Next Article in Journal
Distribution Patterns of Invasive Buffelgrass (Cenchrus ciliaris) in Mexico Estimated with Climate Niche Models under the Current and Future Climate
Next Article in Special Issue
Traditional Uses of Medicinal Plants in South-Western Part of Lithuania
Previous Article in Journal
Anti-Obesity Action of Boerhavia diffusa in Rats against High-Fat Diet-Induced Obesity by Blocking the Cannabinoid Receptors
Previous Article in Special Issue
Eucalyptus globulus and Salvia officinalis Extracts Mediated Green Synthesis of Silver Nanoparticles and Their Application as an Antioxidant and Antimicrobial Agent
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 11
Issue 9
10.3390/plants11091159
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Distribution Patterns of Essential Oil Terpenes in Native and Invasive Solidago Species and Their Comparative Assessment

by
Jolita Radušienė
1,
Birutė Karpavičienė
1,
Mindaugas Marksa
2,
Liudas Ivanauskas
2 and
Lina Raudonė
3,4,*
1
Laboratory of Economic Botany, Nature Research Center, Akademijos Str. 2, 08412 Vilnius, Lithuania
2
Department of Analytical and Toxicological Chemistry, Lithuanian University of Health Sciences, Sukileliu Av. 13, 50162 Kaunas, Lithuania
3
Department of Pharmacognosy, Lithuanian University of Health Sciences, Sukileliu Av. 13, 50162 Kaunas, Lithuania
4
Laboratory of Biopharmaceutical Research, Institute of Pharmaceutical Technologies, Lithuanian University of Health Sciences, Sukileliu Av. 13, 50162 Kaunas, Lithuania
*
Author to whom correspondence should be addressed.
Plants 2022, 11(9), 1159; https://doi.org/10.3390/plants11091159
Submission received: 4 April 2022 / Revised: 19 April 2022 / Accepted: 22 April 2022 / Published: 25 April 2022
(This article belongs to the Special Issue Natural Resources of Berry and Medicinal Plants Volume II)
Browse Figures
Versions Notes

Abstract

:
The importance of invasive Solidago L. species to the environment creates a new approach to controlling their spread through the use of potentially high value raw materials. The aim of this study was to assess the distribution patterns of volatile compounds in the four Solidago spp., by identifying common and species-specific compounds with their potentials, and to confirm the origin of the spontaneous hybrid Solidago × niederederi on the basis of comparative assessment of essential oil (EO) profiles. Plant material in the flowering phase was collected in mixed populations from six different sites. The EOs were isolated separately from the leaf and the inflorescence samples by hydrodistillation for 3 h. The chemical analysis was performed by gas chromatography—mass spectrometry. Multivariate data analysis was employed to explain the interspecies relationships among Solidago spp. The results revealed the similarity among Solidago spp. EO profiles, which were dominated by monoterpenes and oxygenated compound fractions. Solidago spp. differed in species distinctive terpenes and their distribution between accessions and plant parts. Volatile compound patterns confirmed the origin of Solidago × niederederi between Solidago canadensis and Solidago virgaurea, with the higher contribution of alien species than native ones. Correct taxonomic identification of species is highly essential for the targeted collection of raw material from the wild for different applications. Solidago spp. can be considered to be underutilized sources of bioactive secondary metabolites.

1. Introduction

The use of plant products has grown remarkably in recent years, and research into natural products such as volatile terpenoids has become an important task for future human and animal well-being [1]. Natural products are generally easy to prepare and, due to their natural origin, are environmentally friendly and not financially challenging. In this respect, invasive species are of growing interest as a potential resource for obtaining high value-added products. Solidago canadensis L. (Canadian goldenrod) and Solidago gigantea Aiton (Giant goldenrod), native to North America, are considered to be one of the most aggressive plant invaders, which were introduced to Europe as garden ornamentals in the middle of the 18th century and began to spread in the 19th century [2]. Abandoned previously cultivated and disturbed areas contribute to a rapid and successful invasion of goldenrods. Both species form pure dense stands due to the clonal growth of their re-sprouting rhizome system, which provides a strong competitive ability to eliminate other grassland species while reducing biodiversity [3]. Propagation of the Solidago species easily by wind distributed seeds guarantees their distance dispersal and the occupation of new disturbed areas creating homogenized landscape [4]. On the other hand, spontaneous hybridization gives rise to new hybrids, such as sexually reproducing Solidago × niederederi Khek., which was first recorded in Austria more than a century ago [5]. The hybrid has been described as a new alien species between the invasive S. canadensis and native Solidago virgaurea L. (European goldenrod), which is spreading rapidly along with the parental species, increasing the negative impact on the native flora [6,7]. In addition, phytotoxicity of alien species has been often invoked as a significant factor negatively influencing the native species and composition of plant communities [8,9]. The fastest and cheapest result to eradicate or limit the invasion of goldenrods is the use of herbicides [10]. However, the application of herbicides has a negative impact on the environment and their use is limited. Based on the importance of goldenrods to the surrounding environment, a new approach has recently been developed so that invasive species can be a potential source of high value-added products, instead of eliminating them by labor consumption and environmentally unfriendly ways [11]. The high biomass produced by exotic goldenrods is a promising source of renewable energy that can be exploited in rural households as an alternative to expensive firewood and that do not compete with crops for food or animal feed [12]. Late-flowering goldenrods attract pollinators and are honey bee plants that are considered to be superior to crops treated with pesticides [13]. Solidaginis virgaureae herba is included in the ESCOP Monographs with therapeutic indications for the treatment of urinary tract and genital disorders [14]. The European Medicines Agency in a finalized community monograph of Solidago virgaurea confirms traditional use of this plant material for the treatment of minor urinary tract complaints [15]. Furthermore, S. gigantea, S. canadensis, and their hybrids, as well as S. virgaurea, are included in European Pharmacopoeia [16]. A wide range of specialized metabolites have been reported in goldenrod raw materials, of which phenolic compounds and EOs were considered to be the most valuable [17,18,19]. The comparative evaluation of phenolic compounds in Solidago spp. has been presented in our previous studies [20].
Essential oils (EOs), due to the structural diversity in their constituents, expose a wide range of biological effects and are of great interest as a source of functional ingredients for agriculture, food, cosmetics, and pharmaceuticals [21]. Numerous studies have reported the potential use of EOs for integrated weed and pest control as an environmentally friendly approach [22]. Significant antifungal activity of S. canadensis EO was found against Botrytis cinerea, which reduced fruit rot and successfully controlled gray mold in inoculated strawberries [21]. Elshafie et al. [23] has also demonstrated antimicrobial activities of S. canadensis EO in vitro against some other phytopathogens. In this way, EOs of alien Solidago spp. are a promising source for the development of organic pesticides and can meet the high demand for their production. In addition, the allelopathic activity of S. virgaurea is considered as the herbicidal potential of EOs for environmentally acceptable weed control in organic farming [24]. The EO of S. canadensis has been shown to exhibit significant cytotoxic and antiproliferative activities against human tumor cell lines, correlating with the terpene compounds [25,26].
The major constituents of EO usually contribute to the principal role of the biological activity of the mixture, so their efficiency can be predicted to some extent from the complex of components [27]. On the other hand, even minor components have been shown to play a significant role in different biological activities due to their complementary and synergistic effects [28]. Consequently, it is important to know the distribution of phytochemical compounds in species and their populations due to the targeted selection of raw materials for their possible multifunctional use. The study hypothesized that the screening of Solidago spp. growing in the same area and in their mixed populations could provide reasonable comparative information on the volatile profiles and their chemotaxonomic relationships and confirm the origin of the S. × niederederi taxon. The objectives of the study were: (1) to assess the distribution of volatile constituents in the populations of native and alien Solidago spp.; (2) to identify intraspecific and interspecific diversity in Solidago spp.; (3) to identify common and species distinctive volatiles; and (4) to confirm the origin of the spontaneous hybrid S. × niederederi on the basis of a multivariate comparative analysis of volatile profiles.

2. Results

2.1. Essential Oil Content of Solidago Species

Inflorescences took priority over the leaves in EO content in all the evaluated Solidago species. The highest yield of EO was obtained from inflorescences of S. canadensis (0.19–0.26%), followed by S. gigantea (0.16–0.23%), S. × niederederi (0.14–0.20%), and S. virgaurea (0.15–0.18%). Meanwhile, the leaves of S. gigantea accumulated the highest EO content (0.16–0.20%), followed by S. canadensis (0.14–0.18%), S. × niederederi (0.13–0.15%), and S. virgaurea (0.10–0.15%). Previous studies reported the similar range of EO yield in S. canadensis (0.18–0.27%) [23,29] and S. gigantea (0.15–0.16%) [29]. Kalemba [30] reported higher levels of EO contents in S. virgaurea (0.32–0.38%) than levels found in this study.

2.2. Chemical Profiles of Essential Oils

The EOs of four Solidago spp. were dominated by monoterpenes, with an average of 43.9–74.6% of the total composition of EOs in inflorescences and 39.7–69.1% in leaves. The mean percentage of sesquiterpenes ranged from 15.0 to 35.4% in inflorescences and from 25.5 to 38.2% in leaf EOs. Chemical profiles for EOs of Solidago spp. varied according to the contents of individual compounds and their distribution among accessions and plant parts. Examples of fingerprint profiles for inflorescence EOs are shown in Figure 1.

2.2.1. Solidago gigantea

Inflorescence EOs were dominated by monoterpene hydrocarbons (25.4%) and oxygenated sesquiterpenes (19.7%) followed by oxygenated monoterpenes (18.5%) and sesquiterpene hydrocarbons (15.3%). Meanwhile, oxygenated sesquiterpenes (23.3%) and oxygenated monoterpenes (23.1%) were the major chemical fractions in leaf EOs.
The principal compounds in all inflorescence and leaf EOs were α-pinene, bornyl acetate, spathulenol, isospathulenol, and caryophyllene oxide. Nevertheless, there were high differences for other compound prevalences and their concentrations between samples and plant parts. Germacrene D was a major common component in inflorescence oils (3.4–18.3%), whereas this compound was detected in less than half of the leaf samples (1.6–12.7%). One of the major components in the inflorescences was o-cymene (6.8–18.4%), while among the principal compounds in the leaves was β-cubebene (17.3–19.6%), but these compounds were found in only a few EO samples. Additionally, trans-pinocarveol (0.6–1.1%), cis-verbenol (0.3–1.0%), trans-verbenol (1.2–3.0%), and γ-muurolene (0.5–1.1%) were found in minor concentrations in all inflorescence EOs. Meanwhile, camphene (1.54–3.9%), β-pinene (1.0–3.4%), o-cymene (0.8–4.9%), limonene (0.6–1.3%), and γ-cadinene (0.6–1.5%) were common in all leaf EOs.
In agreement with our results, α-pinene, bornyl acetate, germacrene D, and spathulenol have been previously reported to be major components of S. gigantea EOs [29,31,32,33]. In addition, cyclocolorenone, α- and γ-gurjunene, khusinol, and/or ledol and selina-3,11-dien-6-α-ol were also reported as the predominant constituents [31,33], although these sesquiterpenoids were not detected in the S. gigantea EOs tested. According to Gruľová et al. [34], S. gigantea EOs were dominated by sesquiterpene hydrocarbons such as δ-cadinene, γ-muurolene, α-cubebene, and γ-cadinene, and two of them, γ-muurolene and γ-cadinene, were common in the inflorescence or leaf EOs studied.

2.2.2. Solidago canadensis

Monoterpenoids were predominant in S. canadensis EOs, with an average of 46.6.0% in inflorescences and 26.4% in leaves, followed by monoterpenes (28.0%) in inflorescences and sesquiterpenes (24.9%) in leaves. The first or second principal components in most of inflorescence EOs were α-pinene (0.1–36.1), trans-verbenol (5.2–21.7%), and bornyl acetate (3.8–19.8%). Among the most abundant constituents in leaf and inflorescence EOs were α-pinene (1.3–21.8) and bornyl acetate (6.5–20.4%). Leaf EOs were dominated by sesquiterpene hydrocarbons as β-cubebene (6.1–33.6%) and germacrene D (4.0–45.2%), and their concentrations exceeded those in inflorescence oils (0.8–13.1% and 1.9–11.4%, respectively). The other main constituent common for all leaf EOs was isospathulenol (0.7–10.2%). In addition, carvacrol was present as a major compound in two leaf EOs (22.83 and 23.7%) and was not detected in the remaining samples. Other components with noteworthy values in both inflorescence and leaf EOs were limonene (0.3–16.2% and 0.8–10.9%, respectively) and caryophyllene oxide (1.6–10.0% and 1.4–10.4%, respectively). The data revealed that cis-verbenol (0.6–3.7%), pinocarvone (0.9–2.7%), myrtenal (0.8–3.4%), and verbenone (1.0–5.2%) were detected in all inflorescence EOs in highly variable concentrations. Meanwhile, camphene (0.4–2.2%), β-pinene (0.7–2.7%), β-caryophyllene (0.8–6.9%), trans-verbenol (0.5–5.4%), β-elemene (0.6–5.9%), epoxyazulene (0.7–6.47%), and spathulenol (0.4–3.8%) were found in all or most of the leaf EOs.
The presented results are in agreement with previous studies that confirmed α-pinene, limonene, bornyl acetate, germacrene D, β-cubebene, and caryophyllene oxide among the predominant compounds in S. canadensis EOs [19,23,25,33,35]. In addition, studies from different countries have shown that γ-cadinene and myrcene [36,37] sabinene [36], cyclocolorenone [29], or thymol [34] were among the major compounds in S. canadensis EOs. Meanwhile, our results showed a low concentration or frequency of these compounds in the samples tested.

2.2.3. Solidago × niederederi

Solidago × niederederi inflorescence and leaf EO profiles were characterized by oxygenated monoterpenes (41.5 and 35.7%, respectively), followed by monoterpenes (26.4 and 17.7%, respectively), sesquiterpenoids (17.0 and 16.9%, respectively), and sesquiterpenes (6.0 and 15.0%, respectively). The principal constituents in the inflorescence EOs were α-pinene and trans-verbenol, which were the first or second major compounds in seven EOs, accounting for 22.3–31.7% and 13.4–22.9%, respectively. Caryophyllene oxide was among the major constituents in four (7.9–25.3%) and bornyl acetate in three (12.8–21.7%) EOs. Meanwhile, limonene and humulene epoxide II were present in most of the samples, however, dominated only in two (12.2 and 16.3%) and one (28.4%) samples, respectively. All inflorescence EOs contained varied levels of α-campholenal (0.9–6.2%), trans-pinocarveol (1.6–5.4%), and verbenone (0.6–5.1%). Other compounds with a mean content of 1 to 5.0% were β-pinene, camphene, cis-verbenol, pinocarvone, myrtenal, myrtenol, trans-carveol, germacrene D, epoxyazulene, and spathulenol.
Solidago × niederederi leaf EOs contained seven compounds in concentrations above 10% in at least one sample and were considered as principal compounds. The major compounds such as α-pinene (1.1–25.8%), trans-verbenol (2.2–20.2%), bornyl acetate (4.2–20.2%), and caryophyllene oxide (2.1–38.1%) were found in all leaves in highly different concentrations. Verbenone and germacrene D were present in most EOs, averaging 5.2 and 8.8%, respectively, with the exception of the two EOs in which these compounds were predominant, accounting for 20.2 and 18.0%, respectively. Meanwhile, β-cubebene was detected only in two oils (16.4 and 23.9%) in which it was the first or second major compound. One leaf EO contained noteworthy concentrations of thymol (6.4%) and carvacrol (9.5%). In addition, 21 compounds were detected with a mean content of 1 to 5.0%, the most prominent of which were sesquiterpenes such as β-copaene, β-bisabolene, epoxyazulene, humulene epoxide II, and isospathulenol. Similar results for the composition of the major compounds in S. × niederederi EO have been recently published [26]. However, the results of only one plant accession were reported, making the comparison insufficient as the prevalence and number of compounds varied among samples.

2.2.4. Solidago virgaurea

Solidago virgaurea inflorescence and leaf EOs were dominated by monoterpenes fraction, which accounted for an average of 35.9 and 49.0% of the total EO composition, respectively, followed by sesquiterpenes (20.7 and 16.9%, respectively). The main compounds in inflorescence EOs were α-pinene (18.8–36.3%), β-copaene (5.3–21.2%), and caryophyllene oxide (6.7–11.4%). All leaves were predominated by trans-verbenol (10.2–49.0%), two samples prevailed by α-pinene (22.4 and 23.3%) and caryophyllene oxide (10.1 and 14.7%), and one by verbenone (16.9%). Inflorescence and leaf EOs contained 22 and 29 compounds, respectively, with a mean percentage greater than 1% and less or equal to 5%. Among them, the most prominent were β-pinene, limonene, verbenone, α-campholenal, trans-pinocarveol, pinocarvone, bornyl acetate, α-copaene, germacrene D, cubebol, α-muurolene, δ-cadinene, and spathulenol, which were common to all inflorescence and/or leaf EOs.
Similar to our identification, previous studies have confirmed the dominance of monoterpene and sesquiterpene fractions in S. virgaurea EOs [30,32]. Monoterpenes such as α-pinene, myrcene, β-pinene, and limonene together with sesquiterpene germacrene D have been reported as the major constituents in S. virgaurea. In addition, oxygenated sesquiterpenes, humulene epoxide II, spathulenol, selina-3,11-dien-6-α-ol, and caryophyllene oxide have been also considered as major compounds in S. virgaurea EOs [26,33]. Meanwhile, in this study, only α-pinene and caryophyllene oxide were found among the predominant compounds in all EOs tested, and the contents of the other mentioned compounds differed among samples. Meanwhile, selina-3,11-dien-6-α-ol was not detected at all in the presented EOs.

2.3. Interspecific Differences

The results presented revealed similarities and differences in the frequency of distribution and contents of EO constituents among the four Solidago spp. Significant differences in monoterpene and sesquiterpene fractions were found between the inflorescences of the species studied (Table 1). Meanwhile, the chemical groups of compounds in leaves did not differ significantly between the four Solidago spp. (Table 2).
Oxygenated monoterpenes predominated in the EOs of S. canadensis and S. × niederederi inflorescences and S. virgaurea and S. × niederederi leaves. The highest proportion of sesquiterpenoids among the species was found in S. gigantea inflorescences and leaves. Mono- and sesquiterpenes prevailed in the S. virgaurea inflorescence EOs; however, no significant differences were found between the species for monoterpenes. The common principal constituents of the inflorescence and leaf EOs of all four Solidago species were α-pinene, bornyl acetate, and caryophyllene oxide. Species showed significant differences (p ≤ 0.05) in the accumulation of bornyl acetate and caryophyllene oxide in leaf EOs, but no differences in α-pinene were observed between species (Table 1 and Table 2). The highest mean concentration of bornyl acetate was found in inflorescence and leaf EOs of both S. gigantea and S. canadensis, while caryophyllene oxide prevailed in S. × niederederi and S. virgaurea. The other major compound trans-verbenol was prevalent in all inflorescence EOs with the highest level (p ≤ 0.001) in S. canadensis and S. × niederederi. Meanwhile, the leaves of S. virgaurea and S. × niederederi had priority over the other two species in accumulation of trans-verbenol. Inflorescences of S. gigantea accumulated the highest (p ≤ 0.001) level of germacrene D compared to other species, but this compound did not differ significantly (p > 0.05) in the leaves between species. The inflorescences and leaves of S. gigantea were in priority to other species in accumulation of oxygenated sesquiterpenes as epoxyazulene, spathulenol, and isospathulenol. In addition, γ-muurolene, differently other species, was a common compound in all inflorescence EOs of S. gigantea, while other monoterpene hydrocarbons such as camphene and o-cymene were common in all leaf EOs of this species.
The inflorescence EOs of all species differed significantly in the mean concentrations of oxygenated monoterpenes, such as α-campholenal, trans-pinocarveol, cis-verbenol, pinocarvone, verbenone, and trans-carveol, with the highest levels and frequency found in S. canadensis and S. × niederederi, followed by S. virgaurea. The same compounds, with the exception of trans-carveol, differed significantly in leaf EOs, with the highest concentrations in S. virgaurea and S. × niederederi leaves. Meanwhile, trans-carveol was detected in small amounts only in S. canadensis and S. × niederederi leaves. In addition, S. virgaurea inflorescence EOs differed from other species in the highest levels and frequency of distribution in α- and β-copaene, cubebol, α-muurolene, and δ-cadinene. As a consequence, quantitative rather than qualitative differences were observed between the species EOs. However, 10 compounds common in more than 30% of all studied inflorescence and/or leaf EOs did not differ significantly between Solidago spp. (Table 1 and Table 2). Among them, the most abundant were α- and β-pinene, limonene, bornyl acetate, germacrene D, and caryophyllene oxide.

2.4. Principal Component Analysis (PCA)

PCA was employed to explain the phytochemical relationships arising due to inter- and intraspecific differences between the four Solidago spp., using the selected EOs compounds. A scree plot criterion was applied to reduce the number of PCs for explaining the variance in the selected variables. A two-dimensional PCA square matrix model explained more than 53.3% of the total variance and was used to visualize the available patterns of Solidago spp. EOs profiles (Figure 2). PC3 explained only 6.8% of the total variance and had no significant effect on scores differentiation, so results were not presented. PC1 accounted for 29.4% of the total data set variance and showed high negative correlation with α-campholenal, trans-pinocarveol, cis- and trans-verbenol, pinocarvone, myrtenal, myrtenol, verbenone, and trans-carveol and positive with carvone, germacrene D, γ-muurolene, γ-cadinene, spathulenol, and isospathulenol in inflorescences, and camphene, o-cymene, epoxyazulene, and (E)-nerolidol in leaves (Figure 2a). PC2 explained 23.6% of the total data set variance and was highly associated with positive loadings of α- and β-copaene, α-cubebene, cubebol, α-muurolene, and δ-cadinene in inflorescences and with α-campholenal, trans-pinocarveol, cis-verbenol, and pinocarvone in leaves, as well as with negative loadings of bornyl acetate and isospathulenol in leaves.
The PCA score plot model showed the arrangement of 40 EOs into two separate and two overlapping ellipses, each with a 95% confidence interval limit (Figure 2b). The group on the right-hand plot combined all S. gigantea EOs along the positive PC1. Variables with high PC1 loadings contributed the highest impact on the grouping of S. gigantea samples were germacrene D, γ-cadinene, γ-muurolene, and spathulenol in inflorescences, and camphene, o-cymene, epoxyazulene, (E)-nerolidol, and spathulenol in leaves. These compounds were shared among all S. gigantea EOs in the highest amounts compared to the other species studied. Conversely, variables with high PC2 loadings had a weak contribution on the grouping of EOs and were found in minor quantities in S. gigantea.
Solidago virgaurea EOs were clustered into a separate group on the upper positive side of the score plot, in distance from all other samples, indicating differences in their composition. The location of the samples can be explained by the same position of variables, which have a significant positive contribution to PC2. Variables with unit vectors close to each other were positively correlated, and their impact on the position of the samples was similar. Thus, α- and β-copaene, α-cubebene, cubebol, δ-cadinene, and α-muurolene in inflorescences, and α-campholenal, cis-verbenol, trans-verbenol, pinocarvone, and trans-pinocarveol in leaves, were common in S. virgaurea EOs and found in significantly higher amounts than in other species analyzed. Meanwhile, S. canadensis and S. × niederederi EOs were clustered into two partially overlapping ellipses, mainly in the left-hand score plot, showing the similarity of the volatile compound patterns. The arrangement of inflorescence EOs for both species coincided with a significant correlation of α-campholenal, trans-pinocarveol, pinocarvone, verbenone, cis-verbenol, trans-verbenol, myrtenal with PC1. In addition, the clustering of S. canadensis was influenced by myrtenol, trans-carveol, and carvone. Variables with high PC2 loading had no significant impact on EOs’ arrangement, except for trans-verbenol in S. × niederederi leaves, showing similarity of this taxon to S. virgaurea. Meanwhile, a previous study of phenolic compounds showed greater chemical similarity of S. × niederederi to S. virgaurea than to S. canadensis [20]. Consequently, the phytochemical patterns complemented the evidence of S. × niederederi origin between native S. virgaurea and invasive S. canadensis, with the higher contribution of alien species than that of native ones. In addition, S. × niederederi EOs were much more scattered on the PCs space, indicating higher diversity than other species, suggesting that S. × niederederi is a continuously evolving taxon.
Consequently, Solidago spp. EOs differed significantly in the presence of terpenes that could be considered as species distinctive components. The inflorescence EOs of S. gigantea differed from other species by γ-cadinene, γ-muurolene, and spathulenol, and the leaves by camphene, o-cymene, epoxyazulene, (E)-nerolidol, and spathulenol. The inflorescences of S. canadensis and S. × niederederi differed significantly from the other species by the accumulation of oxygenated monoterpenes, such as α-campholenal, trans-pinocarveol, pinocarvone, verbenone, cis-verbenol, trans-verbenol, and myrtenal. In addition, S. canadensis inflorescence EOs were characterized by the prevalence of myrtenol, trans-carveol, and carvone, while S. × niederederi leaves were prominent by trans-verbenol. The species distinctive volatiles in S. virgaurea inflorescence EOs were α- and β-copaene, α-cubebene, cubebol, δ-cadinene, and α-muurolene, and in the leaves—α-campholenal, cis-verbenol, trans-verbenol, pinocarvone, and trans-pinocarveol. Consequently, multivariate data analysis allowed for an explanation in the intra- and interspecific diversity in four Solidago taxa according to the differences in EO volatiles.

3. Discussion

Alien goldenrods are morphologically and phylogenetically close to each other, but differ in their ploidy level; S. gigantea is tetraploid (2n = 36), while S. canadensis, and S. × niederederi together with native S. virgaurea are diploids (2n = 18) [3,38]. The close relationships between Solidago spp. were reflected in the similarity of their phytochemical profiles. A comprehensive metabolomics approach to the different species indicated that the successful alien species had higher total number and more unique composition of secondary metabolites than their native congeners [39]. A comparison of the current and previous reports showed that our results are in agreement with previous reports for higher proportions of sesquiterpenoids in S. gigantea and hydrodrocarbons in S. virgaurea EOs [26,29,32,33]. Similar to our identification, the most abundant common compounds detected in the present study were also observed in previous studies on different species. Thus, the volatiles commonly found in various plant species have a high potential to accumulate in Solidago spp. EOs as well. On the other hand, there were compounds such as thymol and carvacrol, sporadically high levels of which were found in only a few S. × niederederi and S. canadensis EOs. Populations rich in thymol and carvacrol, compounds with a broad spectrum of biological activity [40,41,42], can be considered as a source of high potential raw material. In addition, Solidago spp. EOs differed significantly in some of the terpenes that can be considered as volatiles with great potential in chemophenetic studies of species. The first comparative study on terpenes as species distinctive compounds confirmed the origin of S. × niederederi as an interspecific taxon between S. canadensis and S. virgaurea. According to Orians [43], parental phytochemicals in hybrids tend to mostly express as either intermediate or similar to one of the parent’s compositions. The composition of S. × niederederi EOs was close to S. canadensis, one of parental species. The chromosome number may provide information about the hybrid origin of the species when it display allopolyploidy, but S. × niederederi exhibit a homoploid condition compared to its parental species and may backcross toward parental species. In this way, hybridization can increase the invasive capacity of goldenrods through gene introgression and significantly alter the ecosystems in which they grow [44]. However, species–specific compounds and chromosome number are not the main tools for hybrid identification. DNA fingerprinting techniques are the most reliable tools, but the use of additional phytochemical markers can provide insight into the ecological performance of hybrids and their further applications [45].
More often, the lower proportion of monoterpenes compared to sesquiterpenes [46] accounted for a higher proportion in the Solidago spp. EOs tested. Oxygenated monoterpenes have been proven to be the main phytotoxic active compounds in different plant EOs and have been highlighted as predictors of potential bioherbicides [47]. In addition, a tendency has been suggested that the monoterpene-rich EOs to promote higher phytotoxicity than sesquiterpene-rich EOs [48]. Comparative studies on the toxic activity of oxygenated monoterpenes revealed that the most active were alcohols, myrtenol and trans-pinocarveol, and ketones, verbenone and pinocarvone, which can be classified as predictors of the herbicidal activity of EOs [49,50,51]. Thus, S. canadensis and S. × niederederi, whose EOs differed from other species in some of oxygenated monoterpenes, suggested the potential of their raw materials for herbicidal activity. Meanwhile, terpene hydrocarbons have been found to be low phytotoxic EOs compounds [40,52]. On the other hand, Lawson et al. [36] reported that monoterpenes such as α- and β-pinene, limonene, or myrcene showed weak antifungal activity. Recent findings reported that (E)-nerolidol and spathulenol, which were presented as species–specific sesquiterpenoids in S. gigantea EOs, revealed effective allelopathic and insecticidal effects with potential for the developing a new natural pesticide [53,54,55]. Many findings have demonstrated the biological activity of caryophyllene oxide [53,55,56,57,58] that was a common compound in the presented Solidago spp. EOs. The potential biological activity of EOs is associated with the presence of high oxygenated compounds, as confirmed by a systematic review of phytotoxicity studies [59]. In this context, S. canadensis and S. × niederederi EOs, are of greatest interest in the development of new and safe bioproducts.
Considering the previous and presented results for Solidago spp. EOs, the prevalence of predominant and other compounds varied across different studies, and their comparison is not informative enough. Reports often provide single sample data that are difficult to summarize as a species–specific composition of volatiles. According to Zidorn [60], correct taxonomic identification, geographical location, plant harvesting season, plant parts, and other indirect factors are crucial in phytochemical studies, which often receive little attention. Exogenous factors or environmental regulated factors such as light, precipitation, growing site and soil are often considered to be the most important factors modifying the qualitative/quantitative composition of EOs [61]. Experiments have shown that plants exposed to drought stress increased the concentration of monoterpenes to protect plant cells from ROS damage [62]. Meanwhile, Caser et al. [63] found that drought increased the production of sesquiterpenoids and decreased monoterpenoids. According to Paulsen and Selmar [64], increased terpene synthesis is not supported by carbon allocation theory, but is attributed to changes in biomass production. In addition, differences in the chemical profiles of EOs are often explained in the context of the interaction of the metabolic inversion of the ratio of oxygen-free to oxygen-containing terpenes with the surrounding environment. Sesquiterpenes have been observed to be predominate during the dry season, while higher concentrations of sesquiterpenoids were found during the wet season [65]. The water scarcity increased the production of monoterpenoids and monoterpenes, while the opposite trend was observed for sesquiterpenes [66]. On the other hand, Tsusaka et al. [67], investigating the influence of genetic and environmental factors on sesquiterpenoids in Atractylodes lancea, (Thunb.) DC. found that the genotype had a greater effect on EO compounds than the conditions of the plant cultivation year. The volatiles were stable despite the changing growing conditions, but the absolute values of terpenoids were induced by the site of cultivation. Tardugno et al. [68] determined that the composition of Thymus vulgaris L. essential oils were highly influenced by the cultivating techniques. Over time, local environment leads to differences in metabolomics and the formation of ecotypes and chemotypes within a species [69].
The intraspecific differences in Solidago spp. volatile compounds observed in the present study can be explained by genotypic differences, as the plants grew under close conditions. Sexual reproduction helps maintain a high level of genetic and phenotypic diversity in goldenrods. Our previous study showed a high morphological diversity in Solidago spp. both between populations and between individual genets [3]. Similarly, high variability in volatiles and morphological characters was observed in wild Mentha longifolia L. accessions growing in the same field [70]. According to Zhao et al. [71], high genetic variations are characteristic within invasive and native areas of S. canadensis populations. Considerations suggested that the study of local populations makes it possible to identify intraspecific diversity that potentially reflects local genetic changes rather than the controversial dependence of terpenes synthesis under changing environmental conditions. The outstanding diversity in the goldenrods studied allows the selection of accessions in terms of the desired composition of EO volatiles. Phytochemical profiling of plant raw materials is an informative tool to learn about their potential for further development of new natural products.

4. Material and Methods

4.1. Plant Material

Plant material of four Solidago spp. in the flowering phase was collected from six different sites in Vilnius district, Lithuania, in August 2018. Eighteen accessions of S. canadensis, seven of S. gigantea, nine of S. × niederederi, and three accessions of S. virgaurea were collected at least one kilometre apart from each other in abandoned dry grasslands and disturbed farmlands (Table 3). The vegetation of the collection sites was characterized as semi-ruderal dry grassland dominated by plant communities of Agropyretea intermedii-repentis and Artemisietea vulgaris. The EOs in habitats were sand or sandy loam, with low to moderate humus content (1.8–2.7%), rich in phosphorus (126–260 P2O5 mg kg−1) and potassium (146–205 K2O mg kg−1), pHKCl varied from 5.8 to 7.1.
The harvested plant material consisted of shoots of a single genet derived from a single seed. Individual genets were identified by phenological and morphological characteristics and by rhizome connections. The accessions of the same species were collected at least five meters apart from each other if more than one accession was collected from the same site. The plant material was dissected into inflorescences and leaves and dried separately at 25 °C. The botanical identification of species was based on morphological diagnostic characters such as the shape and size of inflorescences and ray flowers, stem color, and stem hairiness by Birutė Karpavičienė and Jolita Radušienė [3]. The specimens of evaluated Solidago spp. were deposited in the Herbarium of the Institute of Botany of Nature Research Centre (BILAS), Vilnius, Lithuania.

4.2. Isolation of Essential Oils

The plant material from 30 g of air-dried leaves and inflorescences was hydrodistilled separately for three hours using a Clevenger type apparatus. Each sample of yellowish EO was dried over anhydrous sodium sulphate and stored in a sealed vial at 4 °C until analysis. A sample preparation for chemical analysis included 1.0 μL of EO added into 1.0 mL of n-hexane following previous studies [23,33]. The essential oil content was calculated as relative percentages per 100 g of dry plant material.

4.3. Analysis of Essential Oils

The EOs analysis was performed using the GCMS-QP 2010 Ultra system equipped with a Shimazu autoinjector AOC-5000 (Shimadzu, Europa GmbH). A capillary column RXi-5MS (30 m × 0.25 mm i.d. × 0.25 film thickness µm) (Restek, Bellefonte, PA, USA) was used. The sample injection volume was 1 µL, a split ratio was 1:60 (v:v) and the split injector temperature was 260 °C. Helium was used as carrier gas with flow rate of 1.22 mL min−1. The initial column temperature was 50 °C, held for 5 min and raised to 200 °C at the rate of 2 °C min−1, then raised from 200 to 315 °C at the rate of 15 °C min−1 and held for 5 min. The detector ion source and interface temperatures were 200 °C and 280 °C, respectively. Mass spectra were acquired at an ionization voltage of 70 eV, a scan rate of 2500 m/z within the range of 29–500 m/z and a scan time of 0.2 s. The chromatographic analysis was run in triplicate.

4.4. Identification and Quantification of Components

The linear retention indices (LRI) of compounds were calculated using a homologous series of n-alkanes C8–C26 (Sigma-Aldrich, UK, purity >99.2%) injected at the beginning of the analysis and comparing the retention times of the eluted peaks with those of the alkanes [72]. Chromatographic data were analyzed using GC–MS solution software (Shimadzu, Europa GmbH). The EO constituents were identified by comparing the unique mass spectral fragmentation patterns of each peak with the mass spectral computer library database and those presented as standards in the NIST 14, FFNSC, WR10, and WR10R libraries, as well as comparing the obtained LRI with presented in NIST 14 datasets and reference [73] corresponding to the conditions for dimethylsilicone stationary phase with 5% phenyl groups. The relative percentages of analytes as the mean of the three runs were calculated from their peak areas in the chromatographic profiles without the use of correction factors corresponding to the conditions for the stationary phase of dimethylsilicone with 5% phenyl groups.
The repeatability and intermediate precision of analysis, expressed as relative standard deviation (RSD), was evaluated by performing the retention time and peak area values of five analytes in the same S. canadensis EO extract for intra- and inter- daily tests (Table 4).
Repeatability was determined in five consecutive injections of EO in the same day. The RSD for the retention time ranged from 0.22 to 0.32% and for relative peak area from 0.33 to 0.45%. Intermediate precision was assessed by five injections over two different days, with RSD values ranging from 0.54 to 0.92% for retention time and 0.98 to 2.21% for peak areas. The accuracy of the quantification was satisfactory, as RSD value within the 3% range is generally considered as acceptable.

4.5. Data Analysis

Multivariate statistical analysis was performed using software package Statistica 10.0 (StatSoft Inc.). The Kruskal–Wallis ANOVA was used to determine the differences between species. Significant differences were specified by two-tailed test at p ≤ 0.05. Principal component analysis (PCA) was used to identify the similarities and differences between the EOs analyzed using statistically independent variables. The PCA was based on 24 inflorescence and 16-leaf standardized variables that different significantly between species and that represented constituents detected in 30% or more of EO samples in at least one species. Leaf and inflorescence data sets were pooled and used in PCA, resulting in more convincing results than separate leaf and inflorescence PCAs.

5. Conclusions

The frequency and percentage of distribution in the volatile constituents of Solidago spp. varied depending on the species, accessions, and plant parts. The principal compounds common to all Solidago spp. inflorescence and leaf EOs were α- and β-pinene, limonene, bornyl acetate, germacrene D, spathulenol, and caryophyllene oxide. Solidago spp. differed significantly in some of the distinctive terpenes that can be considered as compounds with high potential for chemophenetic and taxonomic studies of the genus. A comparison of volatile profiles for Solidago spp. confirmed the interspecific origin of S. × niederederi between S. canadensis and S. virgaurea with a higher metabolic contribution of alien species than native ones. The findings provide the bioprospecting of Solidago spp. as a source for specified composition of volatiles. The vast resources of invasive goldenrods are of great interest as a convenient and readily acceptable, underutilized source of natural bioactive compounds that can be used for different applications.
The combination of fingerprint and multivariate data analysis demonstrated a simplified assessment of the quality of wild plant materials. Correct species identification is essential for the development of raw material quality control protocols for the targeted collection and assessment of raw materials from wild populations. The screening of a relatively large number of plant accessions from mixed populations of different species allows for a more reasonable comparison of their volatile profiles and enables prediction of the most likely quality of raw materials harvested from the wild.

Author Contributions

Conceptualization, J.R. and B.K.; methodology, L.R. and M.M., software, B.K.; validation, M.M. and L.I.; formal analysis, L.I. and M.M.; investigation, J.R., M.M. and B.K.; resources, L.I. and J.R.; data curation, M.M., J.R. and B.K.; writing—original draft preparation, J.R.; writing—review and editing, J.R. and L.R.; visualization, B.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

All data generated during this study are included in this article.

Acknowledgments

The authors thank to Open Access Centre for the Advanced Pharmaceutical and Health Technologies (Lithuanian University of Health Sciences) for providing the opportunity to use infrastructure for experiments.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Franz, C.M. Essential oil research: Past, present and future. Flavour. Fragr. J. 2010, 25, 112–113. [Google Scholar] [CrossRef]
  2. Weber, E. Current and potential ranges of three exotic goldenrods (Solidago) in Europe. Conserv. Biol. 2001, 15, 122–128. [Google Scholar] [CrossRef]
  3. Karpavičienė, B.; Radušienė, J. Morphological and anatomical characterization of Solidago × niederederi and other sympatric Solidago species. Weed Sci. 2016, 64, 61–70. [Google Scholar] [CrossRef]
  4. Chen, G.Q.; Zhang, C.-B.; Ma, L.; Qiang, S.; Silander, J.A.; Li, L.Q. Biotic homogenization caused by the invasion of Solidago canadensis in China. J. Integr. Agric. 2013, 12, 835–845. [Google Scholar] [CrossRef]
  5. Khek, E. Floristisches aus Ober-Oesterreich. Allg. Bot. Z Syst. 1905, 11, 21–23. [Google Scholar]
  6. Gudžinskas, Z.; Petrulaitis, L. New alien plant species recorded in the southern regions of Latvia. Bot. Lith. 2016, 22, 153–160. [Google Scholar] [CrossRef] [Green Version]
  7. Skokanová, K.; Šingliarová, B.; Španiel, S.; Hodálová, I.; Mereďa, P., Jr. Tracking the expanding distribution of Solidago × niederederi (Asteraceae) in Europe and first records from three countries within the Carpathian region. BioInvasions Rec. 2020, 9, 670–684. [Google Scholar] [CrossRef]
  8. Pal, R.W.; Chen, S.; Nagy, D.U.; Callaway, R.M. Impacts of Solidago gigantea on other species at home and away. Biol. Invasions 2015, 17, 3317–3325. [Google Scholar] [CrossRef]
  9. Yuan, Y.; Wang, B.; Zhang, S.; Tang, J.; Tu, C.; Hu, S.; Yong, J.W.H.; Chen, X. Enhanced allelopathy and competitive ability of invasive plant Solidago canadensis in its introduced range. J. Plant Ecol. 2013, 6, 253–263. [Google Scholar] [CrossRef] [Green Version]
  10. Świerszcz, S.; Szymura, M.; Wolski, K.; Szymuret, T.H. Comparison of methods for restoring meadows invaded by Solidago species. Pol. J. Environ. Stud. 2017, 26, 1251–1258. [Google Scholar] [CrossRef]
  11. Zihare, L.; Blumberga, D. Insight into bioeconomy. Solidago canadensis as a valid resource. Brief review. Energy Procedia 2017, 128, 275–280. [Google Scholar] [CrossRef]
  12. Ciesielczuk, T.; Poluszyńska, J.; Rosik-Dulewska, C.; Sporek, M.; Lenkiewicz, M. Uses of weeds as an economical alternative to processed wood biomass and fossil fuels. Ecol. Eng. 2016, 95, 485–491. [Google Scholar] [CrossRef]
  13. Staab, M.; Pereira-Peixoto, M.H.; Klein, A.-M. Exotic garden plants partly substitute for native plants as resources for pollinators when native plants become seasonally scarce. Oecologia 2020, 194, 465–480. [Google Scholar] [CrossRef] [PubMed]
  14. ESCOP Monographs. Solidaginis Virgaureae Herba (European Goldenrod). 2018. Available online: https://escop.com/downloads/solidaginis-virgaureae-herba-european-goldenrod (accessed on 10 February 2022).
  15. Final Community Herbal Monograph on Solidago virgaurea L., herba. (Doc. Ref. EMEA/HMPC/285758/2007) 2008. Available online: https://www.ema.europa.eu/en/documents/herbal-monograph/final-community-herbal-monograph-solidago-virgaurea-l-herba_en.pdf (accessed on 15 April 2022).
  16. Council of Europe. European Pharmacopoeia. Strasbourg: Council of Europe. 2001. Available online: https://pheur.edqm.eu/app/10-8/search/ (accessed on 15 April 2022).
  17. Demir, H.; Acik, L.; Bali, E.B.; Koc, Y.; Kaynak, G. Antioxidant and antimicrobial activities of Solidago virgaurea extracts. Afr. J. Biotechnol. 2009, 8, 274–279. [Google Scholar]
  18. Marksa, M.; Zymone, K.; Ivanauskas, L.; Radušienė, J.; Pukalskas, A.; Raudone, L. Antioxidant profiles of leaves and inflorescences of native, invasive and hybrid Solidago species. Ind. Crops Prod. 2020, 145, 112123. [Google Scholar] [CrossRef]
  19. Shelepova, O.; Vinogradova, Y.; Zaitchik, B.; Ruzhitsky, A.; Grygorieva, O.; Brindza, J. Constituents of the essential oil in Solidago canadensis L. from Eurasia. Potravin. Slovak J. Food Sci. 2018, 12, 20–25. [Google Scholar] [CrossRef] [Green Version]
  20. Radušiene, J.; Marksa, M.; Karpavičiene, B. Assessment of Solidago × niederederi origin based on the accumulation of phenolic compounds in plant raw materials. Weed Sci. 2018, 66, 324–330. [Google Scholar] [CrossRef]
  21. Liu, S.; Shao, X.; Wei, Y.; Li, Y.; Xu, F.; Wang, H. Solidago canadensis L. essential oil vapor effectively inhibits Botrytis cinerea growth and preserves postharvest quality of strawberry as a food model system. Front Microbiol. 2016, 7, 1179. [Google Scholar] [CrossRef]
  22. Werrie, P.-Y.; Durenne, B.; Delaplace, P.; Fauconnier, M.-L. Phytotoxicity of EOs: Opportunities and constraints for the development of biopesticides. A Review. Foods 2020, 9, 1291. [Google Scholar] [CrossRef]
  23. Elshafie, H.S.; Grul’ová, D.; Baranová, B.; Caputo, L.; De Martino, L.; Sedlák, V.; Camele, I.; De Feo, V. Antimicrobial activity and chemical composition of essential oil extracted from Solidago canadensis L. growing wild in Slovakia. Molecules 2019, 24, 1206. [Google Scholar] [CrossRef] [Green Version]
  24. Sarić-Krsmanović, M.; Gajić Umiljendić, J.; Radivojević, L.; Šantrić, L.; Potočnik, I.; Đurović-Pejčev, R. Bio-herbicidal effects of five EOs on germination and early seedling growth of velvetleaf (Abutilon theophrasti Medik.). J. Environ. Sci. Heal. Part B 2019, 54, 247–251. [Google Scholar] [CrossRef] [PubMed]
  25. Li, D.Q.; Pan, S.H.; Zhu, X.W.; Tan, L.; Cao, Y.F. Anticancer activity and chemical composition of leaf essential oil from Solidago canadensis L. in China. Adv. Mat. Res. 2012, 347, 1584–1589. [Google Scholar] [CrossRef]
  26. Wandjou, J.G.N.; Quassinti, L.; Gudžinskas, Z.; Nagy, D.U.; Cianfaglione, K.; Bramucci, M.; Maggi, F. Chemical composition and antiproliferative effect of EOs of four Solidago species (S. canadensis, S. gigantea, S. virgaurea and S. × niederederi). Chem. Biodivers. 2020, 17, e2000685. [Google Scholar] [CrossRef]
  27. Dhifi, W.; Bellili, S.; Jazi, S.; Bahloul, N.; Mnif, W. EOs’ chemical characterization and investigation of some biological activities: A critical review. Medicines 2016, 3, 25. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Perricone, M.; Arace, E.; Corbo, M.R.; Sinigaglia, M.; Bevilacqua, A. Bioactivity of EOs: A review on their interaction with food components. Front. Microbiol. 2015, 6, 76. [Google Scholar] [CrossRef] [Green Version]
  29. Benelli, G.; Pavela, R.; Cianfaglione, K.; Nagy, D.U.; Canale, A.; Maggi, F. Evaluation of two invasive plant invaders in Europe (Solidago canadensis and Solidago gigantea) as possible sources of botanical insecticides. J. Pest Sci. 2019, 92, 805–821. [Google Scholar] [CrossRef]
  30. Kalemba, D. Constituents of the essential oil of Solidago virgaurea L. Flavour Fragr. J. 1998, 13, 373–376. [Google Scholar] [CrossRef]
  31. Kalemba, D.; Marschall, H.; Bradesi, P. Constituents of the essential oil of Solidago gigantea Ait. (giant goldenrod). Flavour Fragr. J. 2001, 16, 19–26. [Google Scholar] [CrossRef]
  32. Kalemba, D.; Thiem, B. Constituents of the EOs of four micropropagated Solidago species. Flavour Fragr. J. 2004, 19, 40–43. [Google Scholar] [CrossRef]
  33. Kołodziej, B.; Kowalski, R.; Kędzia, B. Antibacterial and antimutagenic activity of extracts above ground parts of three Solidago species: Solidago virgaurea L. Solidago canadensis L. and Solidago gigantea Ait. J. Med. Plant Res. 2011, 5, 6770–6779. [Google Scholar] [CrossRef]
  34. Gruľová, D.; Baranová, B.; Ivanova, V.; De Martino, L.; Mancini, E.; De Feo, V. Composition and bio activity of EOs of Solidago spp. and their impact on radish and garden cress. Allelopath. J. 2016, 39, 129–142. [Google Scholar]
  35. Huang, B.K.; Lei, Y.L.; Qin, L.P.; Liu, J. Chemical composition and cytotoxic activities of the essential oil from inflorescences of Solidago canadensis L., an invasive weed in Southeastern China. J. Essent. Oil-Bear. Plants 2012, 15, 667–671. [Google Scholar] [CrossRef]
  36. Lawson, S.K.; Sharp, L.G.; Powers, C.N.; McFeeters, R.L.; Satyal, P.; Setzer, W.N. Volatile compositions and antifungal activities of native American medicinal plants: Focus on the Asteraceae. Plants 2020, 9, 126. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. El-Sherei, M.; Khaleel, A.; Motaal, A.A.; Abd-Elbaki, P. Effect of seasonal variation on the composition of the essential oil of Solidago canadensis cultivated in Egypt. J. Essent. Oil-BearPlants 2014, 17, 891–898. [Google Scholar] [CrossRef]
  38. Semple, J.C. An intuitive phylogeny and summary of chromosome number variation in the goldenrod genus Solidago (Asteraceae: Astereae). Phytoneuron 2016, 32, 1–9. [Google Scholar]
  39. Macel, M.; de Vos, R.C.H.; Jeroen, J.J.; van der Putten, W.H.; van Dam, N.M. Novel chemistry of invasive plants: Exotic species have more unique metabolomic profiles than native congeners. Ecol. Evol. 2014, 4, 2777–2786. [Google Scholar] [CrossRef]
  40. Synowiec, A.; Kalemba, D.; Drozdek, E.; Bocianowski, J. Phytotoxic potential of EOs from temperate climate plants against the germination of selected weeds and crops. J. Pest Sci. 2017, 90, 407–419. [Google Scholar] [CrossRef]
  41. Baser, K.H.C. Biological and pharmacological activities of carvacrol and carvacrol bearing essential oils. Curr. Pharm. Des. 2008, 14, 3106–3119. [Google Scholar] [CrossRef]
  42. Mastelić, J.; Jerković, I.; Blažević, I.; Poljak-Blaži, M.; Borović, S.; Ivanćić-Baće, I.; Smrećki, V.; Žarković, N.; Brćić-Kostic, K.; Vikić-Topić, D.; et al. Comparative study on the antioxidant and biological activities of carvacrol, thymol, and eugenol derivatives. J. Agric. Food Chem. 2008, 56, 3989–3996. [Google Scholar] [CrossRef]
  43. Orians, C.M. The effects of hybridization in plants on secondary chemistry: Implications for the ecology and evolution of plant—Herbivore interactions. Am. J. Bot. 2001, 87, 1749–1756. [Google Scholar] [CrossRef] [Green Version]
  44. Schierenbeck, K.A.; Ellstrand, N.C. Hybridization and the evolution of invasiveness in plants and other organisms. Biol. Invasions 2009, 11, 1093–1105. [Google Scholar] [CrossRef]
  45. López-Caamal, A.; Tovar-Sánchez, E. Genetic, morphological, and chemical patterns of plant hybridization. Rev. Chil. Hist. Nat. 2014, 87, 16. [Google Scholar] [CrossRef] [Green Version]
  46. Chizzola, R. Regular monoterpenes and sesquiterpenes (EOs). In Natural Products; Ramawat, K., Mérillon, J.M., Eds.; Springer: Berlin/Heidelberg, Germany, 2013; pp. 2973–3008. [Google Scholar] [CrossRef]
  47. Verdeguer, M.; Sánchez-Moreiras, A.M.; Araniti, F. Phytotoxic effects and mechanism of action of EOs and terpenoids. Plants 2020, 9, 1571. [Google Scholar] [CrossRef] [PubMed]
  48. Rolli, E.; Marieschi, M.; Maietti, S.; Sacchetti, G.; Bruni, R. Comparative phytotoxicity of 25 EOs on pre-and postemergence development of Solanum lycopersicum L.: A multivariate approach. Ind. Crops Prod. 2014, 60, 280–290. [Google Scholar] [CrossRef]
  49. Azizan, K.A.; Ghani, N.H.A.; Nawawi, M.F. Discrimination and prediction of the chemical composition and the phytotoxic activity of Wedelia trilobata essential oil (EO) using metabolomics and chemometrics. Plant Biosyst. 2020, 1–16. [Google Scholar] [CrossRef]
  50. Mutlu, S.; Atici, Ö.; Esim, N. Bioherbicidal effects of essential oils of Nepeta meyeri Benth. on weed spp. Allelopath. J. 2010, 26, 291–300. [Google Scholar]
  51. Verdeguer, M.; Blázquez, M.A.; Boira, H. Phytotoxic effects of Lantana camara, Eucalyptus camaldulensis and Eriocephalus africanus essential oils in weeds of Mediterranean summer crops. Biochem. Syst. Ecol. 2009, 37, 362–369. [Google Scholar] [CrossRef]
  52. Vasilakoglou, I.; Dhima, K.; Paschalidis, K.; Ritzoulis, C. Herbicidal potential on Lolium rigidum of nineteen major essential oil components and their synergy. J. Essent. Oil Res. 2013, 25, 1–10. [Google Scholar] [CrossRef]
  53. Benelli, G.; Pavela, R.; Drenaggi, E.; Desneux, N.; Maggi, F. Phytol, (E)-nerolidol and spathulenol from Stevia rebaudiana leaf essential oil as effective and eco-friendly botanical insecticides against Metopolophium dirhodum. Ind. Crops Prod. 2020, 155, 12844. [Google Scholar] [CrossRef]
  54. Landi, M.; Misra, B.B.; Muto, A.; Bruno, L.; Araniti, F. Phytotoxicity, morphological, and metabolic effects of the sesquiterpenoid nerolidol on Arabidopsis thaliana seedling roots. Plants 2020, 9, 1347. [Google Scholar] [CrossRef]
  55. Sen, A.; Kurkcuoglu, M.; Yildirim, A.; Senkardes, I.; Bitis, L.; Baser, K.H.C. Chemical composition, antiradical, and enzyme inhibitory potential of essential oil obtained from aerial part of Centaurea pterocaula Trautv. J. Ess. Oil. Res. 2021, 33, 44–52. [Google Scholar] [CrossRef]
  56. Albouchi, F.; Ghazouani, N.; Souissi, R.; Abderrabba, M.; Boukhris-Bouhachem, S. Aphidicidal activities of Melaleuca styphelioides Sm. essential oils on three citrus aphids: Aphis gossypii Glover; Aphis spiraecola Patch and Myzus persicae (Sulzer). S. Afr. J. Bot. 2018, 117, 149–154. [Google Scholar] [CrossRef]
  57. Boulogne, I.; Petit, P.; Ozier-Lafontaine, H.; Desfontaines, L.; Loranger-Merciris, G. Insecticidal and antifungal chemicals produced by plants: A review. Environ. Chem. Lett. 2012, 10, 325–347. [Google Scholar] [CrossRef] [Green Version]
  58. Nararak, J.; Sathantriphop, S.; Kongmee, M.; Mahiou-Leddet, V.; Ollivier, E.; Manguin, S.; Chareonviriyaphap, T. Excito-repellent activity of β-caryophyllene oxide against Aedes aegypti and Anopheles minimus. Acta Trop. 2019, 197, 105030. [Google Scholar] [CrossRef] [PubMed]
  59. Abd-ElGawad, A.M.; El Gendy, A.E.-N.G.; Assaeed, A.M.; Al-Rowaily, S.L.; Alharthi, A.S.; Mohamed, T.A.; Nassar, M.I.; Dewir, Y.H.; Elshamy, A.I. Phytotoxic effects of plant essential oils: A systematic review and structure-activity relationship based on chemometric analyses. Plants 2021, 10, 36. [Google Scholar] [CrossRef] [PubMed]
  60. Zidorn, C. Guidelines for consistent characterisation and documentation of plant source materials for studies in phytochemistry and phytopharmacology. Phytochemistry 2017, 139, 56–59. [Google Scholar] [CrossRef]
  61. Barra, A. Factors affecting chemical variability of essential oils: A review of recent developments. Nat. Prod. Commun. 2009, 4, 1147–1154. [Google Scholar] [CrossRef] [Green Version]
  62. Nowak, M.; Kleinwächter, M.; Manderscheid, R.; Weige, H.J.; Selmar, D. Drought stress increases the accumulation of monoterpenes in sage (Salvia officinalis), an effect that is compensated by elevated carbon dioxide concentration. J. Appl. Bot. Food Qual. 2010, 83, 133–136. Available online: https://ojs.openagrar.de/index.php/JABFQ/article/view/2138 (accessed on 15 April 2022).
  63. Caser, M.; Chitarra, W.; D’Angiolillo, F.; Perrone, I.; Demasi, S.; Lovisolo, C.; Pistelli, L.; Pistelli, L.; Scariot, V. Drought stress adaptation modulates plant secondary metabolite production in Salvia dolomitica Codd. Ind. Crops Prod. 2019, 129, 85–96. [Google Scholar] [CrossRef]
  64. Paulsen, J.; Selmar, D. Case study: The difficulty of correct reference values when evaluating the effects of drought stress: A case study with Thymus vulgaris. J. Appl. Bot. Food Qual. 2016, 89, 287–289. [Google Scholar]
  65. De Almeida, L.F.R.; Portella, R.O.; Facanali, R.R.; Marques, M.O.M.; Frei, F. Dry and wet seasons set the phytochemical profile of the Copaifera langsdorffii Desf. EOs. J. Essent. Oil. Res. 2016, 26, 292–300. [Google Scholar] [CrossRef]
  66. Ribeiro, A.F.; Andrade, E.H.A.; Salimena, F.R.G.; Maia, J.G.S. Circadian and seasonal study of the cinnamate chemotype from Lippia origanoides Kunth. Biochem. Syst. Ecol. 2014, 55, 249–259. [Google Scholar] [CrossRef]
  67. Tsusaka, T.; Makino, B.; Ohsawa, R.; Ezura, H. Genetic and environmental factors influencing the contents of essential oil compounds in Atractylodes lancea. PLoS ONE 2019, 14, e0217522. [Google Scholar] [CrossRef] [PubMed]
  68. Tardugno, R.; Serio, A.; Purgatorio, C.; Savini, V.; Paparella, A.; Benvenuti, S. Thymus vulgaris L. essential oils from Emilia Romagna Apennines (Italy): Phytochemical composition and antimicrobial activity on food-borne pathogens. Nat. Prod. Res. 2022, 36, 837–842. [Google Scholar] [CrossRef] [PubMed]
  69. Padilla-González, G.F.; Frey, M.; Gómez-Zeledón, J.; Da Costa, F.B.; Spring, O. Metabolomic and gene expression approaches reveal the developmental and environmental regulation of the secondary metabolism of yacón (Smallanthus sonchifolius, Asteraceae). Sci. Rep. 2019, 9, 13178. [Google Scholar] [CrossRef] [PubMed]
  70. Moshrefi Araghi, A.; Nemati, H.; Azizi, M.; Moshtaghi, N.; Shoor, M.; Hadian, J. Assessment of phytochemical and agro-morphological variability among different wild accessions of Mentha longifolia L. cultivated in field condition. Ind. Crop. Prod. 2019, 140, 111698. [Google Scholar] [CrossRef]
  71. Zhao, S.Y.; Sun, S.G.; Dai, C.; Gituru, R.W.; Chen, J.M.; Wang, Q.F. Genetic variation and structure in native and invasive Solidago canadensis populations. Weed Res. 2014, 55, 163–172. [Google Scholar] [CrossRef]
  72. Wei, X.; Koo, I.; Kim, S.; Zhang, X. Compound identification in GC–MS by simultaneously evaluating the mass spectrum and retention index. Analyst 2014, 139, 2507–2514. [Google Scholar] [CrossRef] [Green Version]
  73. Babushok, V.I.; Linstrom, P.J.; Zenkevich, I.G. Retention indices for frequently reported compounds of plant essential oils. J. Phys. Chem. Ref. 2011, 40, 043101. [Google Scholar] [CrossRef] [Green Version]
Plants 11 01159 g001 550
Figure 1. Examples of fingerprint profiles for S. × niederederi, S. virgaurea, S. canadensis, and S. gigantea inflorescence EOs performed by GC–MS using the GC–MS-QP2010 Ultra Gas system. The peak numbers correspond to the number of EO compounds listed in the Table 1.
Figure 1. Examples of fingerprint profiles for S. × niederederi, S. virgaurea, S. canadensis, and S. gigantea inflorescence EOs performed by GC–MS using the GC–MS-QP2010 Ultra Gas system. The peak numbers correspond to the number of EO compounds listed in the Table 1.
Plants 11 01159 g001
Plants 11 01159 g002 550
Figure 2. PCA model representing the accumulation of terpenes in inflorescences and leaves of four Solidago species: (a) loading plot of the variables contributing to PC1 and PC2; (b) scores plot for the tested EOs with a 95% ellipses confidence limit for each species. The numbers of the variables correspond to the numbers of EO compounds listed in the Table 1 and Table 2. Inflorescence variable numbers were marked in brown; leaf variable numbers were marked in green.
Figure 2. PCA model representing the accumulation of terpenes in inflorescences and leaves of four Solidago species: (a) loading plot of the variables contributing to PC1 and PC2; (b) scores plot for the tested EOs with a 95% ellipses confidence limit for each species. The numbers of the variables correspond to the numbers of EO compounds listed in the Table 1 and Table 2. Inflorescence variable numbers were marked in brown; leaf variable numbers were marked in green.
Plants 11 01159 g002
Table
Table 1. The frequency of distribution (F, %) of the compounds detected in more than 30% of the inflorescence EO samples in at least one of the four Solidago species; their mean relative percentage (M) with SD and significance (p) of interspecies differences according to the Kruskal–Wallis two-tailed test.
Table 1. The frequency of distribution (F, %) of the compounds detected in more than 30% of the inflorescence EO samples in at least one of the four Solidago species; their mean relative percentage (M) with SD and significance (p) of interspecies differences according to the Kruskal–Wallis two-tailed test.
NoCompoundsLRI Exp.LRI Ref.S. gigantea (n = 7)S. canadensis (n = 18)S. × niederederi (n = 9)S. virgaurea (n = 3)p
FMSDFMSDFMSDFMSD
1α-pinene93093010010.78.3110018.113.8410017.412.8410028.68.960.196
2camphene94594871.41.80.7772.21.70.6977.81.20.341001.00.350.713
3thuja-2,4(10)-diene95095728.60.60.3566.70.50.1644.40.70.3266.70.60.130.504
4sabinene97197671.42.52.0766.71.10.7966.71.31.7933.30.6–0.258
5β-pinene97498071.43.00.9083.32.31.4088.92.21.711003.61.510.536
6β-myrcene99299142.91.60.3455.60.80.6033.30.60.1566.71.50.230.564
7p-cymene1018101442.92.51.425.60.5–00–00–0.021
8o-cymene10221009–107642.910.96.5755.60.50.4233.30.50.3000–0.338
9limonene10231027071.41.10.191005.24.4888.95.85.051001.10.570.032
10linalool1090109800–16.70.10.0744.40.50.1033.30.8–0.105
111α-campholenal1109110585.71.3 a0.581004.1 b1.451003.6 b1.6166.73.11.350.004
12trans-pinocarveol113511391000.8 a0.2088.92.9 b1.181003.0 b1.281001.60.930.005
13trans-sabinol1139114042.90.30.1600–00–00–0.004
14trans-verbenol114311441002.9 a1.1210013.1 b5.3910013.6 b5.791006.63.430.001
15cis-verbenol114511421000.5 a0.271001.9 b0.881001.8 b0.8866.71.20.230.001
16pinocarvone1158116085.70.4 a0.041001.6 b0.5088.91.8 b0.6266.71.40.340.003
17p-mentha-1,5-dien-8-ol1164116600–5.60.40.3144.40.70.3900–0.016
18α-phellandrene-8-ol1165116600 a–77.80.9 b0.3200 a–00–<0.001
19terpinen-4-ol1174117542.91.00.5116.70.30.0322.20.40.0600–0.241
20myrtenal1192119385.70.5 a0.131001.9 b0.6388.91.7 b0.5766.71.20.240.001
21myrtenol1193119485.70.7 a0.351001.5 b0.6388.91.30.5433.31.1–0.014
22verbenone1205120542.90.4 a0.291002.7 b1.191002.7 b1.381001.20.67<0.001
23trans-carveol1219121514.30.6 a–94.41.9 b0.6988.91.60.6033.30.8–<0.003
24carvone1241124200 a–94.41.3 b0.1877.81.10.5200–<0.001
25bornyl acetate1287128510010.44.8910011.94.741009.35.731004.12.810.098
26α-cubebene1347134500–00 a–00–1001.0 b0.40<0.001
27α-copaene1372137600–11.10.2 a0.0100–1002.6 b1.34<0.001
28β-cubebene1380138900 a–77.84.9 b3.2111.16.0 a0.0400–<0.001
29β-elemene1389139142.90.30.0855.60.80.4655.60.70.2800–0.243
30(E)-β-caryophyllene1414141971.40.90.3188.90.60.1644.40.80.4466.70.70.040.425
31β-copaene1424143214.30.4–22.20.2 a0.1333.33.63.8010012.28.150.006
32α-humulene1448145242.90.40.0438.90.20.2122.21.31.3400–0.588
33γ-muurolene147514771000.8 a0.2300 b–00 b–33.30.7–<0.001
34germacrene D1480148010011.2 a4.8022.28.1 b4.2188.92.51.651001.50.20<0.001
35β-selinene1481148657.10.40.0116.70.30.0822.20.70.0100–0.155
36epi-cubebol1489149314.30.7–00–11.11.0–66.71.61.240.007
37α-muurolene1499149928.60.40.0300 a–22.21.10.161001.4 b0.78<0.001
38γ-cadinene1507151385.70.7 a0.2616.70.4 b0.0900 b–00–<0.001
39cubebol1514151500–00 a–22.21.50.041002.8 b2.08<0.001
40δ-cadinene1520152414.30.5–00 a–22.21.10.161001.3 b0.90<0.001
41epoxyazulene1561155471.46.42.9855.61.91.2288.91.61.3500–0.054
42(E)-nerolidol1565156471.40.70.2811.10.40.1311.10.4–00–0.002
43spathulenol157515761005.0 a2.9738.90.9 b0.7466.72.83.961001.30.20<0.001
44caryophyllene oxide157815811003.62.441003.62.171008.48.261008.52.480.083
45viridiflorol1586159000–00–00–33.31.2–0.010
46humulene epoxide II1607160600–00 a–77.84.5 b8.6000–<0.001
47isospathulenol162716301006.1 a6.4783.32.31.5266.72.10.7333.31.3 b–0.018
Monoterpene hydrocarbons 10025.416.5210028.020.8810026.418.0910035.911.860.608
Oxygenated monoterpenes 10018.5 a6.0410046.6 b15.4210041.5 b16.3510019.27.60<0.001
Sesquiterpene hydrocarbons 10015.3 b6.631007.96.001006.04.8510020.7 a10.640.007
Oxygenated sesquiterpenes 10019.7 a8.851007.1 b3.4810017.015.5410014.75.25<0.001
Oxygenated diterpenes 14.30.1–11.10.90.1922.21.00.5100–0.479
1 Compounds in bold were included in the PCA. Compounds are listed in order of their linear retention indices (LRI exp.) calculated using homologous series of n-alkanes (C8–C26). LRI ref.—linear retention indices from NIST 14 data basis and reference. The mean values of the compounds marked with the letters (a, b) differ significantly at p ≤ 0.05 between species according to the Kruskal–Wallis test. n—number of distilled accessions per species.
Table
Table 2. The frequency of distribution (F, %) of the compounds detected in more than 30% of the leaf EO samples in at least one of the four Solidago species; their mean relative percentage (M) with SD and significance (p) of interspecies differences according to the Kruskal–Wallis two-tailed test.
Table 2. The frequency of distribution (F, %) of the compounds detected in more than 30% of the leaf EO samples in at least one of the four Solidago species; their mean relative percentage (M) with SD and significance (p) of interspecies differences according to the Kruskal–Wallis two-tailed test.
NoCompoundsa LRI Exp.b LRI Ref.S. gigantea (n = 7)S. canadensis (n = 18)S. × niederederi (n = 9)S. virgaurea (n = 3)p
FMSDFMSDFMSDFM SD
1α-pinene9309301007.82.181008.65.6910011.910.3710016.011.770.856
21 camphene9459481002.8 a0.761001.2 b0.4077.81.1 b0.4566.70.5 b0.07<0.001
3thuja-2,4(10)-diene95095700–11.10.20.1333.30.60.1333.30.3–0.187
4sabinene97197642.91.10.6144.40.60.4233.31.11.2166.70.30.010.926
5β-pinene9749801002.2 0.8894.41.4 0.6188.91.91.1666.73.50.640.193
6β-myrcene99298828.61.20.125.61.0–22.20.80.4933.30.4–0.372
7o-cymene10221009–10761002.1 a1.4050.00.5 b0.4622.20.4 b0.0600 b–<0.001
8limonene102310271001.1 a0.161002.5 b2.171002.21.5666.71.10.350.006
9α-campholenal1109110514.30.6 a–77.80.8 0.7277.82.6 1.681002.8 b0.520.007
10trans-pinocarveol1135113942.90.3 a0.1666.70.9 a0.5077.81.6 0.751003.6 b1.830.003
11trans-verbenol1143114442.90.5 a0.231002.7 b1.811008.9 b6.8510024.6 b21.21<0.001
12cis-verbenol1145114200 a–27.80.4 0.2744.41.6 0.391001.5 b0.820.004
13pinocarvone1158116000 a–22.20.6 a0.3166.71.1 0.511001.8 b0.04<0.001
14myrtenal1192119300 –72.20.6 0.2955.61.6 0.4866.71.6 0.020.024
15myrtenol1193119400 –55.60.3 0.2555.61.0 0.3366.71.2 0.030.038
16verbenone1205120642.90.3 a0.1688.91.5 1.3577.85.2 b6.771007.3 b8.370.008
17cis-carveol1208120600–5.61.1–00–33.30.7–0.168
18trans-carveol1219121500 –16.70.2 0.0744.40.90.2133.30.8–0.066
19bornyl acetate1287128510022.4 a5.3710018.7 a7.5510014.0 5.531002.6 b0.460.004
20thymol1295129700–5.60.5–11.19.5–33.33.8–0.330
21carvacrol1306130800–11.123.30.6311.16.4–66.73.2 0.420.079
22α-copaene1372137600 –22.20.30.0900 –66.70.50.030.059
23β-bourbonene1378138585.70.90.4550.00.5 0.4622.22.02.2733.31.8–0.056
24β-cubebene1380138957.114.18.4138.921.310.2522.220.15.2500–0.467
25β-elemene1389139128.60.8 a0.0483.31.7 b1.4566.70.8 0.5733.30.4 –0.005
26(E)-β-caryophyllene1414141985.71.00.2761.12.52.1466.72.01.6766.71.51.420.985
27β-copaene1424143214.30.5–50.00.60.1922.23.84.5666.73.20.790.161
28α-humulene1448145242.90.50.0861.10.80.5433.31.91.8933.30.4–0.380
29γ-muurolene147514771000.8 a0.2300 b–00 b–33.30.7 –<0.001
30germacrene D1480148042.95.95.9550.019.615.2266.78.85.2266.75.26.460.751
31β-selinene1481148614.30.6–38.90.50.4700 –00–0.103
32epi-cubebol1489149300 –00 –00–66.71.4 0.310.012
33α-muurolene1499149900–00–00–33.30.3–0.222
34β-bisabolene1505150900–11.15.01.0511.14.7–33.31.8–0.569
35γ-cadinene150715131001.0 0.325.60.7 –00–00 –<0.001
36cubebol1514151500–00 –00 –66.70.7 0.100.014
37δ-cadinene1520152400–5.60.7 –11.10.9–33.30.4–0.384
38epoxyazulene156115541006.1 a3.221002.7 1.4366.72.9 b2.4933.30.3 b–0.001
39(E)-nerolidol1565156485.70.9 a0.2038.90.6 0.2000 b–00 –0.001
40spathulenol157515761006.7 a6.2588.91.2 b0.9866.72.1 b1.941003.1 1.300.003
41caryophyllene oxide157815811003.1 a0.7777.83.9 a2.2410010.4 b11.181009.06.360.004
42humulene epoxide II1607160657.12.41.2638.92.71.0422.23.20.9266.75.01.440.276
43isospathulenol162716301006.3 a3.111004.8 a2.5466.73.7 2.2600 b–0.004
Monoterpene hydrocarbons 10016.64.0810014.49.4210017.710.9210020.115.280.634
Oxygenated monoterpenes 10023.15.6410027.911.210035.713.0710049.0 27.810.072
Sesquiterpene hydrocarbons 10014.97.8594.423.315.310015.011.3266.78.610.930.252
Oxygenated sesquiterpenes 10023.310.0310013.3 6.0710016.912.5610016.97.630.181
Oxygenated diterpenes 00–5.60.70.2611.10.10.3300–0.375
1 Compounds in bold were included in the PCA. Compounds are listed in order of their linear retention indices (LRI exp.) calculated using homologous series of n-alkanes (C8–C26). LRI ref.—linear retention indices from NIST 14 data basis and reference. The mean values of the compounds marked with the letters (a, b) differ significantly at p ≤ 0.05 between species according to the Kruskal–Wallis test. n—number of distilled accessions per species.
Table
Table 3. Collection sites data on Solidago gigantea (SG), S. canadensis (SC), S. × niederederi (SN), and S. virgaurea (SV).
Table 3. Collection sites data on Solidago gigantea (SG), S. canadensis (SC), S. × niederederi (SN), and S. virgaurea (SV).
Collection SiteAltitude, mLatitude NLongitude ENumber of Accessions
SGSCSNSV
Pavilnys, Vilnius distr.21554°40′35″25°23′01″331–
Didieji Pupojai, Vilnius20654°42′38″25°23′29″1332
Rokantiškės, Vilnius20354°40′03″25°22′58″321–
Raudondvaris, Vilnius distr.14954°52′32″25°31′08″–4––
Dvariškės, Vilnius distr.14954°49′17″25°16′23″–331
Karklinė, Vilnius distr.16454°54′26″25°33′40″–31–
Table
Table 4. Repeatability and intermediate precision on the relative retention time (tR,) and peak area (A) of the five analytes in S. canadensis EOs expressed as relative standard deviation (RSD, %).
Table 4. Repeatability and intermediate precision on the relative retention time (tR,) and peak area (A) of the five analytes in S. canadensis EOs expressed as relative standard deviation (RSD, %).
AnalytesRepeatability (Run-to-Run)Intermediate Precision (Day-to-Day)
tR, minRSD, %A, %RSD, %tR, minRSD, %A, %RSD, %
α-pinene11.850.2324.570.4511.920.8224.831.51
limonene15.240.299.070.3315.310.739.171.42
trans-verbenol23.200.2210.360.4123.360.9210.542.21
bornyl acetate32.700.3210.210.4332.770.5410.260.98
β-cubebene44.590.262.820.3844.740.602.841.02
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Radušienė, J.; Karpavičienė, B.; Marksa, M.; Ivanauskas, L.; Raudonė, L. Distribution Patterns of Essential Oil Terpenes in Native and Invasive Solidago Species and Their Comparative Assessment. Plants 2022, 11, 1159. https://doi.org/10.3390/plants11091159

AMA Style

Radušienė J, Karpavičienė B, Marksa M, Ivanauskas L, Raudonė L. Distribution Patterns of Essential Oil Terpenes in Native and Invasive Solidago Species and Their Comparative Assessment. Plants. 2022; 11(9):1159. https://doi.org/10.3390/plants11091159

Chicago/Turabian Style

Radušienė, Jolita, Birutė Karpavičienė, Mindaugas Marksa, Liudas Ivanauskas, and Lina Raudonė. 2022. "Distribution Patterns of Essential Oil Terpenes in Native and Invasive Solidago Species and Their Comparative Assessment" Plants 11, no. 9: 1159. https://doi.org/10.3390/plants11091159

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop