Na+ in the shoots (Davy, Bishop, Costa, 2001Davy AJ, Bishop GF, Costa CSB. Salicornia L. (Salicornia pusilla J. woods, S. ramosissima J. woods, S. europaea L., S. obscura PW ball & tutin, S. nitens PW ball & tutin, S. fragilis PW ball & tutin and S. dolichostachya moss). J Ecol. 2001;89(4):681-707.; Ushakova et al., 2005Ushakova SA, Kovaleva NP, Gribovskaya IV, Dolgushev VA, Tikhomirova NA. Effect of NaCl concentration on productivity and mineral composition of Salicornia europaea as a potential crop for utilization NaCl in LSS. Adv Space Res. 2005;36(7):1349-1353.).

This species is a source of secondary metabolites that exhibit various biological activities. This species has therapeutic properties such as antioxidant, antidiabetic, anti-inflammatory, cytotoxic and anti-obesity. In Asia, it is used as a traditional medicine for diabetes, nephropathy, hepatitis, diarrhea (Kim et al., 2021Kim S, Lee EY, Hillman PF, Ko J, Yang I, Nam SJ. Chemical structure and biological activities of secondary metabolites from Salicornia europaea L. Molecules. 2021;26(8):2252.). Also, it is used in the treatment of hypertension and as an anticancer, antihypertensive and anti-inflammatory agent (Tundis et al., 2009Tundis R, Menichini F, Conforti F, Loizzo MR, Bonesi M, Statti G, et al. A potential role of alkaloid extracts from Salsola species (Chenopodiaceae) in the treatment of Alzheimer’s disease. J Enzyme Inhib Med Chem. 2009;24(3):818-824.).

S. europaea is especially rich in oil and oleic acid. Ethanol, methanol and aqueous extracts have shown strong antimicrobial and antifungal effects. Methanol extract had the strongest effect (Karan et al., 2021Karan S, Turan C, Sangun MK, Eliuz EAE. Bioactive compounds and antimicrobial activity of glasswort Salicornia europaea. Indian J Pharm Sci. 2021;83(2):238-246.). Immunomodulatory compounds were identified in crude extracts (Im, Kim, Lee, 2003Im SA, Kim GW, Lee CK. Immunomodulatory activity of Salicornia herbacea L. Components Nat Prod Sci. 2003;9:273-277.). Antihyperglycemic and antihyperlipidemic activity was found in mice whose diet was high in fat (Park et al., 2006Park SH, Ko SK, Choi JG, Chung SH. Salicornia herbacea prevents high fat diet-induced hyperglycemia and hyperlipidemia in ICR mice. Arch Pharm Res. 2006;29:256-264.). The polysaccharide extract had anti-inflammatory action in vivo and in vitro (Park et al., 2006Park SH, Ko SK, Choi JG, Chung SH. Salicornia herbacea prevents high fat diet-induced hyperglycemia and hyperlipidemia in ICR mice. Arch Pharm Res. 2006;29:256-264.). Isolated polysaccharides were recorded to activate macrophages playing a significant role in the host defense system (Ksouri et al., 2011Ksouri R, Ksouri WM, Jallali I, Debez A, Magné C, Hiroko I, et al. Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Crit Rev Biotechnol. 2011;32(4):289-326.; Lee et al., 2006Lee KY, Lee MH, Chang IY, Yoon SP, Lim DY, Jeon YJ. Macrophage activation by polysaccharide fraction isolated from Salicornia herbacea. J Ethnopharmacol . 2006;103:372- 378.).

Since high salt intake causes arterial dysfunction and hypertension, the effect of S. europaea on vascular function and blood pressure was investigated. It was determined that it caused no coronary artery dysfunction, despite the high salt content in it. The vascular protective effect is attributed to trans-ferulic acid. These results indicate the potential use of this species as an alternative for salt purification and prevention and alleviation of hypertension (Panth et al., 2016Panth N, Park SH, Kim HJ, Kim DH, Oak MH. Protective effect of Salicornia europaea extracts on high salt intake- induced vascular dysfunction and hypertension. Int J Mol Sci. 2016;17(7):1176.).

Some previously done researches showed that desalinated powder of this species, due to its antihypertensive and antidiapogenic properties, can be used in the diet with the aim of controlling obesity (Rahman et al., 2018Rahman MM, Kim MJ, Kim JH, Kim SH, Go HK, Kweon MH, et al. Desalted Salicornia europaea powder and its active constituent, trans-ferulic acid, exert anti-obesity effects by suppressing adipogenic-related factors. Pharm Biol . 2018;56(1):183-191.). The extracts showed hypoglycemic effects by inhibiting the enzyme α-amylase (Li et al., 2007Li F, Li W, Fu H, Zhang Q, Koike K. Pancreatic lipase- inhibiting triterpenoid saponins from fruits of Acanthopanax senticosus. Chem Pharm Bull. 2007;55:1087-1089.).

S. europaea was also recorded to have a beneficial effect on chronic diseases associated with oxidative and inflammatory stress. Desalinated and enzyme- digested ethanol extract has bioefficiency since it possesses significant polyphenols and f lavonoids. This extract shows multifactorial disease modification activities and can be used as an effective therapeutic or dietary supplement for the treatment of amnesic neurodegenerative complications and neuroinflammatory disorders (Karthivashan et al., 2018Karthivashan G, Park SY, Kweon MH, Kim J, Haque ME, Cho DY, et al. Ameliorative potential of desalted Salicornia europaea L. extract in multifaceted Alzheimer’s- like scopolamine-induced amnesic mice model. Sci Rep. 2018;8(1):1-16.).

Ethanolic extracts showed strong antifungal activity and were effective at very low concentrations. They had an inhibitory effect on four species of fungi: Alternaria alternata, Cladosporium sphaerospermum, Fusarium oxysporum and Botritis cinerea (Al-Abbasi, 2018Al-Abbasi WEAM. Antimicrobial and cytotoxic activities of selected Qatari flora (Master’s thesis). Qatar University. 2018. pp. 81.).

S. europea has been noted to exhibit significant cytotoxic activity against Artemia salina Leach and Daphnia magna Straus. An extract of this plant also showed antineoplastic activity in a potato test (Lellau, Liebezeit, 2003Lellau TF, Liebezeit G. Cytotoxic and antitumor activities of ethanolic extracts of salt Marsh plants from the lower saxonian Wadden sea, Southern North sea. Pharm Biol. 2003;41(4):293-300.). S. europea is collected in salty semi- deserts in Central Asia in order to obtain soda. It is otherwise poisonous because it contains oxalic acid, bound to sodium ions (Stevanović, 1999Stevanović V. Crvena knjiga Flore Srbije. Beograd, Ministarstvo za životnu sredinu Republike Srbije, I tom; 1999.).

An appropriate coordination of carbon fixation and nitrogen metabolism in S. europea chloroplast was determined under saline conditions. This plant could be used to fix carbon from saline soil. Since the photosynthesis is regulated under a high degree of salinity, the possibility of exploiting this pioneer plant should be considered in the future (Fan et al., 2011Fan P, Feng J, Jiang P, Chen X, Bao H, Nie L, et al. Coordination of carbon fixation and nitrogen metabolism in Salicornia europaea under salinity: comparative proteomic analysis on chloroplast proteins. Proteomics. 2011;11(22):4346-4367.).

Genus Suaeda

Suaeda maritima (L.) Dumotr. (Figure 3) is an annual, upright plant that has a hard stem up to 60 cm in height. In the upper part it is branched and hairless, with densely distributed leaves. The leaves are alternate, succulent, gray-green or reddish, 1-2 cm long. The flowers are located in groups of 3 to 5 in the axils of the leaves and form clusters. It is pollinated by anemophilia and dispersed by anemochoria. The seeds are smooth, black and about 8 mm long. This plant blooms from July to September (Stevanović, 1999Stevanović V. Crvena knjiga Flore Srbije. Beograd, Ministarstvo za životnu sredinu Republike Srbije, I tom; 1999.). It is a typical halophyte that grows on highly saline habitats such as the solonchak type of soil. It is found in the Pannonian area of Europe, in Austria, Hungary, Serbia, Romania (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

FIGURE 3
Suaeda maritima (L.) Dumotr.

Individuals of this plant grown in conditions of high salinity have higher fresh and dry weight in comparison to the plants grown on standard medium. Improved plant growth at high salt concentrations was evident only after prolonged exposure to high salinity and was attributed to increased cell size. No growth increase was recorded at low NaCl concentrations. In the state of salinity stress exposure, S. maritima was able to maintain high turgor and relative water content, which can be attributed to its prominent capacity for osmotic adjustment. The main osmotics are Na+ and glycine betaine and the expression of the betaine aldehyde dehydrogenase gene in this species was observed to increase with increasing salt and salt stress. However, at lower salt concentrations, the plant accumulated higher levels of proline in their leaves (Moghaieb, Saneoka, Fujita, 2004Moghaieb RE, Saneoka H, Fujita K. Effect of salinity on osmotic adjustment, glycinebetaine accumulation and the betaine aldehyde dehydrogenase gene expression in two halophytic plants, Salicornia europaea and Suaeda maritima. Plant Sci. 2004;166(5):1345-1349.).

In biological tests of antioxidant activity, the extracts of leaves and stems showed a strong antioxidant property of 70% to 92% for phenol and total antioxidant capacity. They also displayed a fairly good content of ascorbic acid, as well as the ability to chelate metals. From the four extracts estimated to have antimicrobial activity, two leaf extracts (acetone and ethanol) showed pronounced antimicrobial activity. The methanolic extract of the stem demonstrated the activity against one pathogenic bacteria compared to standard amoxicillin. The potential antioxidant and antimicrobial properties of this plant extract can be applied in the pharmaceutical industry (Patra, Dhal, Thatoi, 2011Patra JK, Dhal NK, Thatoi HN. In vitro bioactivity and phytochemical screening of Suaeda maritima (Dumort): A mangrove associate from Bhitarkanika, India. Asian Pac J Trop Med . 2011;4(9):727-734.).

Nutritional values, such as dietary fiber, calcium and antioxidant substances with non-toxic properties, were identified in the dried plant of S. maritima and remained present after the storage period at 25 °C, for a period of 3 months. High levels of dietary fiber and calcium were measured. However, due to the high amount of sodium, the use of this plant should be avoided in some risk groups (hypertension, cardiovascular disease and kidney disease) (Sudjaroen, 2015Sudjaroen Y. Evaluation for nutritive values and antioxidant activities of dried seablite (Suaeda maritima). Sci Res Essays. 2015;10(9):306-312.).

The dried parts of S. maritima extracted with water exhibited higher antioxidant activity than ethanol extract. By comparing the antioxidant activities of dried and fresh plants it was proved that these activities were reduced in dried plants, but the antioxidant effect remained (Patra, Dhal, Thatoi, 2011Patra JK, Dhal NK, Thatoi HN. In vitro bioactivity and phytochemical screening of Suaeda maritima (Dumort): A mangrove associate from Bhitarkanika, India. Asian Pac J Trop Med . 2011;4(9):727-734.; Ravikumar et al., 2011Ravikumar S, Gnanadesigan M, Inbaneson SJ, Kalaiarasi A. Hepatoprotective and antioxidant properties of Suaeda maritima (L.) Dumort ethanolic extract on concanavalin-A induced hepatotoxicity in rats. Indian J Exp Biol. 2011;49:455-460.). Natural antioxidants inhibit tumor growth selectively due to different redox status between normal cells and cancer cells (Nair et al., 2021Nair J, Lima PMT, Abdalla AL, Molnar LJ, Wang Y, McAllister TA, et al. Kochia (Bassia scoparia) harvest date impacts nutrient composition, in vitro degradability, and feed value more than pre-harvest herbicide treatment or herbicide resistance traits. Anim Feed Sci Technol. 2021;115079.).

A cytotoxic activity test showed that hexane and ethanol extract of S. maritima produced no toxic effects (Sudjaroen, 2015Sudjaroen Y. Evaluation for nutritive values and antioxidant activities of dried seablite (Suaeda maritima). Sci Res Essays. 2015;10(9):306-312.). Hepatoprotective and antioxidant properties of this species were also recorded. Preliminary phytochemical analysis showed the presence of triterpenoids (Table I), which may be responsible for hepatoprotective activity. This can be useful for the development of herbal medicine through the usage of this species in the treatment of hepatitis (Ravikumar et al., 2011Ravikumar S, Gnanadesigan M, Inbaneson SJ, Kalaiarasi A. Hepatoprotective and antioxidant properties of Suaeda maritima (L.) Dumort ethanolic extract on concanavalin-A induced hepatotoxicity in rats. Indian J Exp Biol. 2011;49:455-460.).

Genus Salsola

Salsola soda L. (Figure 4) is an annual plant reaching a height from 5 to 70 cm. The stem is smooth, gray-green or gray-red and branches strongly from the base. The branches are upright or lying down. The leaves are opposite and succulent, 2-3 mm thick. They are linearly lanceolate and initially pointed, and later have a rounded tip. The lower ones are longer and opposite, and the upper ones are alternating and short. The flowers in the axils have 1 or 2 classes. The bracts are triangular. The leaves of the flower sheath are ovate, more or less serrated at the top. The fruit is ovoid and together with the shell about 5 mm wide. The seeds are globular, black, shiny and 4 mm wide. It is found in occasionally flooded habitats and very salty places on solonchaks. It is widespread in Europe and Asia (Slavnić, 1972Slavnić Ž. Chenopodiaceae. In: Josfović M, editor. Flora of SR Serbia III, Belgrade: SANU , 1972.).

FIGURE 4
Salsola soda L.

Four flavonoids (rutin, quercetin 3-O-glucuronopyranoside, isorhamnetin 3-O-rutinoside and isorhamnetin 3-O-glucuronopyranoside) were isolated from S. soda and their activity was tested on three human recombinant enzymes: aldose reductase (hAKR1B1), aldose-reductase-like protein (hAKR1B10) and carbonyl reductase 1 (hCBR1). All flavonoids inhibited these three enzymes and quercetin 3-O-glucuronopyranoside was the most effective one. These findings indicate the potential use of this species due to its beneficial effect on pathological conditions associated with diabetic complications and inflammatory processes, as well as in cancer therapy (Iannuzzi et al., 2020Iannuzzi AM, Moschini R, De Leo M, Pineschi C, Balestri F, Cappiello M, et al. Chemical profile and nutraceutical features of Salsola soda (agretti): Anti-inflammatory and antidiabetic potential of its flavonoids. Food Biosci. 2020;37:100713.).

The recent studies have shown that it can potentially be used in phytostabilization of contaminated areas since it accumulates moderate amounts of heavy metals (Milić et al., 2012Milić D, Luković J, Ninkov J, Zeremski-Škorić T, Zorić L, Vasin J, et al. Heavy metal content in halophytic plants from inland and maritime saline areas. Open Life Sci. 2012;7(2):307-317.). The species can accumulate selenium and can be used in the diet as a selenium- rich vegetable (Centofanti, Bañuelos, 2015Centofanti T, Bañuelos G. Evaluation of the halophyte Salsola soda as an alternative crop for saline soils high in selenium and boron. J Environ Manage. 2015;157:96-102.). Extracts of S. soda exhibited a good activity in the treatment of hypertension (hypotensive properties) (Loizzo et al., 2007Loizzo MR, Tundis R, Statti GA, Passalacqua NG, Peruzzi L, Menichini F. In vitro angiotensin converting enzyme inhibiting activity of Salsola oppositifolia Desf., Salsola soda L. and Salsola tragus L. Nat Prod Res . 2007;21(9):846-851.). An alkaloid extract was obtained from the aerial parts and its anticholinesterase activity was tested. This plant showed selective inhibitory activity against butyrylcholinesterase suggesting the potential use of this species against Alzheimer’s disease (Tundis et al., 2009Tundis R, Menichini F, Conforti F, Loizzo MR, Bonesi M, Statti G, et al. A potential role of alkaloid extracts from Salsola species (Chenopodiaceae) in the treatment of Alzheimer’s disease. J Enzyme Inhib Med Chem. 2009;24(3):818-824.).

It is used as a vegetable and it is served in restaurants in Italy. It has recently been documented as one of the endemic species on alkaline soils typical of Central and Eastern Europe, as well as the Carpathian Basin (Török, Kapocsi, Deak, 2012Török P, Kapocsi I, Deak B. Conservation and management of alkali grassland biodiversity in Central Europe. In: Zhang, W.-J. (Ed.), Grasslands: types, biodiversity and impacts. Nova Science Publishers, Haupppage, New York. 2012;109-118.).

DISCUSSION

Halophytes are used in traditional medicine in several ways and in the treatment of various diseases (Ksouri et al., 2011Ksouri R, Ksouri WM, Jallali I, Debez A, Magné C, Hiroko I, et al. Medicinal halophytes: potent source of health promoting biomolecules with medical, nutraceutical and food applications. Crit Rev Biotechnol. 2011;32(4):289-326.; Zhao et al., 2010Zhao L, Niu J, Li C, Ma P, Dang Z. Allelopathy of aqueous extracts of Kochia scoparia on flaxseed. Acta Prataculturae Sin. 2010;19(2):190-195.), such as diabetes, asthma, hypertension, rheumatism, gout, etc. Also, they can be used as diuretics, antiparasitics, antipyretics, laxatives and other (Stanković, 2019Stanković M, Jakovljević D, Stojadinov M, Stevanović ZD. Halophyte species as a source of secondary metabolites with antioxidant activity. Ecophysiology, abiotic stress responses and utilization of halophytes. Springer, Singapore. 2019;289-312.). Many species of the family Amaranthaceae are obligate halophytes (Atriplex, Bassia, Camphorosma, Salicornia, Suaeda, Salsola species) and are present exclusively on saline soils and saline habitats (Stanković, 2019Stanković M, Jakovljević D, Stojadinov M, Stevanović ZD. Halophyte species as a source of secondary metabolites with antioxidant activity. Ecophysiology, abiotic stress responses and utilization of halophytes. Springer, Singapore. 2019;289-312.). Most species of the family Amaranthaceae have economic significance. Chenopodium and Atriplex species have been used in human nutrition for a long time due to their nutritional properties (source of protein, minerals, vitamin A). Salsola soda is also used in diets as a vegetable (Török, Kapocsi, Deak, 2012Török P, Kapocsi I, Deak B. Conservation and management of alkali grassland biodiversity in Central Europe. In: Zhang, W.-J. (Ed.), Grasslands: types, biodiversity and impacts. Nova Science Publishers, Haupppage, New York. 2012;109-118.), while Salicornia europaea is used as a salad and as a spice (Kim et al., 2021Kim S, Lee EY, Hillman PF, Ko J, Yang I, Nam SJ. Chemical structure and biological activities of secondary metabolites from Salicornia europaea L. Molecules. 2021;26(8):2252.; Patel et al., 2016Patel S. Salicornia: evaluating the halophytic extremophile as a food and a pharmaceutical candidate. 3 Biotech. 2016;6(1):104.). Chenopodium and Atriplex species are also used as animal feed (Dadáková et al., 2013Dadáková E, Vrchotová N, Tříska J, Děkanová Z. Content of phenolic substances in the selected species of the Chenopodiaceae family. J Agrobiol. 2013;30(2):127-135.), as well as Kochia species since its seeds contain 84% of unsaturated fatty acids (Salehi et al., 2012Salehi M, Kafi M, Kiani AR. Effect of salinity and water deficit stresses on biomass production of Kochia (Kochia scoparia) and trend of soil salinity. Seed Plant Prod J. 2012;27(4).).

Chenopodium, Salicornia, Suaeda, and Salsola species are used in medicine and pharmacy, but also in traditional medicine due to their medicinal properties. Ch. album is used as a diuretic, laxative, and sedative (Ibrahim et al., 2007Ibrahim LF, Kawashty SA, Baiuomy AR, Shabana MM, El-Eraky WI, El-Negoumy SI. A comparative study of the flavonoids and some biological activities of two Chenopodium species. Chem Nat Compd. 2007;43(1):24-28.) and has antirheumatic, anthelmintic, and antiphlogistic properties (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.). The whole plant Ch. ambrosioides has analgesic, carminative, antiasthmatic, and vermifuge properties and is used to treat intestinal and abdominal pain (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.). It also exhibits antifungal (Kumar et al., 2007Kumar R, Mishra AK, Dubey NK, Tripathi YB. Evaluation of Chenopodium ambrosioides oil as a potential source of antifungal, antiaflatoxigenic and antioxidant activity. Int J Food Microbiol. 2007;115(2):159-164.), anthelmintic (Ketzis, 1999Ketzis JK. The anthelmintic potential of Chenopodium ambrosioides in goats. Cornell Universit; 1999.), trypanocidal (Kiuchi et al., 2002Kiuchi F, Itano Y, Uchiyama N, Honda G, Tsubouchi A, Nakajima-Shimada J, Aoki T. (2002). Monoterpene hydroperoxides with trypanocidal activity from Chenopodium ambrosioides. J Nat Prod . 2002;65(4):509-512.) and Antileishmanial activity (Monzote et al., 2006Monzote L, Montalvo AM, Almanonni S, Scull R, Miranda M, Abreu J. Activity of the essential oil from Chenopodium ambrosioides grown in Cuba against Leishmania amazonensis. Chemoterapy. 2006;52:130-136.). Ch. hybridum possesses analgesic, while Ch. vulvaria has antispasmodic properties (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.).

A large number of species of the family Amaranthaceae form an integral part of arid or ruderal environments and are adapted to these conditions (Gelin, Mosyakin, Clemants, 2003Gelin Z, Mosyakin LS, Clemants ES. Chenopodiaceae. Flora of China. 2003;5:351-414.). Some of them represent weed species (Beta spp., Chenopodium spp., species Atriplex rosea).

Most of the described species have a high content of secondary metabolites, especially phenolic compounds and flavonoids. Flavonoids are mainly present in the Atriplex, Beta, Chenopodium and Suaeda species. Phenolic compounds are present in Atriplex, Chenopodium, Salicornia, and Suaeda species. Chenopodium species, as being representative of this family, can be considered as a very good source of natural antioxidants, since all the described species have a high content of phenolic compounds or flavonoids and exhibit antioxidant activity. Phenols, sterols and terpenes were identified in species Ch. album, Ch. ambrosioides and Ch. rubrum, while only terpenes were observed in species Ch. rubrum and Ch. vulvaria (Kokanova-Nedialkova et al., 2009Kokanova-Nedialkova Z, Nedialkov TP, Nikolov DS. The genus Chenopodium: Phytochemistry, ethnopharmacology and pharmacology. Pharmacogn Rev. 2009;3(6):280-306.).

Chenopodium species have essential oils with a large number of active compounds. Ascaridol is among the two most abundant compounds in the described Chenopodium species. Limonene is the second main ingredient of the essential oil of species Ch. album and Ch. polyspermum. Compound α-terpinene was detected in Ch. rubrum and α-terpinyl acetate in Ch. vulvaria (Dembitsky, Shkrob, Hanus, 2008Dembitsky V, Shkrob I, Hanus LO. Ascaridole and related peroxides from the genus Chenopodium. Biomed Pap Med fac Univ Palacky Olomouc. 2008;152(2): 209-215.).

CONCLUSION

Many species of Amaranthaceae family are adapted to saline environments and inhabit coastal and continental habitats, arid areas, and deserts. Presented halophytic species from the family Amaranthaceae represent a source of biologically active substances exhibiting various activities such as antioxidant, anticancer, antibacterial, antifungal and others. Due to these activities, these species have wide application in traditional and modern medicine. Their extracts can be used in the pharmacological industry, while the aerial parts are often used for making teas and infusions. Also, some of them are a rich source of functional nutrients and can be used in food industry. In addition to numerous economic properties, certain species could be used in phytoremediation, phytostabilization and revegetation. The species of the family Amaranthaceae can have multi- purpose applications, but additional pharmacological studies are needed since a small number of halophytes have been tested so far.

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Publication Dates

  • Publication in this collection
    16 Jan 2023
  • Date of issue
    2022

History

  • Received
    15 Apr 2021
  • Accepted
    04 Nov 2021
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