# Biocidal, Antioxidant, and Anti-Inflammatory Activities of Essential Oils Extracted from Angelica spp. Cultivated on Contaminated Soils

Julien Langrand, Joël Fontaine, Anthony Verdin, Frédéric Laruelle, Natacha

Facon, Sophie Fourmentin, Anissa Lounès - Hadj Sahraoui

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## ► To cite this version:

Julien Langrand, Joël Fontaine, Anthony Verdin, Frédéric Laruelle, Natacha Facon, et al.. Biocidal, Antioxidant, and Anti-Inflammatory Activities of Essential Oils Extracted from Angelica spp. Cultivated on Contaminated Soils. Scientific Reports, 2026, 16, pp.2695. 10.1038/s41598-025-32550-5. hal-05468901

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# Biocidal, antioxidant, and anti-inflammatory activities of essential oils extracted from *Angelica* spp. cultivated on contaminated soils

Julien Langrand, Joël Fontaine, Anthony Verdin, Frédéric Laruelle, Natacha Facon, Sophie Fourmentin & Anissa Lounès - Hadj Sahraoui*

This study investigated the phytochemical profile and biological activities of the essential oil (EO) distilled from *Angelica archangelica* L. seeds grown on trace element (TE)-polluted soil, within a phytomanagement context. The effects of soil pollution and mycorrhizal inoculation on EO composition and its antifungal, herbicidal, antioxidant, and anti-inflammatory properties were assessed. The chemical composition of the EO, predominantly β-phellandrene, α-pinene, α-phellandrene, and β-myrcene, remained stable regardless of mycorrhizal inoculation. While antioxidant activity was moderate, the EO exhibited promising anti-inflammatory potential compared to other EO, suggesting its application in health-related products. Furthermore, the EO demonstrated antifungal activity, notably against *Zymoseptoria tritici* (IC₅₀: 21 mg.L⁻¹), a major wheat pathogen, and inhibited *Fusarium culmorum*, *Fusarium graminearum* and the oomycete *Phytophthora infestans* growth. It also reduced wheat infection by *Blumeria graminis* (responsible for powdery mildew) by 40%. Additionally, the EO showed herbicidal effects on ryegrass (IC₅₀: 144 mg.L⁻¹), indicating its potential as a natural pesticide alternative. Overall, *A. archangelica* EO produced on TE-polluted soils retains desirable chemical and biological activities, supporting its potential for various non-food applications.

**Keywords** *Angelica*, Essential oil, Trace elements, Polluted soils, Biological activities

Essential oils (EO) are complex mixtures of volatile compounds, primarily terpenes, alcohols, acids, esters, aldehydes, ketones, amines, and sulfides, with diverse chemical and biological properties¹⁻³. These compounds are increasingly studied for their antimicrobial, fungicidal, insecticidal, antioxidant and anti-inflammatory, activities⁴⁻⁶. By scavenging free radicals, EO can protect foods from oxidative damage⁷ and contribute to the prevention of diseases such as cancer, cardiovascular disorders, and immune system decline⁸,⁹.

Beyond human health, EO offer promising applications in agriculture as biopesticides. They are considered environmentally friendly due to their low toxicity to humans and animals and are classified as “generally recognized as safe” by the FDA¹⁰,¹¹. EO have also demonstrated effectiveness against plant pathogens, weeds, and pests, and enjoy public support as natural alternatives to synthetic phytopharmaceuticals¹²⁻¹⁴. For instance, clove, spearmint, and sweet orange EO are authorized in France as fungicides, antigerminatives, and insecticides, respectively¹⁵.

The global demand for EO is growing rapidly, increasing pressure on arable land¹⁶. In this context, cultivating aromatic plants on polluted soils unsuitable for food production represents a promising phytomanagement strategy, allowing the valorization of high-value EO while avoiding competition with food crops¹⁷,¹⁸.

Indeed, trace element (TE) contamination is widespread, affecting nearly half of over 10 million polluted sites globally¹⁹. TE accumulation poses risks to ecosystems and human health due to their toxicity and persistence²⁰,²¹. Aromatic plants capable of tolerating and immobilizing TEs at the rhizosphere could be exploited to produce safe, high-value EO from contaminated soils, enhancing the economic viability of phytotechnologies²¹⁻²³.

EO composition is strongly influenced by environmental factors, including soil type, climate, and also pollutants²⁴. TE contamination can alter both yield and chemical profile of EO²⁵⁻²⁷. Arbuscular mycorrhizal fungi (AMF) inoculation has already been reported to mitigate negative effects of soil pollutants and even enhance EO yield and specific bioactive compounds in aromatic plants²⁸⁻³¹. For example, AMF increased sesquiterpene acids in valerian roots and eugenol content in basil leaves³²,³³.

Unité de Chimie Environnementale et Interactions sur le Vivant (UCEIV, UR 4492), Université du Littoral Côte d'Opale, 50 rue Ferdinand Buisson, Calais Cedex 62228, France. *✉*email: anissa.lounes@univ-littoral.fr
Among EO-producing aromatic plants, *Angelica archangelica* (Apiaceae) is widely distributed across Europe, Asia, and North America and is traditionally used for its antioxidant and anti-inflammatory properties³⁴,³⁵. Previous studies reported antifungal and herbicidal activities of *A. archangelica* extracts³⁶,³⁷, highlighting its potential as a natural alternative to synthetic pesticides, particularly in the context of increasing pest resistance³⁸,³⁹.

While EO production on polluted soils has been suggested as a sustainable strategy, comprehensive studies evaluating the combined effects of TE soil contamination and AMF inoculation on EO yield, composition, and biological activities are limited. Specifically, there is a lack of knowledge concerning *A. archangelica* EO produced under TE pollution and its potential applications in agriculture and medicine. The present study investigates the impact of TE-polluted soils and mycorrhizal inoculation on the chemical composition of *A. archangelica* seed EO, distilled from plants cultivated *in situ*. The biological activities of the EO, including antifungal, herbicidal, antioxidant, and anti-inflammatory properties, were also assessed. This work provides a novel and integrated evaluation of EO production on polluted soils, combining soil contamination, mycorrhizal inoculation, and biological activities to advance sustainable phytomanagement strategies.

# Materials and methods

## Essential oil extraction

A. archangelica L., a perennial aromatic plant species, was sown in september 2018 at a seeding rate of 300,000 seeds per hectare and cultivated for 2 years on a 7100 m² TE-polluted soil (50±25′′ 55.5′′ N, 30±2′′ 25.5′′ E) displaying elevated amounts of TE (Pb: 394.5 ppm, Zn: 427.7 ppm and Cd: 6.6 ppm (Table S1). The *Angelica* seeds used for sowing were provided by the technical institute accredited by the French Ministry of Agriculture (https://www.iteipmai.fr/). The experimental field was divided into two plots, one inoculated (I) and the other non-inoculated (NI), using a commercial mycorrhizal inoculant containing the AMF *Rhizophagus irregularis* (AGTIV® Specialty Crops, 125 g·ha⁻¹; Premier Tech, QC, Canada), kindly provided by Premier Tech. The agronomic management was described in Langrand et al.³⁹. *Angelica* seeds were harvested using a combine (Dominator 108 SL Maxi, Claas) during the summer when the seeds reached maturity (June 2020). The EO used in the present work were distilled from *Angelica* seeds harvested in 2020 from NI, and I plots. The seed distillation was performed by Ferrant PHE society (a producer of EO in France) during a three-hour cycle until no more EO was recovered on a steam-distillation unit (14 m³ tank-saturated water steam, 0.3 bar). *Angelica* EO were stored at 4 °C in tightly closed brown glass vials until their analysis and use. To compare the quality of EO produced in polluted soil with that of EO from unpolluted soil, a commercial EO, distilled from seeds of *Angelica* cultivated in the same location and during the same period, and kindly provided by Ferrant PHE, was analyzed and used as a control.

## Chemical composition of *Angelica* EO

The chemical composition of three EO (2020 I and NI; commercial EO provided by Ferrant PHE) was determined by gas chromatography simultaneously coupled to a Flame Ionization Detector and a Mass Spectrometer detector (MS - Shimadzu QP 2010 Ultra). Previously diluted in ethyl acetate (1:500 (v/v)), the EO were injected in split mode (ratio 1:80) in a volume of 0.2 µL at 220 °C onto a ZB-5MS capillary column (Phenomenex – 5% Phenylarylene / 95% dimethylpolysiloxane - length 10 m, internal diameter 0.10 mm, phase thickness 0.10 µm). The carrier gas (helium) was maintained at a constant linear velocity of 60 cm·s⁻¹. The temperature was programmed to start at a temperature of 60 °C for 30 s and then increase linearly at 25 °C min⁻¹ to reach a plateau of 315 °C (1 min).

Mass spectra were determined in the electronic ionization mode at an energy of 70 eV and recorded over a range of 35 to 500 amu (m/z). The temperature parameters of the spectrometer were set at 280 °C for the ion source and 240 °C for the transfer line.

Kovats indices were determined from retention times and co-injection of a series of n-alkanes of a commercial calibration standard with chain lengths between 8 and 40 carbon atoms (C8-C40 Alkanes Calibration STD - Supelco 40147-U). The identification of the EO compounds was performed by comparing the Kovats indices and mass spectra obtained at the column outlet with those of the NIST (National Institute of Standards and Technology, Gaithersburg, MD, USA) and Wiley 275 libraries. The relative percentages of the EO constituents were measured from the peak areas.

## Biological activities of *Angelica* EO

### Crop protection applications

**In vitro** antifungal activities In order to explore the potential of *Angelica* EO in crop bioprotection, the antifungal properties were evaluated against five major phytopathogenic fungi of field crops, namely *Zymoseptoria tritici* (strain 2596, kindly provided by Dr. Ali Siah - Lille, France), *Fusarium culmorum* (purchased from CBS, Netherlands), *Fusarium graminearum* (MUCL 53451, Mycothèque de l'Université catholique de Louvain, Louvain-la-Neuve, Belgium), *Blumeria graminis f. sp. tritici* (kindly provided by Dr M.-P. Latorse from Bayer Crop Science, Lyon, France) and an oomycete *Phytophthora infestans* (MUCL 54981, Louvain-la-Neuve, Belgium). *Z. tritici*, *F. culmorum*, *F. graminearum*, and *P. infestans* are responsible for considerable yield losses in various crops (cereals, potatoes, tomatoes, etc.)⁴⁰,⁴¹ and *Fusarium sp.* is known to produce mycotoxins that cause human and animal diseases ranging from neurotoxic effects to cancer⁴².

The antifungal activity study on *F. culmorum*, *F. graminearum*, and *P. infestans* was performed on Petri dishes containing PDA (Potato-Dextrose-Agar, Condalab, Spain) medium according to a protocol adapted from Znini et al.⁴³. The medium was cooled to 50 °C before introducing the EO, to obtain a range of five concentrations from 0.005 to 1.0% (v/v). A positive control was made following the same concentration range using a reference fungicide registered for the use on field crops against many fungal diseases including *Fusarium*, Aviator XPRO (Bixafen 75 g·L⁻¹ and Prothioconazole 150 g·L⁻¹). Mycelial plugs were then cut from the circumference of a
7-day-old fungal colony and placed in the center of a 9 cm Petri dish containing PDA medium supplemented with EO for each species tested. Mycelium growth diameter is measured after 7 days of culture at 20 °C. Each test is repeated three times independently. The percentage of inhibition is calculated as follows:

$$Percentage of inhibition = \frac{x_0 - x_i}{x_0} \times 100$$

“x₀” is the average diameter of the mycelium of the control.

“xᵢ” is the average diameter of the mycelium of the different conditions studied.

These values are then used to calculate the concentration required to inhibit mycelial growth by 50% (IC₅₀) compared to the control.

The antifungal activity of EO against Z. tritici was assessed using an in vitro microplate assay, adapted from the Fungicide Resistance Committee methods and similar to that developed by Declerck et al.¹², with a range of eight concentrations from 0 to 0.8% of EO in the medium. Briefly, in order to produce spores, Z. tritici was cultivated for 4-days in PDA. Afterward, 60 µl of suspension calibrated, using Malassez counting cell, at 2.10⁵ spores.mL⁻¹ was inoculated in microplates supplemented by 140 µL of glucose peptone medium with or without test product (Fungicide Resistance Action Committee-2006). A positive control using the same concentration range (0 to 0.8% v/v) was made with the same reference fungicide, Aviator XPRO. The microplates are incubated at 20 °C under agitation (110 RPM) for 6 days. Then, the optical densities (OD) are measured at 620 nm. Each test is repeated three times independently. For each concentration, a net OD value is calculated:

$$OD_{net} = OD_{average with fungi} - OD_{average without fungi}$$

IC₅₀ values are obtained using nonlinear regressions (XLStat software) according to the following formula:

$$f(x) = bottom + \frac{top - bottom}{1 + (x \times 10^{-logIC_{50}})}$$

“Bottom”: is the value to which the curve converges for high HE values (total inhibition in the ideal).

“Top”: corresponds to the value for no inhibition.

“logIC₅₀”: corresponds to the logarithm in base 10 of the IC₅₀.

The net OD values are used as dependent values and the logarithms of the product concentrations as explanatory values. The model gives an R² value associated with log IC₅₀ (named pr3), which is then expressed to obtain the IC₅₀ of each product according to the following formula: IC₅₀ = 10pr³. For each modality, three independent replications are performed³⁶.

**Antigerminative test using Blumeria Graminis f. sp. tritici (Bgt) spores** The fungus was grown on wheat cv. Rubisko in a culture room until it was strongly sporulating. Bgt being an obligate biotroph, it cannot be grown it on PDA medium. However, Bgt spores are able to survive and germinate within 24 to 48 h on agar (1%) agar medium⁴⁴,⁴⁵. Antigerminative tests were therefore performed in vitro to assess a possible direct inhibitory effect on the germination of Bgt spores.

A positive control was carried out using the same range of concentrations of the fungicide previously used and registered for use on field crops against powdery mildew, Aviator XPRO. Each test was repeated three times independently.

**In planta antifungal activity** The in planta antifungal tests were carried out on the wheat (Rubisko cultivar, intermediate sensitivity)-Oidium (Blumeria graminis f. sp. tritici) pathosystem as a preventive treatment. Wheat was grown in trays containing standard horticultural potting soil (3 trays per condition) each containing 24 plants, for a total of 72 plants per condition. Ten days after sowing, the wheat received a foliar treatment with EO to assess its potential bioprotective effect. The control (distilled water) is not treated and allows us to verify if the infection is normal, a condition with the formulation alone (tween 0.05% and 0% of EO) was performed to determine the origin of any observed effects. Forty-eight hours after these treatments, the wheat is infected by a suspension of powdery mildew spores (1.5.10⁵ spores.mL⁻¹ (Malassez counting cell) suspended in FC43 (hepta-cosafluorotributylamine, 3 M Electronics Materials Solutions Division, Zwijndrecht, Belgium). The evaluation of the protection rate is performed 12 days after infection by counting the number of conidia formed on leaves 1 and 2. Each test was repeated three times independently.

**In vitro herbicidal activity** The herbicidal effect of EO was studied on ryegrass (monocotyledonous) and lettuce (dicotyledonous), two plant species widely used in phytoxicity tests⁴⁶. The effects of the EO were evaluated on seedling growth of the two plant species using a randomized experimental design.

The protocol for measuring herbicidal activity was adapted from the work of Judd et al. and Lyu et al.⁴⁷,⁴⁸. The water-agar medium (1%) was cooled to 50 °C before introducing the EO at concentrations ranging from 0.005 to 0.5% and casting it into 12 × 12 cm square Petri dishes. A volume of 60 mL of agar medium was prepared for each dish. A positive control prepared in the same way and containing a non-selective systemic herbicide of reference (Glyphosate 1%). 12 seeds were then placed at regular spacing on the agar in Petri dices.

The plates are then placed vertically in growth cabinets (photoperiod of 12 h; daytime temperature of 20 °C and nighttime temperature of 12 °C; constant hygrometry of 70%). Each trial was repeated three times independently. After a period of 8 days, root length is measured with a ruler and the IC₅₀ was calculated relative to the control root length. Each test was repeated three times independently.
### Healthcare product applications

**Cell line and culture conditions** Human bronchial epithelial cells (BEAS-2B, provided by the European Collection of Authenticated Cell Cultures) were cultured in CellBIND® surface plastic flasks (Corning - Thermo Fisher Scientific, Illkirch, France) in LHC-9 medium and incubated conventionally at 37 °C in a humidified atmosphere containing 5% of CO₂⁸.

### EO cytotoxicity assessment

In order to determine doses of interest, the EO cytotoxicity was first assessed at 9 different EO concentrations (i.e., 7.5 × 10⁻⁴ to 1.5 g.L⁻¹). BEAS-2B cells, exposed or not to the different EO, were seeded in 96-well CellBIND® microplates at a density of 20,000 or 10,000 cells/200 µL medium for 24–48 h of exposure, respectively. Cytotoxicity was then evaluated by measuring the extracellular lactate dehydrogenase (LDH) activity in supernatants (Cytotoxicity Detection Kit LDH, Roche Diagnostics, Neuilly-sur-Seine, France), and mitochondrial dehydrogenase (MDH) activity (Cell Proliferation Reagent WST-1, Roche Diagnostics, France), as previously described by Dergham et al. and Kfoury et al.⁸,⁴⁹. Cells not exposed to EO and cells exposed to Triton X-100 (1%) were used as negative and positive controls, respectively. Each test was repeated 8 times independently.

**Cell exposure for the study of EO Anti-Inflammatory potential** The anti-inflammatory potential of EO was assessed through a method adapted from Kfoury et al.⁸. BEAS-2B cells were previously seeded in 96-well Cell-BIND® microplates, in order to obtain 40,000 cells/well at the end of the exposure time. Cells were then exposed to PM₂.₅, i.e. particulate matter with an aerodynamic diameter inferior to 2.5 µm (15 µg.cm⁻²) to induce an inflammatory response⁵⁰,⁵¹. Particles were prepared in the LHC-9 culture medium at the desired concentration in order to reach the final concentration (i.e. 15 µg.cm⁻²) in the well, and sonicated for 5 min before intoxication for a better homogenization⁵⁰,⁵¹. The microplates were then incubated for 48 h, in the presence of EO (1.5 × 10⁻³ g.L⁻¹). Cells unexposed to EO and unexposed to both EO and PM₂.₅ were used as positive and negative controls, respectively. After 48 h of exposure, aliquots of cell-free culture supernatants were collected and frozen (– 80 °C) for the determination of cytokines’ concentrations and total protein content analysis. Cytokines’ concentrations were determined by a sandwich-based Elisa analysis (Quantikine ELISA Kits, R&D Systems Europe, Ltd., Abingdon, UK) and the total protein contents in cell-free culture supernatants were quantified using the BiCinchoninic Acid kit (Sigma-Aldrich, Saint-Quentin-Fallavier, France). Two interleukins, namely IL-6 and IL-8, were selected as cytokines of interest for the assessment of the anti-inflammatory potential of the tested EO, given their known implication as pro-inflammatory mediators in cells exposed to atmospheric particles⁸,⁵². Each test was repeated three times independently.

**Antioxidant activity** The DPPH (2,2-diphenyl-1-picrylhydrazyl) assay was used to study the antioxidant activity of angelica EO. A range of EO concentrations (up to 17 g.L⁻¹) was prepared in ethanol. 1 mL of each ethanolic EO solution was then mixed with 2 mL ethanolic DPPH⁺ solution (0.1 mM). All mixtures were shaken in the dark at 20 ± 1 °C and the absorbance of the solution was measured using a UV/Vis spectrometer (Lambda 2 S, Perkin Elmer) at 517 nm after 1, 2, 3, 4 and 5 h. The radical scavenging activity was evaluated using the following equation:

$$ \text{Antioxidant activity (AA\%)} = \left( 1 - \frac{A_S}{A_0} \right) \times 100 $$

where A_S and A_0 stand for the absorbance of the sample and of the blank, respectively. The results obtained at each time were expressed as EC₅₀ values, defined as the concentration of antioxidant that causes a 50% decrease in the DPPH⁺ absorbance, determined by graphical interpolation. In addition, EO EC₅₀ values were compared with those obtained for 6-hydroxy-2,5,7,8-tetramethylchroman-2-carboxylic acid (Trolox), a water-soluble vitamin E analog, with results expressed as Trolox equivalent antioxidant capacity (TEAC). Each test was repeated three times independently.

### Statistical analysis

Statistical analyses were performed using XLSTAT software (v2021.1.1; Addinsoft, Paris, France). Normality of the data was first subjected to the Shapiro–Wilk test. Depending on the result of this test, parametric (ANOVA) or non-parametric (Kruskal–Wallis or Mann-Whitney) tests were used, followed by Fisher’s post-hoc test (Least Significant Difference, LSD). For biological properties tests, IC₅₀ values were determined using nonlinear regression analysis from three replicates and are expressed as the mean value plus one standard deviation.

### Results and discussion

In this study, EO distilled from the aromatic plant *A. archangelica* L., cultivated on TE-polluted soil, was evaluated for its potential valorization as an effective alternative to conventional pesticides (antifungal and herbicidal) and for its application as a health-promoting product (antioxidant and anti-inflammatory properties).

The influence of TE soil pollution and mycorrhizal inoculation on the chemical composition of *Angelica* EO was evaluated.

### EO composition and environmental resilience

The results of Table 1 revealed that the compositions of *Angelica* EO produced on NI and I plots are comparable. Indeed, EO from seeds of *Angelica* contained mostly monoterpenes and sesquiterpene, the major compounds detected were: β-phellandrene (73–80%), α-pinene (5–7%), α-phellandrene (2–4%), and β-myrcene (0.5–2%)
(Table 1). These EO compositions were consistent with the literature which describes as main components in *Angelica* seeds EO: β-phellandrene (65 to 76%) followed by α-pinene (2 to 2.6%) and α-phellandrene (2 to 2.6%)⁵³⁻⁵⁵. Interestingly, it is important to note that the EO compositions are not altered by the presence of mycorrhizal inoculation (Table 1, Fig S1). These results are inconsistent with some studies that found that the EO composition of some aromatic plants such as *Coriandrum sativum* L. was modified by mycorrhization⁵⁶,⁵⁷. However, they are in accordance with the findings of Raveau et al.⁵⁸ which showed that mycorrhizal inoculation of *Coriandrum sativum* L. and *Salvia sclarea* L., did not lead to major modifications in EO compositions. Although the literature has reported many factors that can influence the EO composition such as the water deficiency, the nature of the soil, or the amount of sunshine, the data are often contradictory⁵⁹,⁶⁰.

However, TE pollution seems to affect slightly *Angelica* EO chemical composition as for example the percentage of monoterpenes was little lower in EO distilled from *Angelica* seeds produced from polluted soil by comparison to the commercial one (Fig S1). However, we also cannot exclude the potential influence of the soil's pedo-agronomic characteristics. The pollution effect is controversial. Whereas some studies have shown that the presence of TE in the soil, affects EO chemical composition, some others reported no influence¹⁸,²⁵,²⁷. In particular, it has been suggested that TE-induced stress in plants could lead to changes in secondary metabolism²⁷,⁶¹. For example, peppermint (*Mentha × piperita* L.) exposed to 40 mg.L⁻¹ of Cd, decreased menthol content from 54.1 to 40.8%, but increased menthofuran and pulegone contents by 5.7 and 1.2%, respectively, compared with the control⁶². However, these changes vary considerably depending on the species of aromatic plant, their ability to accumulate TE, the type of TE and their phytotoxicity²⁷,⁶³. Indeed, reactive oxygen species produced in response to TE can lead to lipid peroxidation, which stimulates the formation of highly active signaling compounds capable of inducing the production of secondary metabolites and thus modifying EO composition⁶⁴.

As the chemical compositions of *Angelica* EO distilled from the cultures harvested from NI and I plots, are similar (Table 1, Fig S1), all the biological activities were assessed only on the EO distilled from the seeds of *Angelica* cultures harvested from the NI plot.

## Antioxidant and anti-inflammatory activities

### Antioxidant activity

This assay evaluates the ability of an antioxidant compound to donate hydrogens to reduce the stable DPPH* to nonradicals. The EC₅₀ as well as the Trolox* equivalent antioxidant capacity (TEAC) values for the *Angelica* EO are presented in Fig. 1. Specifically, their efficacy was compared to a well-known antioxidant standard, Trolox*, and expressed in terms of TEAC, which is inversely proportional to the EC₅₀ values obtained. These values are below 1 µmol eq Trolox*/g EO at 1 h and close to 2 after 5 h. It is difficult to compare these results with those reported in the literature, as antioxidant assays are not always conducted under the same conditions. For example, in a previous study, values up to 7608 were obtained in *Pimenta racemosa* EO, which contains more phenols than angelica EO [65]. However, a comparative study of 13 EO was performed and *Angelica* seeds exhibited moderate antioxidant activity, comparable, for example, to Jasmine EO³⁵. In another study, the

<table><caption>**Table 1.** Chemical composition of EO (in %) distilled from the seeds of *Angelica* cultivated on non-inoculated (NI) and inoculated (I) polluted soils as well as on non-polluted soil (commercial EO), RT—retention time; KI*—Retention indices calculated relative to n-alkanes (C-8 to C-40) using capillary column ZB-5MS; KI—Retention indices found in the literature and the Pherobase.</caption><thead><tr><th rowspan="2">Compounds</th><th rowspan="2">RT</th><th rowspan="2">KI*</th><th rowspan="2">KI</th><th colspan="2">EO distilled from seeds of Angelica grown on polluted soils</th><th rowspan="2">Commercial EO distilled from seeds of Angelica grown on non-polluted soil</th></tr><tr><th>NI plot</th><th>I plot</th></tr></thead><tbody><tr><td>α-Pinene</td><td>1.262</td><td>933</td><td>918</td><td>7.36 ± 0.69</td><td>7.41 ± 0.31</td><td>7.02 ± 0.08</td></tr><tr><td>Sabinene</td><td>1.467</td><td>961</td><td>973</td><td>0.43 ± 0.10</td><td>0.40 ± 0.07</td><td>0.45 ± 0.03</td></tr><tr><td>β-Pinene</td><td>1.491</td><td>966</td><td>980</td><td>0.71 ± 0.02</td><td>0.71 ± 0.01</td><td>0.77 ± 0.04</td></tr><tr><td>β-Myrcene</td><td>1.552</td><td>979</td><td>991</td><td>1.43 ± 0.07</td><td>1.31 ± 0.08</td><td>1.65 ± 0.05</td></tr><tr><td>α-Phellandrene</td><td>1.644</td><td>999</td><td>1005</td><td>3.26 ± 0.11</td><td>3.27 ± 0.09</td><td>4.20 ± 0.14</td></tr><tr><td>β-Phellandrene</td><td>1.795</td><td>1026</td><td>1031</td><td>76.27 ± 0.20</td><td>76.30 ± 0.40</td><td>80.16 ± 0.14</td></tr><tr><td>β-Ocimene</td><td>1.868</td><td>1040</td><td>1050</td><td>0.50 ± 0.04</td><td>0.55 ± 0.20</td><td>0.40 ± 0.02</td></tr><tr><td>Ylangene</td><td>3.705</td><td>1370</td><td>1375</td><td>0.24 ± 0.01</td><td>0.24 ± 0.01</td><td>0.15 ± 0.01</td></tr><tr><td>Copaene</td><td>3.735</td><td>1376</td><td>1377</td><td>0.40 ± 0.01</td><td>0.39 ± 0.05</td><td>0.17 ± 0.01</td></tr><tr><td>β-Bourbonene</td><td>3.782</td><td>1385</td><td>1384</td><td>0.23 ± 0.02</td><td>0.22 ± 0.01</td><td>0.09 ± 0.02</td></tr><tr><td>β-Elemene</td><td>3.809</td><td>1390</td><td>1391</td><td>0.25 ± 0.04</td><td>0.29 ± 0.05</td><td>0.14 ± 0.04</td></tr><tr><td>Humulene</td><td>4.154</td><td>1457</td><td>1440</td><td>1.40 ± 0.08</td><td>1.38 ± 0.04</td><td>1.63 ± 0.04</td></tr><tr><td>α-Curcumene</td><td>4.446</td><td>1495</td><td>1517</td><td>0.12 ± 0.02</td><td>0.17 ± 0.1</td><td>-</td></tr><tr><td>β-Curcumene</td><td>4.458</td><td>1553</td><td>1513</td><td>2.06 ± 0.03</td><td>2.11 ± 0.09</td><td>-</td></tr><tr><td>1,8-Bis(Dimethylamino)Naphthalene</td><td>4.463</td><td>1519</td><td>-</td><td>0.64 ± 0.10</td><td>0.67 ± 0.06</td><td>-</td></tr><tr><td>Monoterpenes</td><td></td><td></td><td></td><td>89.46</td><td>89.40</td><td>94.25</td></tr><tr><td>Sesquiterpenes</td><td></td><td></td><td></td><td>5.20</td><td>4.85</td><td>3.17</td></tr><tr><td>Others</td><td></td><td></td><td></td><td>4.70</td><td>4.85</td><td>3.17</td></tr></tbody></table>
<figure><img src="image_4.png" /><figcaption>**Fig. 1.** Kinetics of antioxidant activity of *Angelica* EO. Significant differences using a one-way ANOVA comparison (α = 0.05), between results (n = 3) are indicated by different letters.</figcaption></figure>

obtained values were similar to those reported for *Salvia officinalis* inflorescence and *Coriandrum sativum* seed EO⁵⁸. *Angelica* seeds EO is mainly composed of mono- and sesquiterpenes⁸,⁶⁶,⁶⁷. In our study, this may partially explain the moderate antioxidant activity observed. Additionally, sabinene, present in *Angelica* EO at 0.2 to 0.4, could contribute to the overall reducing capacity, as suggested in previous reports describing its strong radical-scavenging potential⁶⁸.

### Anti-inflammatory activity

Before evaluating the anti-inflammatory potential of our EO, we determined the dose of interest (non-cytotoxic) to be applied to the BEAS-2B cell line using two complementary cytotoxicity tests: lactate dehydrogenase activity (LDH) and mitochondrial dehydrogenase activity (MDH) (data not shown). For the LDH test which allows us to measure the alteration of the membrane integrity, we can notice toxic effects from the concentration of 7.5 mg.L⁻¹, with high cytotoxic effects after exposure to the highest concentration (1500 mg.L⁻¹). Concerning MDH test, cytotoxic effects were observed after exposure 15 mg.L⁻¹ of *Angelica* EO. Thus, concentrations of 0.9375, 1.875 and 3.75 mg.L⁻¹ do not present any significant cytotoxic effect on the BEAS-2B cell line. In order to study the potential anti-inflammatory effect of *Angelica* EO, we therefore decided to retain the concentration 1.5 mg.L⁻¹ which, according to our results, does not present any cytotoxic effect.

Then, to evaluate the anti-inflammatory activity of *Angelica* EO on the BEAS-2B lung cell line, we previously induced an inflammatory response in the cells by the addition of fine atmospheric particles (PM₂.₅), a toxic agent known to trigger an inflammatory and oxidative stress on pulmonary cells⁸. The inflammatory response was assessed by quantifying interleukin 8 (IL-8) which is secreted by cells during exposure to pro-inflammatory stress. The Fig. 2 showed that exposure to PM₂.₅ led to a threefold increase in IL-8 concentration compared with the control, confirming successful inflammation induction. However, combining EO addition to PM₂.₅ exposure, the obtained concentration of IL-8 was decreased by 6, thus underlining the promising anti-inflammatory effect of *Angelica* EO.

Previous studies have shown that several components present in EO such as trans-anethole, estragole, eugenol and isoeugenol, tested alone, had the ability to protect cells against inflammation⁸, and similar effect was observed with coriander EO⁵⁸. Regarding *Angelica* EO, Fraternale et al.⁶⁸ also demonstrated its anti-inflammatory properties with a decrease in the level of the pro-inflammatory interleukin-6 in human umbilical vein endothelial cells, as a model of *in vitro* senescence, after cells exposure to lipopolysaccharide, one of the most powerful pro-inflammatory. In addition, the anti-inflammatory potential of *Angelica* EO could result from the synergistic action of several components, including α-phellandrene, which has been reported in previous studies to reduce cytokine expression in inflammatory models⁶⁶. So the observed decrease in IL-8 levels after EO addition suggested that similar molecular pathways might be involved⁹. Recently, the appeal of various essential oils in biomedicine has generated increasing interest due to their therapeutic potential as anti-inflammatory, antioxidant, and antibacterial mediators⁶⁹,⁷⁰. Oxidative stress and inflammation are well known to be two related processes common to many human pathologies. Pontes-Quero et al.⁶⁹ described how the antioxidant, anti-inflammatory, and biocompatibility properties of curcumin essential oil open up real research prospects for the treatment of inflammatory and oxidative stress-related diseases with essential oils. More recently, Veljovic et al.⁷¹ demonstrated in their study that treating human BEAS-2B bronchial epithelial cells with an EO significantly decreased LPS-induced IL-8 expression. The results obtained in our study corroborate this observation and suggest that the use of such EO could have a beneficial effect in many inflammatory lung diseases. Further *in vitro* and *in vivo* studies are certainly needed to explore in depth the anti-inflammatory potential of EO and their possible applications in drug delivery systems.
<figure><img src="image_5.png" /><figcaption>**Fig. 2.** Cytokine levels in BEAS-2B cells exposed for 48 h to PM<sub>2.5</sub> in the presence of *Angelica* EO: (C) control, (PM) PM2.5, (PM + EO) *Angelica* EO NI 2020 – 1.5 × 10<sup>-3</sup> g.L<sup>-1</sup>. Data are presented as mean ± standard deviation (n = 3). Significant differences using a two-way ANOVA comparison (α = 0.05), between results are indicated by different letters. BEAS-2B: human bronchial epithelial cells; IL-8: interleukin 8; PM<sub>2.5</sub>: particulate matter with an aerodynamic diameter inferior to 2.5 µm.</figcaption></figure>

<table><caption>**Table 2.** Average IC<sub>50</sub> (mg.L<sup>-1</sup>) of *Angelica* EO and aviator against plant fungal pathogens: *F. culmorum*, *F. graminearum*, *Z. tritici*, *B. graminis*, and the oomycete *P. infestans*. Values are means ± SD (n = 3). Significant differences for each pathogen, between *Angelica* EO and the positive control, using a nonparametric test with Mann–Whitney α = 0.05 performed independently, are indicated by different letters.</caption><thead><tr><td>Phytopathogens</td><td>Aviator</td><td>Angelica EO</td></tr></thead><tbody><tr><td>F. culmorum</td><td>3.54.10<sup>-1</sup> ± 7.17.10<sup>-2</sup> A</td><td>198.0 ± 238 B</td></tr><tr><td>F. graminearum</td><td>3.24.10<sup>-2</sup> ± 8.34.10<sup>-2</sup> A</td><td>92.5 ± 75.9 B</td></tr><tr><td>Z. tritici</td><td>5.50.10<sup>-2</sup> ± 3.83.10<sup>-2</sup> A</td><td>21.0 ± 6.19 B</td></tr><tr><td>B. graminis</td><td>1.93.10<sup>-1</sup> ± 2.59.10<sup>-2</sup> A</td><td>221.0 ± 186 B</td></tr><tr><td>P. infestans</td><td>3.38.10<sup>-2</sup> ± 1.83.10<sup>-3</sup> A</td><td>128.0 ± 6.78 B</td></tr></tbody></table>

Antifungal and herbicidal applications

*Growth Inhibition of F. culmorum, F. graminearum, Z. tritici, B. graminis and P. infestans*

Numerous studies have demonstrated that the biological activities of EO often result from the synergistic interaction among their constituents, rather than from the activity of a single major compound ¹,⁷⁴,⁷². Moreover, the mechanism of action of EO on fungi has not been fully elucidated, studies have highlighted interactions between certain EO compounds and the tyrosine-tRNA ligase of various fungi, suggesting possible alteration of fungal protein synthesis as a mechanism of fungitoxicity⁷³,⁷⁴. Others have reported damage to fungal cell envelopes, particularly at the mitochondrial level⁷⁵,⁷⁶.

Overall, several key modes of antifungal action have been described in the literature, including the inhibition of fungal cell wall biosynthesis, ergosterol production, cell division, and efflux pump activity, as well as interference with nucleic acid (RNA/DNA) and protein synthesis²,⁴¹,⁷⁷,⁷⁸. In the present study, *Angelica* EO exhibited antifungal activity with IC<sub>50</sub> values ranging from 21 mg.L<sup>-1</sup> against *Z. tritici* to 221 mg.L<sup>-1</sup> against *B. graminis* (Table 2). After these tests, the subculture of these fungal species (*F. culmorum*, *F. graminearum*) and the oomycete (*P. infestans*) on an EO-free medium of demonstrated the fungistatic activity of *Angelica* EO on the studied phytopathogens.

To date, fungistatic effects of *Cinnamomum cassia* and *C. zeylanicum* EO have been demonstrated on *F. culmorum* and *F. graminearum* and to a lesser extent on *P. infestans*, including a fungistatic effect of *Angelica* seed and root EO against *F. culmorum*¹²,³⁶,⁴¹. However, the biological effects of EO are mostly dose-dependent¹². Indeed, selecting the appropriate concentration is crucial to maximize efficacy while minimizing adverse effects⁷⁹. A thorough understanding of the dose-response relationship is essential for optimal use of EO⁸⁰. It has been described that, *Angelica* EO has strong antibacterial activity against *Clostridium difficile*, *C. perfringens*, *Enterococcus faecalis*, *Eubacterium limosum*, *Peptostreptococcus anaerobius*, and *Candida albicans*⁶⁰. In the present study, antifungal activity of *Angelica* EO against *F. culmorum*, *F. graminearum*, *Z. tritici* and the oomycete *P. infestans* has been evidenced. For example, sabinene, α-pinene, β-elemene, cis-β-ocimene, and curcumene which
represent around 8% of total *Angelica* EO composition are reported for antifungal activity against *Aspergillus*, *Trichophyton* or *Candida* spp$^{60,81–83}$. In addition, Zhan et al.$^{83}$ showed a decrease in *Saccaromyces cerevisiae* membrane fluorescence when treated with EO from *Chrysanthemum morifolium* cv. *Fubaiju*, suggesting that the above-mentioned EO components caused severe damage to the cytoplasmic membrane, up to and including its total destruction. This characteristic could be valuable in preventive applications as a means of controlling fungal diseases before and after harvest. Although EO IC$_{50}$ are higher than those of marketed chemical fungicides, the EO tested still showed interesting antifungal activity. Furthermore, EO are known to be less harmful to the environment, human health and non-target organisms than conventional fungicides$^{12}$. In particular, because of their low persistence in soils, as well as their volatile nature$^{12}$. What is more, unlike pesticides, they do not lead to the development of resistance in target pest species$^{84,85}$. This could be explained by the complexity, diversity and large number of components in EO, or their less frequent use.

In all cases studied, the IC$_{50}$ of *Angelica* EO are statistically higher to those of the fungicide, Aviator, used as conventional positive control with values ranging from 3.24 $10^{-2}$ for *F. graminearum* to 3.54 $10^{-1}$ mg.L$^{-1}$ for *F. culmorum*. Nevertheless, *Angelica* EO activity remains promising given that unlike the reference plant protection product, the EO have not been formulated. As EO are highly volatile compounds, a formulation aimed at limiting their volatility could both reduce the quantity of EO used, and prolong their activity, thus limiting the need for repeated treatments and increasing their effectiveness. Recent work has shown that the formulation strategy can be as important as the intrinsic composition of the EO for determining its antifungal efficacy. Although the Angelica EO demonstrated promising biocidal activities *in vitro*, its practical application in the field may be limited by high volatility and environmental degradation. To address these challenges, nano-encapsulation approaches—such as nanoemulsions or mesoporous silica matrices—have been shown to significantly enhance EO stability and bioactivity$^{86,87}$. For instance, encapsulated systems not only improve persistence but also amplify antimicrobial activity by ensuring a controlled release and enhancing cellular uptake, as demonstrated for fenugreek and coriander EO$^{88–90}$. Furthermore, such formulations have proven successful in reducing phytotoxicity while maintaining efficacy against pests in horticultural crops$^{91}$. Consequently, the moderate activity observed in our study could be optimized through appropriate formulation strategies, offering a promising pathway to valorize this phytomanagement by-product as a sustainable biopesticide.

### *Herbicidal activity*

In addition to antifungal properties, the *Angelica* EO revealed herbicidal activity compared to the control (Table 3) on both lettuce and ryegrass, two plant species frequently used in phytotoxicity tests$^{46}$. For the lettuce, the IC$_{50}$ of angelica EO was significantly higher than that obtained with the control (glyphosate). On the other hand, we note an interesting herbicidal activity of *Angelica* EO against ryegrass, since the IC$_{50}$ of EO and the positive control are not statistically different.

Regarding the phytotoxic effects of EO, some authors have concluded that EO affect membrane lipid organization and domain formation, particularly in the case of monoterpenes, while phenylpropanoids interact with plasma membrane receptors$^{92}$. For example, *Citronella* EO components reduced germination of *Digitaria horizontalis* and *Cenchrus echinatus*, and decreased their chlorophyll and total protein content$^{93}$. Citronella EO also caused cuticular wax rupture, stomatal obstruction and rapid electrolyte leakage, as a consequence of disrupted membrane integrity [94]. In addition to its activity on the membrane, Citronella EO has also been shown to affect the structure of microtubules in plant cells$^{1,95}$. Similarly to angelica seed EO, lemongrass EO contains a majority of monoterpenes, which are the source of its biological activity$^{96}$.

### *In planta* tests

Tests of protection wheat against powdery mildew by preventive treatments of *Angelica* EO were performed *in planta*. The application of 5% angelica EO resulted in a significant decrease, estimated to 35%, in the number of colonies per plant by comparison to the non-treated wheat control. Thus, *Angelica* EO allowed a wheat protection of 40% (Fig. 3). To our knowledge, there is few studies evaluating EO antifungal activity *in planta*. Only, Hafez in 2008$^{97}$ demonstrated that formulated *Nigella sativa* EO, rich in monoterpenes and sesquiterpenes$^{98}$ like *Angelica* EO, was effective as a curative treatment on barley and cucumber powdery mildew. These authors showed a strong toxic effect on hyphal growth and spore germination treated with *Nigella sativa* EO, with damaged conidia and an inhibition of hyphal formation$^{97}$. According to Hafez$^{97}$, the inhibition of spore germination and hyphal growth observed with other EO may be associated with oxidative stress responses, including increased H$_{2}$O$_{2}$ and O$_{2}$ levels and the activation of antioxidant enzymes such as ascorbate peroxidase and glutathione-S-transferase. Although these parameters were not evaluated in the present study, similar processes could potentially contribute to the antifungal activity observed with *Angelica* EO.

<table><caption>**Table 3.** Average IC$_{50}$ (mg.L$^{-1}$) of *Angelica* EO resulting from the growth Inhibition bioassay against lettuce and ryegrass. Values are means ± SD (n = 3). Letters indicate a significant difference (Student, α = 0,05) performed independently for each plant species.</caption><thead><tr><td>Plants</td><td>Glyphosate</td><td>Angelica EO</td></tr></thead><tbody><tr><td>Ryegrass</td><td>1.47 ± 6.91 10<sup>-1</sup> A</td><td>144 ± 82.9 A</td></tr><tr><td>Lettuce</td><td>4.65 10<sup>-1</sup> ± 4.26 10<sup>-1</sup> B</td><td>5390 ± 4760 A</td></tr></tbody></table>
<figure><img src="image_6.png" /><figcaption>**Fig. 3.** Bioprotection tests of wheat against powdery mildew. Mean values ± SD (n=72). Letters indicate a significant difference (Kruskal-Wallis, α = 0.05). Control: water.</figcaption></figure>

## Conclusion

Analysis of the chemical composition of EO distilled from *Angelica* cultivated on TE-polluted soil revealed the presence of sabinene, α-pinene, β-elemene, cis-β-ocimene and β-curcumene. It was also showed that mycorrhizal inoculation did not noticeably modify the chemical composition of *Angelica* EO. r. This study highlights the potential of *Angelica* EO, distilled from plants grown on TE-polluted soil, for applications in both crop protection and health sector. Indeed, *Angelica* EO exhibited moderate antioxidant and significant anti-inflammatory properties. In addition, this EO could be interesting for its potential use as an alternative to conventional pesticides. *In vitro* tests pointed antifungal activities for *Angelica* EO against *F. culmorum*, *F. graminearum*, *Z. tritici*, *B. graminis*, and the oomycete *P. infestans*. Furthermore, the strong herbicidal activity against ryegrass suggests its potential use in weed management strategies. However, further research is needed to evaluate its effectiveness under field conditions and to optimize its formulation for improving its efficacy. Actually, EO can be formulated in various ways (emulsions, encapsulations and nano-encapsulation, powders) to enhance their stability and field efficacy. When combined with other agroecological practices, such as crop rotation or the use of natural allies, they offer the possibility of developing innovative and ecologically responsible integrated crop protection strategies. Finally, the findings of this study strongly support the integration of *A. archangelica* cultivation into phytomanagement strategies for TE-contaminated soils. By demonstrating that EO distilled from plants grown on polluted sites exhibits interesting biological activities, this work validates the potential of this crop to valorize marginal lands while producing high-value non-food products. Utilizing these EO as natural, eco-friendly alternatives to synthetic phytopharmaceuticals could not only enhance the economic viability of phytotechnologies but also contribute to sustainable agriculture by reducing reliance on conventional chemical inputs.

## Data availability

No datasets were generated or analysed during the current study.

Received: 7 July 2025; Accepted: 10 December 2025

Published online: 18 December 2025

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## Acknowledgements

The authors wish to thank the "Université du Littoral Côte d'Opale" and the "the French Region of Hauts-de-France" for providing financial support for J. Langrand Ph.D thesis. This research was funded by l'Agence De l'Environnement et de la Maîtrise de l'Energie (ADEME, Angers, France) in the framework of DEPHYTOP project. This work has also been carried out in the framework of the BiHauts Eco de France CPER project, which
is funded by the European Union, the French State, and the French Region of Hauts-de-France and in the frame-
work of PRIMA BIO-TEAM project.

Author contributions

Conceptualization, J.L., A.L.-H.S. and J.F.; methodology, N.F., F.L., J.L., S.F., A.V., A.L.-H.S., and J.F.; writing—
original draft preparation, J.L.; writing—review and editing, J.L., A.L.-H.S., S.F., A.V., and J.F.; supervision, A.L.-
H.S. and J.F.; project administration, A.L.-H.S.; funding acquisition, A.L.-H.S. All authors have read and agreed
to the published version of the manuscript.

Funding

This research was funded by l'Agence De l'Environnement et de la Maîtrise de l'Energie (ADEME, Angers, France) in the framework of DEPHYTOP project. This work has also been carried out in the framework of the BiHauts Eco de France CPER project, which is funded by the European Union, the French State, and the French Region of Hauts-de-France, and PRIMA BIO-TEAM project (funded by ANR).

Declarations

Competing interests

The authors declare no competing interests.

Additional information

**Supplementary Information** The online version contains supplementary material available at https://doi.org/1
0.1038/s41598-025-32550-5.

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