Russian Sage Revealed: Exploring Biology, Cultivation, and Chemical Dimensions of Salvia yangii

Abstract

Plant species in the Lamiaceae family are known worldwide for their therapeutic potential, conferred in particular by the great diversity of essential oils they produce. Although much less known and cultivated than the “star” species of this family, Salvia yangii (formerly Perovskia atriplicifolia) presents special potential both medicinally and as an ornamental species due to its special abilities to withstand conditions unfavorable to other related species. This paper explores the specialized literature from both a bibliometric and comprehensive point of view, in order to systematize the existing information about this species from the last 28 years. S. yangii is a species with a rich array of bioactive compounds, such as terpenoids, diterpenoids, triterpenoids, phenolic compounds, and essential oils, offering promising therapeutic effects including antibacterial, antifungal, anti-inflammatory, antioxidant, and neuroprotective properties. Despite its significant potential, this species remains insufficiently studied and undervalued; further research is needed to fully understand its medicinal and ecological value, optimize extraction methods, and explore its broader applications in pharmaceuticals, agriculture, and eco-friendly solutions in phytoremediation.

1. Introduction

The Lamiaceae family is one of the largest and most promising botanical families consisting of approximately 230 genera and more than 7000 species [1]. It includes a wide variety of aromatic and medicinal plants, many of which are cultivated. This family is economically important due to the diverse uses of its species in therapeutic, cosmetic, industrial, culinary, and ornamental applications [2].

Salvia yangii B. T. Drew, popularly known as Russian Sage [3], is a species from the Lamiaceae family with significant potential due to its medicinal properties [4], as well as its ornamental value. The species is native to Afghanistan, Pakistan, Tibet, West Himalaya, and Xinjiang [5] and cultivated worldwide [3]. Although not as well-known or widely used as its relatives rosemary, lavender, oregano, basil, and common sage, S. yangii offers a diverse array of chemical compounds that could serve as a valuable resource in phytotherapy. At the same time, it holds high ornamental value and can play a beneficial role in arid ecosystems by consolidating soil and providing habitat for pollinators such as bees and butterflies [6]. Its traditional uses include being a parasiticide and analgesic in Tibet [7], treatingfevers [8] and rheumatic pain [9], and acting as an antidiabetic [10], sedative, expectorant, and antibacterial drug [11].

Russian sage is being explored as a promising candidate for phytoremediation due to several key characteristics. It is capable of tolerating and accumulating heavy metals from contaminated soils without transferring these metals to its essential oils, which makes it safe for use in areas where the cleanup of pollutants is needed [12,13]. Studies have shown that S. yangii can grow in polluted and dry areas, demonstrating resistance to both metal contamination and radioactivity.

Its high growth rates, pest resistance, and drought tolerance [14,15] further enhance its suitability for phytoremediation. The plant’s ability to thrive in harsh environments, such as those with heavy metal contamination, without significant reduction in yield, makes it an effective choice for cleaning up polluted soils [13].

This species has shown potential in improving air quality due to its volatile oils, which contain monoterpenes known to help enhance the atmosphere [13]. These factors position S. yangii as a valuable plant for soil and air remediation, especially in arid, polluted areas.

Although species in the Lamiaceae family have been intensively studied over time, S. yangii has not received the same attention from the researchers. However, existing work reveals special properties that this species possesses and requires further investigation to elucidate some aspects, as well as optimize its potential uses.

The purpose of this paper is (1) to bibliometrically analyze articles indexed in the Web of Science database to observe research trends, the main themes addressed regarding Salvia yangii (formerly Perovskia atriplicifolia Benth.), and identify further areas for investigation; and (2) to conduct a comprehensive analysis of the existing knowledge about this species up to date, including aspects related to taxonomy, culture, morphology, anatomy, bioactive compounds extracted from various parts of the plant, and their main actions.

2. Materials and Methods

To carry out this study, an extensive analysis of various databases was conducted. For the bibliometric analysis, the Web of Science (WOS) (accessed 18 January 2025) database was queried (All Fields) using the keywords “Perovskia atriplicifolia” or “Salvia yangii”. This source was chosen because it contains articles that have undergone a rigorous peer-review process and are considered to include the most significant scientific papers. The Web of Science (WoS) is a primary resource for evaluating global scientific output, known for its broad multidisciplinary and international scope. It covers more than 10,000 journals and incorporates four citation databases [16]. We performed the database query also using the name Perovskia atriplicifolia because the species was only recently relocated to the genus Salvia [17], and some authors have continued to use the older, synonymous name in their research after that date.

The query of the WOS database resulted in 58 records. Of these, 3 were eliminated because their content did not specifically refer to S. yangii (1 was referring to P. artemisioides and 2 referring to P. abrotanoides). In total, 53 records were retained. These data were exported in RIS and BibTeX formats and used in the bibliometric analysis.

The bibliometric analysis was performed using the Bibliometrix software (University of Naples Federico II, Italy) (version 4.3.1) available at https://www.bibliometrix.org/home/index.php (accessed on 18 January 2025) [18] and VOSviewer (Leiden University, the Netherlands) (version 1.6.20) available at https://www.vosviewer.com (accessed on 18 January 2025).

Given that this review aims to gather as much existing data as possible from the specialized literature on S. yangii, including its biology, cultivation, chemical composition, and main uses, a detailed search of papers indexed in Scopus and Google Scholar was conducted to complement the information obtained from the primary Web of Science database.

3. Results

3.1. Bibliometric Analysis Regarding the Evolution of Knowledge About the Species S. yangii

To highlight the research trends on S. yangii from 1997 to 2024, the following bibliometric parameters were examined: the type of paper, the number of papers published per year and their citation trends, the most relevant countries of the authors, the Web of Science (WoS) categories in which the articles are classified, the most significant publications, the co-occurrence network of terms derived from the titles and abstracts of the papers, and a word cloud diagram based on the “Keywords Plus” to highlight the major research themes addressed by the authors.

Of the fifty-five papers analyzed, fifty are articles (90.91%), three are proceeding papers (5.45%), and two are meeting abstracts 2 (3.63%). These collected 446 citations without self-citations.

The number of publications is relatively low, but the trend is clearly increasing. Between 1999 and 2014, the number of records per year was low, ranging from 0 to 2. However, in 2015, this number rose to 6, and in the following years, until 2024, it has often been 4 to 5 per year. The number of citations followed a similar trend, starting at under 10 per year between 1999 and 2006 (corresponding to the low number of publications on this subject), and reaching 100 per year in 2023. This increase reflects growing interest among researchers in a less-studied species with great potential (Figure 1).

The countries with the most authors, in descending order, are Iran (18), Pakistan (15), Poland (13), China (10), the USA (5), Italy (3), Egypt, Iraq, Romania, and Turkey (2 each), Austria, Canada, France, Hungary, Lithuania, Saudi Arabia, South Korea, Spain, Sweden, Switzerland, and Yemen (1 each).

A more interesting perspective emerges from the analysis of the most relevant countries, conducted with Bibliometrix. This analysis visually represents both papers produced through international collaboration and those created by authors from a single country (Figure 2).

The results show that researchers from Turkey and Canada (with only one registered paper) have conducted all their works without collaboration, while Poland has produced most of its studies through collaboration with international researchers. In contrast, authors from Iran, Pakistan, and Italy have about half of their papers in collaboration with foreign researchers, whereas China, Romania, and Korea have published papers without external collaboration.

The first 10 WOS categories are the following (Figure 3): Plant Sciences (14, representing 25.45%), Chemistry Medicinal (11, representing 20%), Chemistry Multidisciplinary (9, representing 16.36%), Pharmacology Pharmacy (9, representing 16.36%), Horticulture (8, representing 14.54%), Chemistry Applied (6, representing 10.9%), Biochemistry Molecular Biology (5, representing 9.1%), Food Science Technology (5, representing 9.1%), Agronomy (3, representing 5.45%), and Biology (3, representing 5.45%). This highlights the growing interest of researchers in the fields of chemistry, pharmacy, and experimental biology regarding this species, due to its medicinal properties and the numerous active compounds with pharmacological effects that have been extracted and identified. The horticultural potential of S. yangii should not be overlooked either, as it is successfully cultivated worldwide for its ornamental as well as therapeutic properties.

Keyword analysis plays a central role in bibliometric studies, as it offers valuable insights into the evolving themes and trends within a research domain. By examining the frequency and context of keywords, we can identify emerging topics, track shifts in focus over time, and gain a deeper understanding of the direction in which a particular field is advancing [19].

The co-occurrence network was realized using Vos Viewer v.1.6.20, a very good tool that can be used to perform correlation analysis between terms extracted from different sections of papers. In our analysis, we used the keywords from the title and abstract. The counting method was the binary one, which quantifies in the occurrence calculation the number of documents in which the term appears at least once. Out of 1608 terms, at an occurrence of five, 33 words met the criteria. Of these, four were eliminated as too general or irrelevant (benth, value, number, study). Twenty-nine terms remained, grouped into three clusters (Figure 4), as follows: Cluster 1—12 items: “addition”, “alpha humulene”, “camphor”, “cineol”, “composition”, “concentration”, “effect”, “essential oil”, “Lamiaceae”, “Pakistan”, “Perovskia”, “plant”. Cluster 2—12 items: “change”, “content”, “expression”, “gene”, “leaf”, “medicinal plant”, “root”, “rosmarinic acid”, “S. yangii”, “Salvia”, “species”, “treatment”. Cluster 3—5 items: “analysis”, “compounds”, “Perovskia atriplicifolia”, “structure”, “value”.

Cluster 1 (in red) represents research on essential oils derived from S. yangii, specifically looking at the chemical composition, concentration of compounds, and the effects of these oils, with a focus on plants found in Pakistan, which is one of the species’ range of origin and the country where most of the phytochemical research on this species has been conducted. The presence of terms like alpha humulene, camphor, and cineol suggests the analysis of the main bioactive compounds in these oils.

Cluster 2 (in green) represents research on S. yangii, focusing on gene expression, medicinal properties, and the presence of important bioactive compounds. The studies involve both the leaf and root of the plant, in the context of their pharmacological effects or treatment applications. Cluster 2 indicates a focus on the genetic, biochemical, and medicinal aspects of S. yangii with an emphasis on rosmarinic acid and its potential therapeutic uses.

Cluster 3 (in blue) represents research focusing on the chemical analysis of S. yangii (syn. P. atriplicifolia), particularly on its bioactive compounds. The research investigates the chemical structure of these compounds and evaluates their value, either in terms of therapeutic potential or other commercial applications.

The word cloud diagram (Figure 5), based on the “Keywords Plus” feature, was created using Bibliometrix. Keywords Plus are generated by WOS and include terms or phrases that appear frequently in the titles of the references cited within an article, but are not present in the article’s own title (Popescu et al., 2024 [20]). These keywords often highlight related concepts or topics, providing further insight into the article’s research area. The diagram offers a visual summary of the most frequently mentioned concepts in the references of the selected papers, revealing central themes and emerging trends in the field. Terms such as “chemical composition”, “essential oil” and “constituents” represent the most common keywords, as they relate to the numerous studies on the chemical composition of the species.

The appearance of the term “abrotanoides” among the top five Keywords Plus is linked to studies comparing Perovskia abrotanoides to S. yangii, with most investigations on this species being referenced. The word cloud also features terms related to the biochemistry of the species, such as “tanshinone”, “secondary metabolites”, “essential oil” and “diterpenoids”; its uses, including “folk medicine” and “antioxidant activity”; as well as its morphological and physiological properties, such as “drought stress”, “metabolism” “morphology” and “trichomes”. These terms summarize the three main research directions that have been explored so far regarding S. yangii.

3.2. Taxonomy

Salvia yangii was known until a few years ago as Perovskia atriplicifolia Benth., with most studies using this name for the investigated species. The genus Perovskia Kar. belongs to the Nepetoideae subfamily, Mentheae tribe, and Salviinae subtribe [4].

Recently, five genera from the Lamiaceae family, subtribe Salviinae, namely Perovskia, Rosmarinus, Dorystaechas, Meriandra, and Zhumeria were included in the genus Salvia, based on a molecular phylogeny study using two low-copy nuclear gene regions (PPR-AT3G09060, GBSSI). In this context, P. atriplicifolia has become a synonym for the currently accepted species S. yangii [17].

The genus Salvia is the largest genus within the Lamiaceae family comprising over 1000 species spread across all continents, originating from Southeast Asia, Europe (Mediterranean area), Central America, and South America [21,22].

Although the genus Salvia was long assumed to be monophyletic [21], particularly based on the characteristic presence of two fertile stamens, molecular biology research has revealed its polyphyletic nature [17,21]. Recent phylogenetic studies show that the particularities regarding stamen structure along with other morphological features, evolved independently [23]. Staminal evolution within the Salvia clade demonstrates three independent origins of the staminal lever mechanism, each arising from the elongation of connective tissue and progressing through a similar series of stages, such as elongation, loss of fertility in the posterior theca, and fusion of connective branches. Using the rbcL and trnL-F gene regions along with broad sampling within Salvia, Walker (2004) [21] was the first to identify that the Salvia genus is non-monophyletic.

The affinities between Rosmarinus and Perovskia have been previously reported [24], these being considered “satellite” genera for Salvia, according to the opinion expressed by Frodin [25], according to which most large genera, containing over 500 species, usually have satellite taxa.

3.3. Morphological Description

S. yangii is a deciduous perennial species that grows to a height of 0.8–1.5 m [26]. The stems are rigid, grayish-white, and covered with trichomes, with each individual having several branches on the same rhizome [27]. The young stems are square in cross-section [28], this being a common characteristic of species from the Lamiaceae family. The silvery-grey leaves are opposite, decussate and short petioled, pinnatipartite, with a cuneate base. They measure approximately 5 cm in length and 2.5 cm in width [29,30]. The leaves at the base of the inflorescence are undivided. Like the stems, the leaves are covered with numerous trichomes. The inflorescence is violet in color, and pleasantly fragrant, with verticillasters in lax racemes or panicles approximately 10–30 cm long. The calyx is deciduous, and purple, with five or six lobes with a ciliate margin. The corolla is tubular, bilaterally symmetrical, and bilabiate; four petals unite in the upper lip, and one remains to form the lower lip [27]. The fruit is an obtuse, glabrous nutlet.

The distyly phenomenon has been described in S. yangii: there are two types of flowers, some with two exerted stamens and a short style (S-morph), and others with a long style and short stamens (L-morph) [31].

The flowering period is long, but variable depending on the climatic conditions in which the species grows; this can last from June to October [32,33].

3.4. Culture

S. yangii is a shrub species cultivated worldwide, both as an ornamental plant, valued for its purple inflorescences and pleasant, long-lasting scent, and for its medicinal properties, which have been recognized since ancient times [10]. The species is undemanding, growing in semi-arid habitats and being tolerant to drought and pests [34], and it can be maintained in cultivation with minimal effort [13]. The species tolerates high-intensity solar radiation, as well as large temperature variations [15]. These properties make it advisable for cultivation in countries with large arid areas, including urban habitats. In a study conducted in Iran, on three species of sage belonging to the genus Perovskia, S. yangii proved to be the most resistant to drought conditions, compared to S. artemisioides and S. abrotanoides [35].

The species prefers alkaline soils, not being favorable to acidic and swampy soils [28].

When grown in culture, it is recommended that in early spring the stems of the previous year be cut to 10–25 cm above the ground; this stimulates the formation of new stems, which will bear the inflorescences [28].

The species is suitable for cultivation in gardens, with Bredikhina and collaborators [36] proposing a “rock garden” variant featuring medicinal plants, which includes, in addition to S. yangii, other well-known Lamiaceae species from the genera Mentha, Hyssopus, Lavandula, and Thymus.

The species shows adaptations to survive in water-deficient environments, its growth is slowed down in the case of severe water stress. For example, root volume is reduced by approximately 50% under extreme drought conditions, while root length increases slightly [37]. The drought resistance of the species can be improved by treatment with chitosan, which increases the amount of assimilatory pigments, and proline content (which plays an important role in water uptake and protects plants against oxidative stress) [38], as well as root and stem biomass [37].

From an ornamental point of view, S. yangii can subsume lavender species, due to its morphological and coloristic similarities with it [39]. Adding to this its greater drought resistance compared to lavender, S. yangii can replace this popular species, especially in habitats with limited water resources.

Although S. yangii is a species resistant to less favorable environmental conditions, it responds positively to the application of nitrogen fertilizers in moderate doses [40]. Following the application of fertilizers at concentrations of 150 and 250 mg·L⁻¹ N, a slight increase in dry matter and overall plant quality was recorded. However, at higher concentrations of 350 mg·L⁻¹ N, these parameters decreased, indicating that the plant does not tolerate elevated fertilization levels, as observed in other Lamiaceae species such as Salvia nemorosa L. and Lamium maculatum (L.) L. [40].

Due to its medicinal and ornamental properties, S. yangii has also attracted the interest of researchers in the field of in vitro culture to preserve the unique characteristics of valuable individuals. The plant has demonstrated increased potential for micropropagation through cuttings [41]. Adventitious root formation can be stimulated using indole-3-butyric acid (IBA) and alpha-naphthyl acetic acid (ANA). The rooting percentage increased nearly tenfold when using a mixture of Rhizopon AA (20% IBA) and Rhizopon B (10% ANA) solutions, from 6.72% in the control to 66.4% in the treated variant. Cuttings of S. yangii treated with 500 ppm IBA showed the highest rooting percentage, rooting speed, as well as root length compared to S. abrotanoides and S. artemisioides [42]. Additionally, when using a perlite and sand substrate, the roots obtained were of superior quality in terms of both their number and length [41]. This phenomenon is explained by the plant’s known preference for sandy soils in its natural habitat [14].

From a metabolic point of view, the species shows important plasticity in terms of adaptation to environmental conditions: cultivated in vitro, S. yangii showed significant changes in the carnosic acid content, which increased with increasing temperature to which the plants were exposed [15]. Cold treatment for a prolonged period (5 months) on S. yangii seeds led to an increase in their germination capacity, as well as to obtaining more vigorous and larger seedlings compared to two other related species—S. abrotanoides and S. artemisioides (all three species previously belonging to the genus Perovskia) [42].

3.5. Anatomical and Micromorphological Aspects

In contrast to the existing literature on the essential oils produced by S. yangii, information on the secretory structures that produce these metabolites is very limited. The leaves, stems, and flowers are covered with peltate and capitate glandular trichomes [43], as well as multicellular, ramified non-glandular trichomes [13], with the latter being responsible for the silvery color of the aboveground parts of the plant [33]. These non-glandular trichomes are short and branched [44], forming a dense covering that contributes to the plant’s protection from solar radiation and confers tolerance to extreme environmental conditions. The density of glandular trichomes decreases from young to mature leaves, which correlates with the cessation of new glandular trichome formation as the leaf matures [13].

Peltate glandular trichomes are classified into two types. Type I, which is more widespread on leaves, stems, and floral parts, has a short unicellular stalk and a large secretory head with 12 glandular cells. These trichomes are located in epidermal depressions. Type II, which is rarer, is found only on the sepal surface and differs from Type I by having a longer stalk. Capitate trichomes are more common than peltate trichomes and consist of a basal cell, a short unicellular stalk, and a bi-cellular secretory head [13]. At maturity, these glandular trichomes accumulate volatile oil in subcuticular spaces, which is released when the cuticle breaks. Micromorphological investigations, using scanning electron microscopy (SEM), revealed that the cuticle covering the glandular trichomes lacks pores or spaces for volatile oil exudation, which only occurs when the cuticle breaks accidentally or at the end of the glandular trichome’s life [13]). A rare type of trichome, with both branched tector trichomes and a terminal part resembling Type I, was also found on the stem. This was first described in Phlomis fruticosa L. [45] and later described in detail in P. herba-venti L. [46].

The anatomy of the leaf of S. yangii reflects its adaptation to environments with very intense lighting. The leaf structure is bifacial isofacial, with bi- or tri-stratified palisade tissue, formed by long and narrow cells, under both epidermises [47]. This architecture of the assimilatory tissue is possible only if the light intensity is high enough to ensure the efficiency of photosynthesis throughout the thickness of the leaf blade.

3.6. Biotic Interactions

In the current context of the major decline in pollinators worldwide, stable pollinator populations can be maintained in urban areas through targeted horticultural practices, such as planting diverse floral resources and managing pollinator habitats [48]. In addition to its medicinal uses, we note that S. yangii plays an important role in supporting pollinators.

Russian sage is a very good melliferous plant, that is attractive to bees that produce a transparent honeydew with a specific aroma when feeding on this plant [6]. Giovanetti and collaborators [49] investigated the attractiveness of S. yangii plants to Anthidium spp. bees (Hymeoptera: Megachilidae) in both urban and rural parks. They observed bee visitation frequencies and collected data on flower characteristics and morphology. They found that S. yangii strongly attracted Anthidium bees in both areas, with different bee communities visiting the plants in urban and rural environments. Anthidium bees were more frequent visitors than honeybees, especially in urban parks, and both male and female bees visited the flowers. The floral traits of the plant were consistent with the genus Salvia, making it beneficial to pollinators and visually attractive. Although not native, S. yangii is non-invasive and could be recommended for use in urban and rural gardens to support wild pollinators [49].

Another study [48] on the attractiveness of S. yangii to bees compared it with another Salvia species, S. azurea Michx. ex Vahl, a resource for a wide range of pollinators, including monarch butterflies, Danaus plexippus (L.), (Lepidoptera: Nymphalidae) [50]. S. yangii plants attracted 317 insects (data collection took place for 5 h per week during the flowering season over 2 years). Of the visiting insects, the majority were Apis mellifera L. (over 50%), followed by Bombus impatiens Cresson (Hymenoptera: Apidae) and Anthidium manicatum (L.) (Hymeoptera: Megachilidae). The latter, the European wool-carder bee, is an invasive species recently introduced to North America. It is a direct competitor to the native bumblebee, B. impatiens, limiting access to resources provided by local flora on which it typically feeds [51]. Other insect species that pollinated S. yangii included Agapostemon virescens (Fabricius) (Hymenoptera: Halictidae), A. manicatum, Ceratina ssp., and Xylocopa virginica L. (Hymenoptera: Apidae), but their numbers were significantly lower. In contrast, S. azurea was visited by only 155 insects, with the first three species being the same as those found on S. yangii, which indicates that the species share the same pollinator groups [48].

Other studies have highlighted the presence in the vicinity of S. yangii flowers of various pollinators, from Hymenoptera (honeybees, bumblebees, carpenter bees), but also from Diptera and Lepidoptera [52], within a larger study that targeted 20 species of perennial plants with an ornamental role in the parks of Texas.

Limonene in the composition of essential oils has an attractive effect on pollinating insects [53], which explains the quality of the S. yanggi species as a melliferous plant and a support for wild pollinators.

Its vibrant flowers attract not only bees, but also butterflies, and other beneficial insects, contributing to the health of local ecosystems. The plant’s ability to thrive in urban and suburban environments while providing a food source for pollinators highlights its ecological importance [48].

Pests are rarely reported on S. yangii, their absence probably being determined by the effect deterrent of the essential oil it produces. Monoterpenes are synthesized by plants as a defense strategy to safeguard against herbivores and pathogens. High concentrations of these compounds can make plants unpalatable or toxic to many potential predators like insects or mammals, effectively deterring them from feeding on the plant [53]. The Rosemary beetle Chrysolina americana (Coleoptera: Chrysomelidae) has been reported to be one of the few species that has the ability to feed and live on the leaves of S. yangii [54]. The species is considered a pest for other Lamiaceae species lavender, rosemary, and thyme, which denotes low sensitivity to the components of essential oils from species of this family.

3.7. Chemical Compounds from Salvia yangii

3.7.1. Terpenes

Terpenes and their oxygenated derivatives, the terpenoids, represent the largest group of secondary metabolites produced by plants (over 25,000 compounds) [55]. In S. yangii, diterpenoids, triterpenoids as well as monoterpenes/monoterpenoids and sesquiterpenes/sesquiterpenoids (as components of essential oils) have been identified as active compounds.

• Diterpenoids

Diterpenoids (oxygenated derivatives of diterpenes) are a class of secondary metabolites, with 20 carbon atoms, formed from four isoprenoid units [56], with one or more oxygen-containing functional groups (such as aldehyde, ketone, or hydroxyl groups).

Icetexanes are a group of diterpenoids naturally produced by plants, which are based on a 6-7-6 tricyclic framework [57]. Przewalskin E was isolated from the aerial parts of the species S. yangii, harvested from Tibet [7]. This compound was first isolated from Salvia przewalskii Maxim [58].

Perovskatone A [59], perovskatone B, 1α-hydroxybrussonol [7], and compounds from the same icetexane diterpenoids group have demonstrated inhibitory actions on hepatitis B virus activities (HepG 2.2.15 cell line was tested). Other compounds of the same class, isolated from S. yangii are 1α-hydroxypisiferanol, perovskatones C and D, and brussonol [7]. Although no tests have been performed on extracts obtained from S. yangii, brussonol and derivatives have demonstrated antiplasmodial properties, manifesting potent inhibitory activity against Plasmodium falciparum (Welch), including efficacy against resistant strains [60]. Considering that brussonol offers a natural, effective, and potentially safer alternative to synthetic antimalarial drugs, the use of extracts obtained from S. yangii deserves investigation in this regard.

Abietane diterpenoids, including carnosic acid and carnosol (its major derivatives), represent some of the most valuable groups of active substances isolated from species of the genus Salvia; they are composed of a tricyclic skeleton with three fused six-membered rings and alkyl functional groups [61]. Along with essential oils, these are the main constituents with therapeutic effects in species of the Perovskia subgenus [59].

Among the abietane diterpenoids—carnosic acid and carnosol have been isolated from the roots of S. yangii [62], which have a strong antioxidant effect, comparable to that of synthetic substances such as butylated hydroxyanisole (BHA) [63]. The amount of carnosol in leaves decreases in S. yangii as the end of the flowering season approaches; the related species, S. abrotanoides, shows the opposite behavior, with the amount of carnosol increasing with the completion of the flowering stage [62]. Carnosic acid and its derivatives have been shown to have significant antifungal effects [64]. The tested compounds were isolated from Salvia canariensis L., a species closely related to S. yangii [22]. Also, carnosic acid is rare in the plant kingdom, found in only nine out of two hundred and twenty Lamiaceae genera, and is valued for its antioxidant properties, making it increasingly used as a food additive in Europe (under the code E392) [15].

Other abietane diterpenes isolated from the leaves of S. yangii were rosmanol (detectable only in the middle of the growing season, at flowering), epi-rosmanol, isorosmanol 12-dimethylrosmanol (present only at the beginning and end of the flowering season) [65], 11-methylrosmanol, and 7-methylrosmanol; from roots OH-cryptotanshinone, isograndifoliol, and cryptotanshinone were extracted in larger quantities [62].

Two new diterpenoids, one of the abeoabietane type (biperovskatone B) and one of the icetexane group (1α-hydroxyl demethylsalvicanol quinine), extracted from the aerial part of the plants harvested in Chengdu (China) have significant anti-HBV activity [66].

Tanshinones are red-colored diterpenoid quinones that were first extracted from the roots of Salvia miltiorrhiza Bunge, a species used in traditional Chinese medicine [65]; the compounds exhibit antibacterial, antioxidant, anti-inflammatory, anti-aging, anti-convulsant, cardiac protective, and anticancer effects [3,67]. Ślusarczyk and collaborators [3] describe four diterpenoids extracted from the mature roots of S. yangii, namely (1R)-1-acetoxytanshinone IIA, (15R)-1-oxoaegyptinone A, (1R,15R)-1-acetoxycryptotanshinone, and isograndifoliol. The latter two compounds have shown significant activity in inhibiting butyrylcholinesterase (BChE), positioning this species as a potential source of bioactive compounds for combating dementia and other neurodegenerative diseases.

• Triterpenoids.

Triterpenoids are a class of substances derived from triterpenes (which have 30 carbon atoms). The extract obtained from the dried aerial parts of S. yangii, specifically from the chloroform-soluble sub-fraction, contains compounds with cholinesterase inhibitory activity [68]. The authors identified nine triterpenoids in this extract, two of which—2α,3β,24-trihydroxyolean-12-en-28-oic acid and 2α,3β,19β-trihydroxyurs-12-en-28-oic acid—specifically inhibited butyrylcholinesterase (and also acetylcholinesterase) at a concentration comparable to that of galantamine, an alkaloid used in the treatment of Alzheimer’s disease [69].

Two other triterpenes, Atricins A and Atricins B, oleanane-type triterpenes, were isolated from chloroform-soluble fractions obtained from the aerial parts of S. yangii, originating from Quetta (Pakistan) [70]. Oleanane triterpenoids are pentacyclic structures that have been identified in various organs of some lamiaceae species, usually in leaves (Ocimum tenuiflorum L. Origanum vulgare L., Rosmarinus officinalis L., Salvia officinalis L.), less often in flowers (Lavandula angustifolia Mill.) or roots (Dracocephalum tanguticum Maxim) [71]. Their medicinal potential is high, being used as antimicrobial, anti-inflammatory, cytotoxic, hepatoprotective, and antitumoral [72], but the extraction method, as well as the relatively low quantities in which they are found in the organs of higher plants, do not make them, at least for now, economically attractive for large-scale use [71].

• Monoterpenes, sesquiterpenes, and their derivates from essential oils

Lamiaceae species are known for their significant production of essential oils that give them the status of medicinal and aromatic plants (MAPs). The main components of essential oils from Lamiaceae are monoterpenes and sesquiterpenes (along with their derivatives—monoterpenoids and sesquiterpenoids) [73]. The amount of oil extracted from different plant organs varies considerably depending on the origin of the plant material, the environmental conditions, and the organs from which it is extracted: from 0.38% in S. yangii from Crimea [74], up to 3.2% in populations from Pakistan [6] (

Table 1. The chemical composition of essential oils from Salvia yangii (a synthesis).

Plant Material/Developmental Stage	Essential Oil Yield (w/w)%	The Main Components of the Essential Oil	Collection Site	Components Numbers/ Accounting % of the Oil	Reference
Aerial part/complete flowering	-	P-thujone (45.9%), sabinene (26.6%), α-pinene (12.1%), 1,8-cineole (10.5%)			[76]
Aerial part/complete flowering	2.3	1,8-cineole + limonene (40.13%), α-pinene (17.87%), Δ3-carene (9.13%), β-pinene (6.59%), camphene (6.17%), camphor (5.36%)	National Botanical Garden, Teheran, Iran	19/92.3	[77]
Leaves and flowers	1.32	1,8-cineole (27.5%), Δ3-carene (22.3%), b-caryophyllene (10.8%), α-pinene (5.9%) α-humulene (5.7%)	Quetta, Pakistan	19/96.4	[78]
Leaves/complete flowering	1.47	β-caryophyllene (12.51%), 1,8-cineole (11.7%), limonene (9.66%), α-humulene (9.36%), camphor (7.58%)	Botanical Garden of the Research Institute of Forests and Rangelands Tehran, Iran	46/98	[32]
Stems/complete flowering	2.1	1,8-cineole (15.64%), β-caryophyllene (11.92%), camphor (11.63%), α-humulene (9.55%), α-terpinyl acetate (6.28%), bornyl acetate (6.05%)
Flowers/complete flowering	1.45	1,8-cineole (19.52%), α-pinene (13.97%), camphor (8.6%), limonene (4.76%), β-caryophyllene (8.36%), α-humulene (6.39%)
Aerial part/before flowering (stem 20–30 cm)	1.69	β-caryophyllene (15.87%), α-humulene (14.36%), limonene (11.37%), Δ3- carene (9.77%), T-cadinol (5.35%)		48/98
Aerial part/before flowering (stem 40–50 cm)	1.69	β-caryophyllene (15.52%), α-humulene (13.46%), limonene (11.36%), Δ3-carene (10.75%), camphor (8.19%), 1,8-cineole (7.98%)
Aerial part/before flowering (stem 40–60 cm)	1.57	β-phellandrene (13.55%), camphor (13.49%), Δ3-carene (13.15%), β-caryophyllene (11.68%), 1,8-cineole (10.27%), α-humulene (9.7%), limonene (8.95%)
Aerial part/beginning of flowering (stem 60–75 cm)	1.6	1,8-cineole (19.52%), α-pinene (13.97%), camphor (8.6%), limonene (8.6%), β-caryophyllene (8.36%), α-humulene (6.39%)
Aerial part/complete flowering (stem 90–100 cm)	1.06	1,8-cineole (15.74%), β-caryophyllene (12.3%), camphor (10.16%), α-humulene (9.47%), limonene (7.55%), α-pinene (6.31%), Δ3-carene (5.71%)
Aerial part/complete flowering (stem 100–110 cm)	1.64	1,8-cineole (20.74%), camphor (14.52%), limonene (8.58%), β-caryophyllene (7.9%), α-pinene (7.77%), α-humulene (6.28%), Δ3-carene (6.04%)
Leaves and flowers/flowering stage		1,8-cineole+ limonene (29%), camphor (14.8%), β-caryophyllene (8.7%), Δ3-carene (5.4%), α-pinene (7.3%), α-humulene (6.7%)	National Garden in Tehran, Iran	28/96.9	[8]
Aerial part/flowering stage	3.2	camphor (28.91%), limonene (16.72%), α-globulol (10.2%), trans-caryophyllene (9.3%), α-humulene (9.25%)	Tira, Pakistan	18/96.6	[6]
Aerial part/flowering stage	-	limonene (18%), γ-terpinene (16%), β-caryophyllene (13%), α- caryophyllene (12%), cymene (11%)	SC Miroslava, Iasi, Romania	27/96.02	[29]
Flowers/flowering stage	-	1,8-cineole (15.83%), tau-cadinol (14.67%), α-pinene (10.88%), camphor (8.91%), β-caryophyllene (7.99%), α-caryophyllene (6.96%), 3-carene (4.54%)	Bacău, Romania	52/97.79	[79]
Leaves/flowering stage	-	1,8-cineole (21.36%), camphor (14.31%), tau-cadinol (9.63%), β-caryophyllene (5.88%), α- caryophyllene (5.42%), 3-carene (5.30%)		66/92.22
Aerial part/flowering stage	-	1,8-cineole (24.62%), o-cymene (17.87%), borneol (15.37%), γ-terpinene (6.39%), bornyl acetate (4.83%) camphene (4.66%)	Iasi, Romania	32/94	[13]
Stems/flowering stage	-	1,8-cineole (18.44%), o-cymene (18.23%), bornyl acetate (14.65%), borneol (9.61%), cariophyllene oxide (6.02%)		34/97.16
Leaves/flowering stage	-	borneol (20.41%), 1,8-cineole (19.7%), o-cymene (13.91%), bornil acetate (5.2%), cariophyllene oxide (4.78%), β-caryophyllene (4.66%)		33/98.08
Flowers/flowering stage	-	1,8-cineole (16.3%), o-cymene(11.81%), α-pinene (7.33%), borneol (9.71%), bornil acetate (7.46%), γ-terpinene (14.37%),		47/96.05
Aerial part/flowering stage	-	limonene (17.75%), cymene (17.93), borneole (14.67%), cis-β-ocimene (8.37%), γ-terpinene (7.15%), camfene (4.5%)	Iasi, Romania	28/99.3	[11]
Aerial part/flowering stage	-	limonene (21.47%), 1,8-cineole (16.19%), α-pinene (8.17%), β-caryophyllene (6.20%), bornyl acetate (6.06%)	Botanical Garden of Chişinău, Republic of Moldova	28/95.5	[26]
Flowers/complete flowering	-	1,8-cineole (18.65%), Δ3-carene (11.23%), α-pinene (9.98%), viridiflorene (8.45%), α-humulene (7.55%),	Sistan– Baluchestan region, Iran	24/99.9	[9]
Aerial part/complete flowering	0.9	camphor (27.2%), 1.8-cineol (14.3%), linalool (5.5%), borneol (4.8%), carvacrol (5%)	Nikitsky Botanical Garden, Crimea	30	[80]
Aerial part/complete flowering	-	α-myrcene (16.57%), 1,8-cineole (10.69%), borneol (8.52%), β-caryophyllene (8.30%), α-caryophyllene (7.42%)	Afganistan	-	[81]
Aerial part/complete flowering cultivar ‘Little Spire’	-	1,8-cineole (17.79%), camphor (14.28%), D-limonene (10.93%), Δ3-carene (6.76%), α-pinene (6.64%)
Aerial part/complete flowering cultivar ‘Blue Spire’	-	1,8-cineole (15.72%), β-caryophyllene (10.32%), α-caryophyllene (9.35%), borneol (9.32%), camphor (7.3%), δ-3-carene (7.10%)
Aerial part/complete flowering	0.54	1,8-cineole and limonene (40.13%), α-pinene (17.87%), δ-3-carene (9.13%), β-pinene, (6.59%), camphene (6.17%), camphor (5.36%)	National Botanical Garden Chişinău, Republic of Moldova	39/95.01	[28]
Aerial part/complete flowering (sample 1)	0.38	camphor (21.19%), 1,8-cineole (20.1%), α-pinene (9.54%), endoborneol (6.56%), bornyl acetate (5.7%)	Crimea, Russia	38/99.09	[74]
Aerial part/complete flowering (sample 2)	0.53	endoborneol (29.28%), 1,8-cineole (16.17%), α-pinene (6.28%), bornyl acetate (6.16%), β-caryophyllene (5.04%)		42/98.69
Leaves/before flowering	1.28	geranyl acetate (24.17%), δ-3-carene (6%) 1,8-cineole (5.7%), α-humulene (4.96%), linalool (4.66%), α-pinene (3.8%)	Sistan, Baluchestan, Iran	52/92	[14]
Leaves/flowering	1.15	δ-3-carene (9.88%), 1,8-cineole (9.32%), linalyle acetate (8.15%), geranyl acetate (7.79%), linalool (6.07%), α-humulene (4.21%)		62/86.31
Leaves/complete flowering	1.03	geranyl acetate (33.26%), δ linalyle acetate (8.15%), linalool (7.49%), 1,8-cineole (5.5%), geraniol (5.07%), transcaryophyllene (4.79%), Δ3-carene (4.09%)		43/66.46
Aerial part/complete flowering	0.61	camphor (13.3%), bornyl acetate (11.9%), δ 3-carene (10.8%), 1,8-cineole (10.2%)	Baluchestan, Iran	28/97.4	[37]
Aerial part/complete flowering	1.4	1,8-cineole (12.55%), linalyl acetate (11.48%), Δ3-carene (9.03%), linalool (6.15%), bornyl acetate (3. 51%)	Taftan mountain, Baluchestan, Iran	33/99.41	[82]
Aerial part dry/complete flowering	0.43	1,8-cineole (24.2%), camphor (8.6%), endoborneol (7.3%), bornyl acetate (6.2%), caryophyllene (4.4%)		57/94.0
Aerial part/complete flowering	0.9	1,8-cineole (22.02%), borneol (9.19%) bornyl acetate (10.39%), ∆3-carene (9.09%), camphor (6.08%), β-caryophyllene (5.46%)	Khash– Sistan and Baluchestan, Iran	24/94.27	[83]

), with average values above 1%, which means a significant amount of oil compared to other Lamiaceae species [75].

Based on the data collected from specialized literature, three chemotypes of S. yangii can be deduced, considering the composition of the essential oils:

• Camphor-dominant chemotype: Found in various plant parts, particularly in regions such as Crimea, Iran, and Pakistan, this chemotype has camphor as a major compound (up to 28.91%) [6], along with other compounds like 1,8-cineole and β-caryophyllene [37,74,80].
• 1,8-Cineole-dominant chemotype: This chemotype is the most widespread, observed in several samples, with 1,8-cineole present in high concentrations (27.5% in one sample) [78]. Other common components include limonene, α-pinene, α-humulene, and Δ3-carene.
• Limonene-dominant chemotype: In certain samples from Romania, limonene is one of the major compounds, such as 18% in Miroslava [29] and 17.93% in Iasi [11]. This chemotype is often accompanied by other terpenes like β-caryophyllene and α-pinene.

Additionally, isolated volatile oils have been reported as the main components in specific samples: an oil containing 13.55% β-phellandrene was obtained from the aerial parts of plants harvested before flowering in Iran [32], and an oil rich in P-thujone (45.9%) was described by Mucciarelli [76]. Borneol (20.41%) predominated in the essential oil was extracted solely from leaves harvested during the flowering phase [13], and geranyl acetate (24.17%) was found in leaves harvested before flowering, rising to 33.26% in leaves harvested at full flowering from plants in Baluchestan, Iran [14].

Although there is variability in the chemical composition of essential oils across the samples analyzed by different researchers (Table 1), 1,8-cineole, β-caryophyllene, camphor, and limonene are the main components in most samples, especially those originating from Central Asia. Essential oils with a high content of monoterpenes have anti-aging effects [84]: 1,8-cineole has demonstrated the ability to restore mitochondrial membranes, with a positive effect on ATP synthase. Similar effects are also exerted by linalool, which reduces oxidative stress exerted on mitochondria; their dysfunction is directly linked to the onset of brain diseases, such as Alzheimer’s or cerebral ischemia [85]. Likewise, essential oils containing limonene and 1,8-cineole have analgesic properties, experimentally demonstrated [86]. In most cases, monoterpenes and monoterpenoids exceeded 50% of the total components identified in essential oils from S. yangii [28,78,87].

The quality of the essential oil, and the percentage of the different components, respectively, also varies depending on the method of extraction. A comparative study conducted by Pourmortazavi and collaborators [8], using supercritical carbon dioxide extraction of essential oils, showed that temperature, pressure, and extraction medium can significantly modify the final concentrations of the main constituents. In this case, 1,8-cineole and limonene, which were present at 29% in the case of classical extraction by hydrodistillation, increased to 37.3% (at 100 atm, 35 °C, in CH₂Cl₂) or decreased to 16.8% (at 300 atm, 45 °C).

• Insecticidal effect of essential oil

Essential oils have been reported to have insecticidal activity and are safer for humans and the environment [20]. The essential oil of S. yangii demonstrated complete protection against mosquitoes for 60 min at a dose of 330 μg/cm², similar to the commercial repellent DEET [88]. The main compounds in the essential oil in the tested variety were camphor (19.7%), limonene (10.9%), and α-humulene (6.3%), this being supposed to confer its prolonged protective effect.

The essential oil from three Salvia species, including S. yangii, S. abrotanoides, and S. artemisoides, collected from Taftan mountain, Baluchestan, Iran were tested on the potato tuber moth, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae) [82]. The combined essential oils of S. yangii and S. abrotanoides, applied by fumigation, were toxic to this pest, exhibiting ovicidal and repellent effects. The 25:75 mixture ratio showed higher toxicity to adults (LC₅₀ = 5.82 µL/L air) than to eggs (LC₅₀ = 10.10 µL/L air) and reduced the ovipositional rate.

Ahmadi and collaborators [89] explored the combined effects of gamma radiation and essential oils from R. officinalis and S. yangii on the mortality of Tribolium castaneum Herbst. (Coleoptera: Tenebrionidae) (red flour beetle). The results showed that the combination of gamma radiation and essential oils increased insect mortality more than the individual treatments alone, with a synergistic effect. Sublethal radiation doses (130 Gy and 230 Gy) caused minimal mortality on their own, but when combined with essential oils, mortality was significantly higher. The synergistic effect of the combined treatment was observed to be more effective than either treatment alone.

b.

Antibacterial effect of the essential oil

The essential oil rich in limonene and cymene, extracted from the aerial part during the flowering period (Iasi area, Romania) had an inhibitory action on the species Staphylococcus aureus (Gram-positive), but did not show any effect on the Gram-negative species Escherichia coli [11].

The essential oil with a high content of camphor (28.91%) and limonene showed inhibitory action on Micrococcus luteus, but its effect was 3–4 times lower than that of antibiotics such as penicillin or tetracycline. In the same study, three Gram-positive bacterial species, namely Bacillus subtilis, B. mycoides, and B. cereus. showed increased sensitivity to S. yangii oil, with inhibition zones of 10–14 mm being observed using the agar diffusion method (15 µL essential oil/disk) [6]. Essential oils from Lamiaceae taxa are usually more effective against Gram-positive bacteria than Gram-negative bacteria, which often show increased resistance to them [90] due to the high content of oxygenated monoterpenes.

The increased resistance of Gram-negative bacteria to the effect of essential oils is related to their structural peculiarities, as they have an increased amount of lipopolysaccharides in the outer membrane, which acts as a hydrophobic barrier that prevents the oils from penetrating the membrane [91]. However, some essential oils with a high content of aldehydes (cinnamaldehyde), such as cinnamon oil, disrupt the membrane permeability of Escherichia coli, causing electrolyte leakage and, ultimately, bacterial cell death [91].

c.

Antifungal effect of the essential oil

The essential oil from S. yangii has rarely been tested for its antifungal effects. Inhibitory effects on Candida albicans were recorded by Askarova and collaborators [87], who tested an essential oil with a high content of 1,8-cineole. However, the inhibitory effect was much weaker than that of synthetic fungicides (diameter of the inhibition zone: 6.04 mm vs. 26.04 mm for Fluconazole). Different results were obtained by Erdemgil and collaborators [6], who tested an oil with camphor as the main component on C. albicans. In this case, the essential oil of S. yangii showed a significant antifungal effect, even greater than that of the fungicide Amphotericin B (zone of inhibition: 14 mm compared to 13 mm). The same authors also reported the antifungal activity of the essential oil against species such as Aspergillus niger, A. flavus, A. fumigatus, and Geotrichum candidum, with effects nearly identical to those of synthetic fungicides. Oils with a similar biochemical profile may be useful in the cosmetic, pharmaceutical, and food industries. The antifungal activity of essential oils containing camphor has been demonstrated in several studies on plant species from the families Lamiaceae, Asteraceae, and Zingiberaceae [92].

3.7.2. Phenolic Compounds

Phenolic compounds can be found as secondary products of metabolism in plants in general and in those of the Lamiaceae family in particular [93]; they possess important pharmacological properties, having antioxidant, antibacterial, anti-inflammatory, cardioprotective, anti-aging neuroprotective, and antitumoral activities [93,94].

Perovskoate, a compound derived from isorinic acid (an isomer of rosmarinic acid) and perovskoside, a catechol derivative, were isolated from the ethyl acetate soluble fraction obtained from the aerial part of the species S. yangii [95]. The same authors isolated, for the first time, caffeic acid (a hydroxylated derivative of cinnamic acid) and ferulic acid from this species.

Lariciresinol is a polyphenolic lignan, which was isolated from the chloroform-soluble fraction of the methanolic extract of S. yangii and evaluated for its anti-inflammatory action on leukotriene C4 (LTC4) [30]. The same compound extracted from another plant species (Rubia philippinensis Elmer) showed pronounced antibacterial activity, especially against Staphylococcus aureus [96].

A recent study [93] focused on the antiglycation activity of polyphenolic compounds from S. yangii, a property that explains its use in traditional medicine for the treatment of diabetes [10]. Rosmarinic acid (41.45 mg/100 g dry weight), rutin (25.08 mg/100 g dry weight), and caffeic acid (9.42 mg/100 g dry weight) were the most abundant phenolic compounds out of the 11 total identified [93]. Although there are synthetic glycation inhibitors that have shown promising results in laboratory studies, the identification of natural compounds is preferred due to the numerous side effects of synthetic products [97]. Rutin and rosmarinic acid can prevent or reduce fibril formation, helping to mitigate conditions related to protein aggregation in diseases such as diabetes, kidney dysfunction, Alzheimer’s, and cardiovascular diseases [93].

The large number of compounds with anti-inflammatory activity from extracts made from various parts of the plant suggests the possibility of using them as alternatives to synthetic steroidal anti-inflammatories, which, in addition to their beneficial effects, also have numerous adverse reactions on human and animal organisms [30].

3.7.3. Other Chemical Compounds

A new acylated steroid glucoside, named Atroside A, was isolated from the whole plant harvested in June from Baluchistan, Pakistan [38]. Along with this, other compounds known to have therapeutic properties in other Lamiaceae species, but not evaluated in the S. yangii species, have been isolated: beta sitosterol glucoside (antiinflammatory, chemoprotective, analgesic, anthelmintic, immunomodulatory) [98], stigmasterol (antioxidant, anti-inflammatory, anticancer, and antiosteoarthritis) [99].

4. Conclusions and Future Perspectives

The bibliometric study on S. yangii reveals a clear upward trend in both publications and citations from 1997 to 2024, highlighting a growing global interest in the species. Through keyword and co-occurrence network analyses, the bibliometric study identifies the primary research directions on S. yangii, focusing on its essential oil composition, medicinal properties, bioactive compounds, and its biochemical and morphological characteristics. The study provides important insights into the evolving themes and trends, and underlined the species’ pharmacological and therapeutic potential.

The future of S. yangii is promising, particularly in the pharmaceutical, agricultural, and cosmetic industries, due to its particular chemical profile. The plant’s essential oils, containing bioactive compounds like camphor, 1,8-cineole, limonene, and β-caryophyllene, have shown potential in neurological health, cancer treatment, pest control, and antimicrobial uses. However, further research is needed to isolate active compounds, refine concentrations, and standardize production processes for consistent quality and effectiveness.

Additionally, the structure of glandular trichomes, which synthesize essential oils, needs more study. Investigating their localization and distribution across plant parts and stages could help explain the variation in essential oil composition. With the growing demand for natural, therapeutic products, S. yangii may offer an alternative to synthetic treatments, while its sustainability makes it a candidate for eco-friendly agricultural applications.