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    Topic review

    Artemisia Genus as Biopesticides

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    Submitted by: Bianca Ivanescu

    Definition

    The Artemisia L. genus includes over 500 species with worldwide distribution and diverse chemical composition. Many secondary metabolites of this genus are known for their antimicrobial, insecticidal, parasiticidal, and phytotoxic properties, which recommend them as possible biological control agents against plant pests. Given the negative impact of synthetic pesticides on human health and on the environment, Artemisia‐derived biopesticides and their nanoformulations emerge as promising ecofriendly alternatives to pest management.

    1. Introduction

    The Artemisia L. genus contains over 500 species, herbaceous plants and shrubs, widespread in the northern hemisphere, in Asia, Europe, and North America. Artemisia species are found in various ecosystems, ranging from arid regions to wetland at sea level as well as in the mountains. The largest number of species are located in the steppes of Asia [1]. Common names of Artemisia species are wormwood, mugwort, and sagebrush. Due to their biological and chemical diversity, Artemisia species have numerous applications in the treatment of plant and human diseases, in cosmetic and pharmaceutical industry. In addition, various Artemisia species are used all over the world as foods, spices, condiments, and beverages [2]. Many important medicinal plants belong to this genus and exert a range of therapeutic actions: antibacterial, antifungal, antiviral, antiprotozoal, anthelmintic, anti-inflammatory, anti-ulcer, appetite stimulating, hepatoprotective, antispasmodic, bronchodilator, hypolipidemic, antihypertensive, analgesic, neuroprotective, neurotrophic, anti-depressant, antioxidant, cytotoxic, antitumor, estrogenic, anti-allergic, immunomodulatory, insecticidal, repellent, and anticonvulsant [3][4][5][6][7][8].
    Most Artemisia species are aromatic plants that produce volatile oil in the secretory hairs on the aerial organs but also through the secretory ducts in the parenchyma tissues. Essential oils could be used as biocontrol agents based on the antibacterial, antifungal, repellent, insecticidal, nematicidal, and phytotoxic effect of volatile compounds. Moreover, the complex mixture of substances with different mechanisms of action, often having synergistic activity, can be effective in preventing the emergence of resistant strains of phytopathogens [9][10][11][12].
    The global use of synthetic pesticides has many disadvantages, such as high cost, danger to non-target organisms, accumulation of pesticide residues in the environment, the emergence of resistant phytopathogenic strains, and negative impact on human health [12]. In contrast, biological pesticides can achieve pest management in an environmentally friendly way and could become safer alternatives for the treatment of crop diseases. Many agents are considered biopesticides, such as viruses, microbes, fungi, entomophagous invertebrates, parasitoids, predators, and substances produced by living organisms such as bacteria, fungi, plants, algae, animals, etc. Throughout this review, we will use the word “biopesticides” for plant-derived substances or extracts. During evolution, plants developed different mechanisms to defend themselves from predators and diseases by producing substances with bactericidal, fungicidal, insecticidal, nematicidal, or repellent activity. At present, these phytochemicals are explored as biocontrol agents for crops integrated pest management. Plant compounds are cheaper, safer for farmers, less toxic to non-target organisms, and rapidly degraded in the environment [13].
    In this context, numerous researchers have identified new potential biopesticides in plants of the Artemisia genus. Since most species are fragrant, the vast majority of investigations have focused on the biological actions of volatile oils and compounds. Essential oils contain a variety of volatile molecules such as mono- and sesquiterpenes as well as phenolic-derived aromatic and aliphatic components [1]. The percentage of individual compounds in the essential oil is variable and depends on genetic factors (species, chemotype), plant origin, plant organ, period of harvest or developmental stage, environmental factors (climate, altitude, sun exposure), and cultivation conditions. Qualitative and quantitative differences in the composition of the essential oil can also be caused by drying methods, extraction procedure and time, quantification methods, and conditions of analysis [11]. All these elements could change the chemical composition of an essential oil, leading to changes in activity; thus, standardization is necessary to guarantee the effect, and also for regulatory and marketing purposes. Moreover, plants with desirable pesticide action may give low yields of essential oil, hence the need for new and more efficient extraction methods, which will increase the quantity and quality of extracted oil while reducing the time and cost of extraction [14].

    2. Artemisia Compounds and Extracts with Pesticide Activity

    2.1. Antifungal and Anti-Oomycete Activity

    Pathogenic fungi produce almost 30% of crop diseases, threatening the health and food security of a growing human population dependent on substantial agricultural production [15]. Phytopathogenic fungi affect plants during their cultivation or after harvest, causing significant losses in crop plants. In addition, certain fungi (Aspergillus spp., Fusarium spp., Alternaria spp. etc.) produce mycotoxins that endanger the health of consumers through hepatotoxic, nephrotoxic, and carcinogenic effects or even cause death [16]. In an effort to find an ecological solution to this problem, numerous studies have assessed the antifungal effect of Artemisia species, focusing especially on volatile oil and compounds. Different methods of evaluation were used in vitro, in planta, or in field conditions, and the results were expressed in various ways: half maximal inhibitory concentration—IC50, minimal inhibitory concentration—MIC, minimum fungicidal concentration—MFC, median effective concentration—ED50, inhibition zone, and percent of inhibition (Table 1).
    Table 1. Antifungal activity of Artemisia extracts and compounds against phytopathogenic fungi.
    Artemisia Species Extract * or Compound Tested Fungi Inhibitory Dose Type of Study Reference
    A. abrotanum
    fresh aerial parts
    essential oil (eucalyptol) Sclerotinia sclerotiorum MIC = 1200 μL/L in vitro [17]
    A. absinthium
    aerial parts
    essential oil
    (cis-epoxyocimene, (−)-cis-chrysanthenol, chrysanthenyl acetate, linalool and β-caryophyllene)
    Botrytis cinerea ED50 = 0.01–0.07 mg/mL in vitro [18]
    Fusarium moniliforme ED50 = 0.24–0.43 mg/mL
    F. oxysporum ED50 = 0.29–0.40 mg/mL
    F. solani ED50 = 0.24–0.50 mg/mL
    A. absinthium
    leaves
    aqueous extract (1:1) Alternaria alternata 79.75% inhibition in vitro [19]
    Mucor piriformis 73.04% inhibition
    Penicillium expansum 75.42% inhibition
    A. annua
    fresh aerial parts
    essential oil (artemisia ketone) Sclerotinia sclerotiorum MIC = 2400 μL/L in vitro [17]
    A. annua
    aerial parts
    essential oil (artemisia ketone, α-selinene and γ-terpineol) Alternaria solani EC50 = 21.78 mg/mL in vitro
    agar diffusion
    [20]
    EC50 = 14.18 mg/mL in vitro spore germination
    A. annua
    leaves
    methanol extract (ultrasound-assisted) Fusarium oxysporum 36.94% inhibition in vitro [21]
    essential oil (camphor, germacrene D, β-caryophyllene, camphene) F. oxysporum MIC = 0.22 mg/mL
    F. solani MIC = 0.37 mg/mL
    L-camphor F. oxysporum MIC = 0.11 mg/mL
    F. solani MIC = 0.31 mg/mL
    DL-camphor F. oxysporum MIC = 0.14 mg/mL
    F. solani MIC = 0.16 mg/mL
    β-caryophyllene F. oxysporum MIC = 0.13 mg/mL
    F. solani MIC = 0.23 mg/mL
    camphene F. oxysporum MIC = 0.16 mg/mL
    F. solani MIC = 0.22 mg/mL
    petroleum ether extract F. oxysporum, F. solani 27.78% and 25% infection incidence, at 0.25 mg/g and 0.5 mg/g in the culture media, respectively in vivo on Panax notoginseng
    A. annua
    whole plant
    ethanol extract Aspergillus flavus 14 mm inhibition zone at 200 μg/mL in vitro [22]
    A. niger 14.5 mm inhibition zone at 200 μg/mL
    A. annua artemisinin Aspergillus fumigatus IC50 = 125 µg/mL
    IC90 = 250 µg/mL
    in vitro [23]
    A. arborescens essential oil (chamazulene, camphor) Rhizoctonia solani 47.2% inhibition at 12.5 µL/20 mL medium
    100% inhibition at 50 µL/20 mL medium
    in vitro [24]
    A. argyi
    leaves
    essential oil (caryophyllene oxide, neointermedeol, borneol, α-thujone, β-caryophyllene) Aspergillus niger MIC = 6.25 µL/mL in vitro [25]
    A. argyi
    inflorescence
    essential oil (spathulenol, juniper camphor, caryophyllene oxide, terpineol, 1,8-cineole, borneol, camphor, chamazulene) Alternaria alternata 84.7% inhibition at 1000 mg/L in vitro [26]
    Botrytis cinerea 93.3% inhibition at 1000 mg/L
    A. austriaca
    fresh aerial parts
    essential oil
    (camphor)
    Sclerotinia sclerotiorum MIC = 2400 μL/L in vitro [17]
    A. caerulescens ssp. densiflora essential oil (terpinen-4-ol, p-cymene, γ-terpinene, 1,8-cyneole, α-terpineol) Alternaria spp. 20 mm inhibition zone at 1:2 dilution in vitro [27]
    Aspergillus spp. 12 mm inhibition zone at 1:1 dilution
    Fusarium spp. 16 mm inhibition zone at 1:8 dilution
    A. campestris
    aerial parts
    methanol extracts (1:10) Aspergillus niger 32.5–33.1 mm inhibition zone at 20 µg/mL in vitro [28]
    A. campestris
    aerial parts
    essential oil (α-pinene, β-pinene, β-myrcene, germacrene D) Aspergillus flavus MIC = 2.5 μL/mL
    MFC = 2.5 μL/mL
    in vitro [29]
    Aspergillus niger MIC = 10 μL/mL
    MFC >20 μL/mL
    Aspergillus ochraceus MIC = 2.5 μL/mL
    MFC = 5 μL/mL
    Aspergillus parasiticus MIC = 2.5 μL/mL
    MFC = 5 μL/mL
    Fusarium culmorum MIC = 2.5 μL/mL
    MFC = 5 μL/mL
    Fusarium graminearum MIC = 1.25 μL/mL
    MFC = 1.25 μL/mL
    Fusarium moniliforme MIC = 2.5 μL/mL
    MFC = 2.5 μL/mL
    Penicillium citrinum MIC = 5 μL/mL
    MFC > 20 μL/mL
    Penicillium expansum MIC = 2.5 μL/mL
    MFC = 2.5 μL/mL
    Penicillium viridicatum MIC = 10 μL/mL
    MFC > 20 μL/mL
    A. chamaemelifolia aerial parts essential oil (carvacrol, thymol, p-cymene α-cadinol) Aspergillus oryzae MIC = 312.5 μg/mL
    MFC = 312.5 μg/mL
    in vitro [30]
    Aspergillus niger MIC = 2500 μg/mL
    MFC = 2500 μg/mL
    Byssochlamys spectabilis MIC = 625 μg/mL
    MFC = 625 μg/mL
    Paecilomyces variotii MIC = 625 μg/mL
    MFC = 625 μg/mL
    Penicillium chrysogenum MIC = 625 μg/mL
    MFC = 625 μg/mL
    Trichoderma harizanum MIC = 312.5 μg/mL
    MFC = 312.5 μg/mL
    A. dracunculus
    fresh aerial parts
    essential oil
    (sabinene)
    Sclerotinia sclerotiorum MIC = 2400 μL/L in vitro [17]
    A. dracunculus var. pilosa
    fresh aerial parts
    essential oil
    (borneol)
    MIC = 2400 μL/L
    A. herba-alba
    aerial parts
    essential oil
    (davanone, camphor, thujone)
    Fusarium moniliforme MIC = 0.5% in vitro
    direct contact
    [31]
    Fusarium oxysporum MIC = 0.5%
    Fusarium solani MIC = 0.75%
    Stemphylium solani MIC = 0.75%
    A. herba-alba
    leaves
    essential oil (β-thujone, α-thujone camphor) Penicillium aurantiogriseum 100% inhibition at 0.89% in vitro [32]
    P. viridicatum 100% inhibition at 1.33%
    A. herba-alba
    fresh leaves
    essential oil Mucor rouxii 100% inhibition at 1000 µg/mL in vitro [33]
    Penicillium citrinum 100% inhibition at 1000 µg/mL
    carvone Mucor rouxii IC50 = 7 µg/mL
    Penicillium citrinum IC50 = 5 µg/mL
    piperitone Mucor rouxii IC50 = 1.5 µg/mL
    Penicillium citrinum IC50 = 2 µg/mL
    A. herba-alba
    aerial parts
    chloroform-methanol extract Fusarium solani MIC = 62.5 μg/disc in vitro [34]
    11-epiartapshin MIC = 50 μg/disc
    A. incisa
    aerial parts
    santolinylol-3-acetate Aspergillus flavus MIC = 300 μg/mL in vitro [35]
    santolinylol MIC = 300 μg/mL
    trans-ethyl cinnamate MIC = 500 μg/mL
    isofraxidin MIC = 400 μg/mL
    eupatorin MIC = 1000 μg/mL
    scopoletin inactive
    esculetin inactive
    A. judaica
    aerial parts
    essential oil
    (piperitone, 3-bornanone)
    Aspergillus niger MIC = 1.25 μg/disc in vitro [36]
    Fusarium solani MIC = 2.5 μg/disc
    A. khorasanica
    aerial parts
    essential oil (davanone, p-cymene, Z-citral, β-ascaridol, thymol) Fusarium moniliforme MIC = 2000 µL/L in vitro [37]
    Fusarium solani MIC = 1500 µL/L
    Rhizoctonia solani MIC = 1000 µL/L
    Tiarosporella phaseolina MIC = 2000 µL/L
    A. lavandulaefolia
    aerial parts
    essential oil (eucalyptol,
    (-)-terpinen-4-ol, α-terpineol)
    Alternaria solani EC50 = 10.45 mg/mL in vitro
    agar diffusion
    [20]
    EC50 = 6.64 mg/mL in vitro
    spore germination
    A. lerchiana
    fresh aerial parts
    essential oil
    (eucalyptol)
    Sclerotinia sclerotiorum MIC = 2400 μL/L in vitro [17]
    A. maritima
    aerial parts
    essential oil
    (1,8-cineole, chrysanthenone, germacrene D, borneol)
    Aspergillus flavus 35.4% inhibition at 10 µL/plate in vitro [38]
    A. niger 60.6% inhibition at 10 µL/plate
    A. ochraceus 56.1% inhibition at 10 µL/plate
    A. parasiticus 32.45% inhibition at 10 µL/plate
    A. terreus 58.3% inhibition at 10 µL/plate
    Fusarium moniliforme 33.9% inhibition at 10 µL/plate
    Penicillium chrysogenum 28.6% inhibition at 10 µL/plate
    A. nilagirica
    shoot
    essential oil (camphor, β-caryophyllene, α-thujone, sabinene) Aspergillus flavus, A. niger,
    A. ochraceus
    MIC = 0.29 μL/mL
    MFC = 0.58 μL/mL
    in vitro [39]
    100% mycotoxin inhibition at 0.16 μL/mL
    Aspergillus terreus, Cladosporium cladosporioides, Fusarium moniliforme, Fusarium oxysporum, Mucor mucedo, Penicillium expansum, P. funiculosum, Rhizopus stolonifer 100% inhibition at 0.29–0.58 μL/mL in vitro
    0% disease incidence at 300 μL/2 L in situ
    fumigation test on grapes, 10 days storage
    A. nilagirica
    aerial parts
    essential oil (1,5-heptadiene-4-one,3,3,6-trimethyl, artemisia alcohol, α-ionone, benzene, methyl (1-methylethyl)) Aspergillus flavus
    toxigenic strain
    MIC = 1.4 µL/mL
    MFC = 4.0 µL/mL
    in vitro [40]
    Alternaria alternata, Aspergillus flavus, A. minutus, A. niger, A. sydowii, A. terreus, Cheatomium spirale, Curvularia lunata, Mucor spp., Mycelia sterilia Penicillium italicum, P. purpurogenum, Rhizopus stolonifer, 70–100% inhibition at 1.4 µL/mL in vitro
    71% protection from fungal contamination at 1.4 μL/mL in air in situ on Eleusine
    coracana seeds, 12 months storage
    A. nilagirica
    aerial parts
    essential oil (α-thujone, β-thujone, germacrene D, 4-terpineol, β-caryophyllene, camphene, borneol) Macrophomina phaseolina ED50 = 93.23 mg/L in vitro [41]
    Rhizoctonia solani ED50 = 85.75 mg/L
    Sclerotium rolfsii ED50 = 87.63 mg/L
    A. nilagirica
    leaves
    essential oil (α-thujone, borneol, β-thujone, 1,8-cineole) Phytophthora capsici 100% inhibition at 100 ppm in vitro [42]
    A. pallens
    leaves
    methanol extract 1:10 Sclerospora graminicola Inhibition of zoosporangium formation in vitro [43]
    A. parviflora
    twigs
    methanol extract 1:1 Sclerospora graminicola Inhibition of zoosporangium formation
    A. pontica
    fresh aerial parts
    essential oil
    (eucalyptol)
    Sclerotinia sclerotiorum MIC = 2400 μL/L in vitro [17]
    A. proceriformis
    fresh leaves
    essential oil
    (α-thujone)
    Aspergillus carbonarius MIC = 10.6 mg/mL in vitro [44]
    Aspergillus niger MIC = 21.2 mg/mL
    Fusarium graminearum MIC = 10.6 mg/mL
    F. verticillioides MIC = 10.6 mg/mL
    Septoria glycines MIC = 2.7 mg/mL
    Septoria tritici MIC = 2.7 mg/mL
    A. santonica
    fresh aerial parts
    essential oil
    (α-thujone)
    Sclerotinia sclerotiorum MIC = 2400 μL/L in vitro [17]
    A. scoparia
    aerial parts
    essential oil (acenaphthene,
    curcumene, (+) caryophyllene oxide, spathulenol, methyl eugenol, β-caryophyllene)
    Alternaria solani EC50 = 12.2 mg/mL in vitro
    agar diffusion
    [20]
    EC50 = 3.8 mg/mL in vitro
    spore germination
    A. sieberi
    aerial parts
    1R, 8S-dihydroxy- 11R,13-dihydrobalchanin Fusarium solani 6 mm inhibition zone at 200 μg/10 μL in vitro [45]
    11-epiartapshin 7 mm inhibition zone at 200 μg/10 μL
    3′-hydroxygenkwanin 8 mm inhibition zone at 200 μg/10 μL
    A. sieberi
    aerial parts
    essential oil (camphor, 1,8-cineole, camphene, chrysanthenone) Botrytis cinerea 100% inhibition at 1000 µl/L in vitro [46]
    A. stricta f. stricta
    aerial parts
    essential oil (capillene, spathulenol, β-caryophyllene) Aspergillus flavus, Aspergillus niger, Sporothrix schenckii MIC = 0.625 mg/mL in vitro [47]
    A. terrae-albae leaves camphor, 1,8-cineole, camphene, β-thujone Aspergillus carbonarius MIC > 1.20 mg/mL in vitro [48]
    Aspergillus niger MIC > 1.20 mg/mL
    Fusarium graminearum MIC = 0.60–1.20 mg/mL
    Fusarium verticillioides MIC = 0.60 mg/mL
    A. turanica
    aerial parts
    essential oil (1,8-cineol, cis-verbenyl acetate, camphor) Aspergillus niger 68.6% inhibition at 1 μL/mL in vitro [49]
    A. vulgaris
    whole plant
    crude methanol extract (1:10) Botrytis cinerea 60% inhibition at 2 mg/mL in vivo on
    Cucumis sativus
    [50]
    Blumeria graminis f. sp. hordei 25% inhibition at 2 mg/mL in vivo on
    Hordeum sativum
    Magnaporthe grisea 16% inhibition at 2 mg/mL in vivo on
    Oryza sativa
    Phytophthora infestans 32% inhibition at 2 mg/mL in vivo on Lycopersicon esculentum
    Puccinia recondita 52% inhibition at 2 mg/mL in vivo on
    Triticum aestivum
    Thanatephorus cucumeris 9.3% inhibition at 2 mg/mL in vivo on
    Oryza sativa
    A. vulgaris
    leaves
    methanol extract 1:1 Sclerospora graminicola Inhibition of zoosporangium formation in vitro [43]
    A. vulgaris
    fresh aerial parts
    essential oil (germacrene D) Sclerotinia sclerotiorum MIC = 2400 μL/L in vitro [17]
    * To highlight the active compounds, the major constituents of the volatile oils were noted in parentheses.
    The in vitro antifungal activity was frequently determined by the agar diffusion test, which involves placing the tested plant extract in wells or paper discs on the agar plate previously inoculated with the pathogen [24][25]. Since essential oils diffuse less in the culture medium, it was preferred to include them in agar after prior solubilization, followed by inoculation of the pathogen [20][31][42]. Moreover, for volatile compounds, the fumigation method was used [20]. In vivo antifungal evaluations involved treating the plants with the tested compounds/extracts by spraying them followed by inoculation with the fungal pathogen or by including the compounds in the soil and then planting the inoculated seedling in the treated soil. The disease severity was assessed after a period of infection [21][50]. In situ antifungal efficacy against postharvest pathogens was determined by fumigation in the case of stored foods [39][40].
    The extraction method influences the antifungal activity of the volatile oil, as can be seen from the investigation carried out by Julio et al. [18]: A. absinthium oil obtained by steam pressure extraction was more effective in inhibiting mycelium growth than that obtained by hydrodistillation, which was due to a different ratio of the major volatile compounds. Similarly, A. argyi essential oil obtained by simultaneous distillation–extraction had a higher antifungal activity compared to oils prepared by subcritical extraction or hydrodistillation. Although regardless of the extraction method, the oils had the same five major compounds, in the oil obtained by simultaneous distillation–extraction, the sesquiterpene compounds predominated [25]. Conversely, in the case of A. chamaemelifolia essential oil, the method of extraction—microwave-assisted hydrodistillation and classical hydrodistillation—had no influence on the inhibitory effect against the tested fungi. Both oils contained the same major compounds in comparable ratio [30].
    The type of extract, the part of the plant used, and the time of harvest also influence the antifungal activity, as underlined in a study carried out with methanol, ethanol, and hexane extracts of Artemisia annua against Aspergillus niger and A. flavus. Whole plant extract was the most efficient in inhibiting the growth of the two fungi, regardless of the type of extract, compared to root, leaf, or stem extracts. Regarding the extraction solvent, ethanol extract had the highest inhibitory effect, followed by methanol and hexane, on both fungal species. Although the harvesting period of the plant had little influence on the antifungal activity, most of the extracts made with the plant collected during anthesis were more active [22].
    From analyzing literature data, it appears that sesquiterpenes components of the oil have significant antifungal activity. Oxygenated sesquiterpenes were the major components of A. khorasanica volatile oil active against four soil-borne phytopathogenic fungi [37]. Artemisia scoparia essential oil, rich in sesquiterpenes, was more efficient in inhibiting mycelial growth and spore germination of Alternaria solani compared to A. lavandulaefolia and, especially, A. annua oils, where monoterpenes were the major compounds. Furthermore, the mode of volatile oil administration influences the outcome: A. lavandulaefolia oil was more effective when applied by fumigation than when mixed in the agar medium [20].
    Alongside the sesquiterpenes, it seems that thujones present in high amounts in the volatile oil are associated with intense antifungal activity [32][42]. To prove this point, Shafi et al. [42] used a mixture of thujones (α-thujone, β-thujone, and fenchone) at the same concentration instead of A. nilagirica oil to achieve the same result against Phytophthora capsici—100% inhibition. Borneol was also tested in the aforementioned study and showed no antifungal activity. On the other hand, the antifungal property of A. terrae-albae essential oil against Fusarium spp. was associated with the presence of camphor, 1,8-cineole, camphene, α- and β-thujone, borneol, and the high content of oxygenated monoterpenes [48]. Other oxygenated monoterpenes, piperitone and carvone, were correlated with the antifungal activity on Penicillium citrinum and Mucor rouxii; the two ketones are major components of A. herba-alba volatile oil [33].
    Some volatile compounds (L-camphor; DL-camphor, β-caryophyllene, and camphene) from A. annua oil were as efficient as synthetic antifungal products such as flutriafol and hymexazol against Fusarium oxysporum and F. solani, in vitro [21]. Different compounds isolated from the methanol extract of A. incisa were tested against Aspergillus flavus with various results: two monoterpenes and one phenolic acid derivative were more active compared to flavones and coumarins, the latter being less active [35].
    Moreover, the synergistic action of essential oils and chemical fungicides was evaluated. Thus, A. annua essential oil combined with flutriafol exhibits additive inhibitory effect against Fusarium solani, while with hymexazol, it manifests synergistic activity on F. solani and additive action on F. oxysporum [21].
    Most Artemisia extracts were tested on Fusarium, Alternaria, Aspergillus, and Penicillium species. Fungi have different susceptibility to varied antifungal compounds: for example, Fusarium solani was moderately sensitive to the action of isolated substances from A. sieberi (two sesquiterpene lactones and one methoxylated flavone), while Alternaria alternata and Aspergillus niger were resistant [45]. In an analogous manner, Aspergillus niger was sensitive to the methanol extract of A. campestris and resistant to A. vulgaris extract, despite similar quantities of flavonoids and phenolic compounds. Quercetin was reported in higher amounts in A. campestris extract and seems to be correlated with antifungal activity [28].
    Few studies assessed the antifungal activity in vivo. Ma et al. [21] showed that the petroleum ether extract of A. annua, imitating the composition of the essential oil, decreased the incidence of infected Panax notoginseng plants when added in the culture mixture. A. vulgaris crude methanol extract exhibited weak to moderate antifungal activity against Magnaporthe grisea, Thanatephorus cucumeris, Botrytis cinerea, Phytophthora infestans, Puccinia recondite, and Blumeria graminis when tested on plants grown in greenhouse conditions [50].
    Stored foods can be degraded by fungi such as Alternaria spp., Penicillium spp., and Mucor spp., which reduce their quality and make them unsuitable or even toxic for consumption. The use of chemical products for the control of postharvest pathogens endangers the environment, human health, and can induce resistance to fungicides. Such being the case, some investigations tried to estimate the reduction of postharvest fungal spoilage after treatment with Artemisia extracts. Fumigation of table grapes with A. nilagirica essential oil (200–300 µL) decreased the weight loss, berry shrinkage, and berry browning, increasing the shelf life for up to 10 days [39]. In addition, A. nilagirica volatile oil at a concentration of 1.4 μL/mL in airtight containers provided 71% protection from fungal contamination after 12 months of storage to millet grains [40].
    In addition to the direct inhibition of postharvest phytopathogenic fungi, some studies also evaluated the mycotoxins suppression ability of plant extracts. For instance, Artemisia herba-alba keto-rich essential oil completely inhibited the toxin production (penicillic acid, terrestric acid, brevianamide A, aurantiamine, xanthomegnin) for P. aurantiogriseum at 0.44% and for P. viridicatum at 0.22% [32]. Similarly, Artemisia nilagirica essential oil inhibited the production of aflatoxin B1 by Aspergillus flavus toxigenic strain at 1 µL/mL. A common seed contaminant, aflatoxin B1 is a powerful human carcinogen and a serious health risk; it also contributes to food deterioration by lipid peroxidation [40]. In another experiment, A. nilagirica volatile oil (0.16 µL/mL) completely inhibited the production of aflatoxin B1 by Aspergillus flavus and ochratoxin A by A. niger and A. ochraceus [39].
    The phytocompounds mechanism of action against fungi involves the inhibition of enzymes that control energy or structural compounds production, degeneration of fungal cell wall with loss of cytoplasm, and plasma membrane dysfunction. Due to their lipophilic nature, components of essential oils can penetrate cell walls, increase cellular membranes permeability and disturb the fungal cells metabolism, causing their death [11]. Monoterpenes delay sclerotic differentiation and promote the generation of lipid peroxides, which can lead to cell death, while phenols present in the essential oil bond to the active sites of fungal enzymes through their hydroxyl group [51]
    In addition, spore germination and germ tube growth are negatively influenced by terpenes from the essential oil. A. annua volatile oil arrested mycelia growth and conidia germination of Fusarium oxysporum and Fusarium solani [21]. Electron microscope observations proved that A. argyi essential oil affected the cell morphology and the structure of cell walls in Aspergillus niger [25]. An earlier study showed that Artemisia herba-alba essential oil inhibited mycelium growth, spore germination, and sporulation of Zygorrhynchus spp., Aspergillus niger and Penicillium italicum [52].
    The antifungal mode of action of A. nilagirica essential oil was investigated by Kumar et al. The fungal cells treated with 1.4 μL/mL volatile oil exhibited important deformity and shrinkage, detachment of plasma membrane from the cell wall, and development of lomasomes. At the same dose, A. nilagirica essential oil completely inhibited ergosterol synthesis in the cell membrane of Aspergillus flavus and provoked the leakage of Ca2+, K+, and Mg2+ ions from the cell [40].
    It is worth mentioning that in addition to the secondary antifungal metabolites produced by plants, certain endophytic organisms present in Artemisia species are able to inhibit the development of phytopathogenic fungi. Thus, in the root, stem, and leaves of A. argyi, researchers identified endophytes (Bacillus subtilis, B. cereus, Paenibacillus polymyxa) that produce substances capable of inhibiting the growth of the mycelium of Fusarium oxysporum, Magnaporthe grisea, and Alternaria alternata [53].

    2.2. Antibacterial Activity

    Only a small number of studies investigated the effect of Artemisia spp. extracts on phytopathogenic bacteria. For instance, different A. nilagirica leaves extracts were tested in vitro against four phytopathogenic bacteria, Erwinia spp., Clavibacter michiganense, Pseudomonas syringae, and Xanthomonas campestris, which cause diseases in potato, tomato, leafy greens, carrot, onion, and green pepper. The hexane extract was the most efficient in inhibiting all tested bacteria with MIC of 32 µg/mL. The ethanol, methanol, diethyl ether, and chloroform extracts were moderately active against the four bacteria, while the petroleum ether extract was the least effective [54]. Methanol, ethanol, and chloroform extracts from leaves of Artemisia parviflora (1:6 w/v) were almost ineffective against Xanthomonas vesicatoria and Ralstonia solanacearum, with inhibition zones of 1 and 2 mm [55].
    The essential oil of Artemisia turanica exhibited inhibitory activity at 2% (v/v) concentration against tumor galls induced by Agrobacterium tumefaciens on potato discs, but it did not demonstrate antibacterial activity in vitro against A. tumefaciens at the same dose [49]. In addition, the methanol extracts of roots, leaves, and flowers of Artemisia fragrans inhibited tumor growth in different percentages at 10, 100, and 1000 ppm. Leaves and flowers extract had the highest inhibition at all concentration (20, 38, 46%) compared to root extract (15, 24, 34%). No extract had any significant effect on the viability of A. tumefaciens when tested by agar diffusion assay [56].
    Dadasoglu et al. [57] evaluated the antibacterial activities of essential oils, hexane, chloroform, acetone, and methanol extracts from the aerial parts of A. santonicum, A. spicigera, and A. absinthium against 25 plant pathogenic bacterial strains. A. spicigera essential oil was only active (MIC = 500 μL/mL) against Erwinia amylovora, Pseudomonas syringae pv. syringae, and Xanthomonas axonopodis pv. vesicatoria. The volatile oil of A. absinthium exhibited moderate activity (MIC = 250–500 μL/mL) against most of the phytopathogenic bacteria. A. santonicum essential oil was the most effective with MIC values 125–250 μL/mL on 22 out of 25 bacteria tested, with the exception of Pseudomonas aeruginosa, P. cichorii, and Clavibacter michiganensis subsp. michiganensis. None of the Artemisia solvent extracts manifested antibacterial activity on the tested strains. The main constituents of A. absinthium oil were chamazulene, nuciferol butanoate, nuciferol propionate, and caryophyllene oxide, while A. santonicum and A. spicigera oil shared similar major components: camphor, 1,8-cineole, cubenol, borneol, terpinen-4-ol, and α-terpineol.
    In the previously mentioned study, some constituents isolated from the essential oils were evaluated individually for their antibacterial activity. Caryophyllene oxide, camphor, borneol, and 1,8-cineole did not show activity against the phytopathogenic bacteria. Terpinen-4-ol inhibited the growth of all tested bacteria with MIC values ranging from 60 to 110 μL/mL and linalool blocked the development of 22 bacterial strains with MIC values in the 50–110 μL/mL domain. α-Terpineol was active (MIC = 60–70 μL/mL) only on Pseudomonas cichorii, P. huttiensis, P. syringae pv. syringae, and Xanthomonas axonopodis pv. vesicatoria [57].
    The essential oil extracted from fresh leaves of Artemisia proceriformis manifested weak antimicrobial activity against four bacteria: Erwinia carotovora (MIC = 21.2 mg/mL), Pseudomonas corrugate (MIC = 21.2 mg/mL), Pseudomonas syringae (MIC = 5.31 mg/mL), and Xanthomonas vesicatoria (MIC > 42.5 mg/mL). The major component was α-thujone, in proportion of 66.9% [44].
    Terpenes and phenolic compounds found in the essential oils are responsible for the intense antimicrobial activity. Terpenes have the ability to increase membrane permeability by infiltrating the phospholipidic bilayer; the damage to the bacterial membrane causes the loss of cytoplasmic components, which leads to cell death. Plant extracts are studied not only as inhibitors of bacterial growth, but also for the prevention of biofilm formation. Such is the case of A. herba-alba, A. absinthium, and A. campestris essential oils that can reduce biofilm formation by up to 70% [58].

    2.3. Insecticidal Activity

    Insects are the more diverse group of animals on Earth, and only 0.5% are considered pests. Nonetheless, herbivorous insects destroy every year one-fifth of the world’s crop production. Synthetic chemicals used to control insect pests are toxic to humans, animals, and the environment through accumulation. In addition, the development of insecticide resistance and the migration of harmful insects require the search for an alternative for plant protection. Considering these facts, botanical insecticides represent a viable substitute with low toxicity toward humans and the environment [59].
    Plant-derived substances or plant extracts usually have a lower acute toxicity toward insects compared to synthetic insecticides. Nevertheless, their subacute toxicity was frequently noted and is important because it can limit insect spreading (diminished fertility, fecundity, vitality, or shorter lifespan) and decrease crop loss due to repellent, suppressant, or deterrent activity. These effects are generally called “antifeedant” and are manifested in insects by lower weight and body size, decreased fertility, and altered behavior [60].
    Artemisia compounds can influence insects by direct contact or fumigation, can repel insects or keep them from feeding, or can hinder their reproduction. Volatile compounds can induce toxicity to insects via inhalation or direct contact by forming an impermeable film on the cuticle leading to suffocation. Some volatile components can penetrate through the cuticle, affecting cellular membrane function and oxidative phosphorylation [61]. Phytochemicals such as cinnamyl alcohol, eugenol, and trans-anethole can activate octopamine receptors, interfering with the normal activity of octopamine, a neurotransmitter, neuromodulator, and neurohormone in an invertebrate system [62]. Furthermore, volatile compounds can interfere with the γ-aminobutyric acid (GABA) receptor in insects [14]. Other studies reported the inhibition of acetylcholinesterase by 1,8-cineole, (-)-citronellal, limonene, α-pinene, pulegone, and 4-terpineol [63] or inhibition of adenosinetriphosphatase by essential oils [64]. In addition, plant substances may cause the suppression of cytochrome P450 in insects (the enzymes responsible for phase I metabolism of xenobiotics) and may alter various biochemical processes, which shift the balance of the endocrine system [14].
    The activity of Artemisia compounds and extracts depends on the solvent used, the susceptibility of pest species to the active substance, the development stage of the insect, whether it is male or female, and the method of application. Table 2 lists the more recent studies on insecticidal activity of Artemisia genus. Essential oils and volatile compounds can be applied via fumigation, which is a procedure used frequently in the pest management of stored products. This method has obvious advantages such as the possibility to spread the substance evenly, even in unreachable places, and the ability to maintain an effective level of insecticides within a closed space [60]. Some of the shortcomings of natural insecticides are poor water solubility and rapid degradation in the environment, leading to low persistence and poor efficiency. To solve these problems, plant insecticides may be formulated as micro- and nanocapsules, nanoparticles, or nanoemulsions. These nanoformulations can increase the solubility, persistence, and stability of bioinsecticides, enhancing their activity and, at the same time, limiting their negative impact on the environment [65].
    Table 2. Insecticidal activity of Artemisia compounds and extracts.
    Artemisia spp. Extract or Compound Tested Target Species Reference
    A. absinthium essential oil Leptinotarsa decemlineata
    Myzus persicae
    Rhopalosiphum padi
    Spodoptera littoralis
    [18]
    essential oil Trialeurodes vaporariorum
    Tuta absoluta
    [66]
    essential oil Tetranychus cinnabarinus [67]
    essential oil Diaphania hyalinata [68]
    methanol extract Sitophilus oryzae [69]
    essential oil Orysaephilus surinamensis
    Tribolium castaneum
    [70]
    powdered plant Oryzaephilus surinamensis [71]
    water extract
    ethanol extract
    Hyphantria cunea [72]
    supercritical extracts Spodoptera littoralis [73]
    essential oil Myzus persicae [74]
    essential oil
    carvacrol
    (−)-α-bisabolol
    chamazulene
    Diaphorina citri [75]
    A. annua methanol extract
    essential oil
    Helicoverpa armigera [76]
    methanol extract
    artemisinic acid
    artemisinin
    scopoletin
    arteannuin-B
    deoxy-artemisinin
    artemetin
    casticin
    chrysosplenetin
    Helicoverpa armigera [77]
    essential oil Glyphodes pyloalis [78]
    methanol extract Pieris rapae [79]
    methanol extract Hyphantria cunea [80]
    methanol extract Glyphodes pyloalis [81]
    essential oil Diaphania hyalinata [68]
    A. arborescens essential oil Rhysopertha dominica [24]
    A. argyi ethanol extract Brevicoryne brassicae [82]
      essential oil Diaphania hyalinata [68]
    water extract
    ethanol extract
    Hyphantria cunea [72]
    essential oil Plodia interpunctella [83]
    A. frigida essential oil Liposcelis bostrychophila
    Sitophilus zeamais
    [84]
    essential oil
    terpinen-4-ol
    verbenone
    camphene
    α-terpineol
    α-terpinyl acetate
    Lasioderma serricorne
    Liposcelis bostrychophila
    Tribolium castaneum
    [85]
    A. herba-alba essential oil Orysaephilus surinamensis
    Tribolium castaneum
    [70]
    A. judaica essential oil Sitophilus orizae [64]
    A. lavandulaefolia essential oil
    1,8-cineole
    chamazulene
    β-caryophyllene
    Lasioderma serricorne [86]
    A. monosperma essential oil Sitophilus orizae [64]
    essential oil Aphis nerii [87]
    A. nilagirica cow urine extract Scirpophaga incertulas [88]
    A. spicigera essential oil Dendroctonus micans [89]
    A. vulgaris essential oil Callosobruchus maculatus
    Rhyzopertha dominica
    Tribolium castaneum
    [90]
    essential oil Diaphania hyalinata [68]
    water extract
    ethanol extract
    Hyphantria cunea [72]

    2.4. Nematicidal Activity

    Plant parasitic nematodes cause severe yield losses in different crops, especially in tropics and subtropics. Frequent nematodes that affect plants include Meloidogyne (root-knot nematodes), Pratylenchus (lesion nematodes), Xiphinema (dagger nematodes), Aphelenchoides (foliar nematodes), Globodera (potato cyst nematodes), and Heterodera (soybean cyst nematodes). Meloidogyne species induce histological damages to roots, with the appearance of visible galls. Some phytoparasitic nematodes act as vectors for plant viruses, such as Xiphinema species [91].
    Various Artemisia species were evaluated for nematicidal activity, some with promising results. For instance, A. judaica essential oil (1 μL/L) caused 85% mortality on Meloidogyne javanica second-stage juveniles and inhibited the hatching of eggs. The main component of the essential oil was artemisia ketone. In the same study, A. arborescens and A. dracunculus essential oils were poorly active on the root-knot nematode [92]. In vitro toxicity of Artemisia annua essential oil was evaluated against second-stage juveniles of Meloidogyne incognita and pre-adults of Rotylenchulus reniformis (reniform nematode). Concentrations of 500 and 250 ppm induced 100% mortality in both nematode species [93]. Moreover, there are reports of nematicidal activity exhibited by the alcoholic and aqueous extracts of Artemisia annua against Meloidogyne incognita and Pratylenchus loosi (tea root lesion nematode) [91].
    Artemisia herba-alba essential oil produced 94.4% mortality on Meloidogyne incognita second-stage juveniles at 15 µg/mL and 100% mortality on Xiphinema index females at 2 µg/mL, after 24 h exposure. However, mixed-age infective specimens of Pratylenchus vulnus were more resistant to the activity of A. herba-alba essential oil with mortality values ranging from 56.8% to 67% after 24 to 96 h of exposure. The major components of the essential oil were cis- and trans-thujone, camphor, 1,8-cineole, trans-chrysantenyl acetate, and camphene. In an additional test, the three nematode species were exposed to various compounds of the essential oils of four plants, including A. herba-alba. Borneol and α-pinene manifested poor to moderate activity, while limonene lack activity on the three nematode species. Camphor exhibited a moderate nematicidal effect, whilst thymol and thujone (mixture of cis-thujone, 70% and trans-thuione) displayed strong activity against M. incognita, and less so on P. vulnus and X. index. The fact that the activity of the components of the volatile oil is weaker than that of the whole oil suggests a possible synergistic action of the mixture. In addition, soil treatments with 100 or 200 µg/kg A. herba-alba essential oil, by fumigation or application of water solution, significantly inhibited nematode density on tomato roots and in soil and also increased the plant biomass. Fumigation was proven to be more effective than drenching treatment [94].
    A. absinthium essential oil (β-thujone 51% and linalyl acetate 24%) had over 99% mortality rate at 0.25 and 0.5% concentrations (v/v) against Meloidogyne javanica juveniles in an in vitro test. Furthermore, in vivo experiments were conducted in order to assess the ability of the essential oil to inhibit root-knot nematode development after being absorbed by the tomato plants. It was observed that spraying the oil on tomato leaves actually increased the number of galls and eggs in treated plants, and applying the essential oil into the soil at 0.25% and 0.5% concentrations did not lower the number of galls or nematode eggs in tomato plants. The authors believe that the nematicidal compounds could have been volatilized or degraded by microorganisms in the soil or by the plant, or possibly, the root exudates were modified by the absorbed essential oil, making the tomato plants more appealing to the nematodes [95]. In another study, commercially available A. absinthium volatile oil had only a slight effect on Meloidogyne javanica in vitro (the median lethal dose LC50 of 937 µg/mL at 48 h and 734 µg/mL at 72 h). The major components of the oil were borneol acetate, β-terpineol, 1,8-cineol, linalool, sabinene, and o-cymene [96].
    The nematicidal activity of Artemisia absinthium hydrolate, a by-product of essential oil extraction, was evaluated on the root-knot nematode, Meloidogyne javanica. The hydrolate caused high mortality of second-stage juvenile and suppression of egg hatching, proving the ability of the A. absinthium hydrolate to penetrate the gelatinous matrix of eggs. In vivo tests showed a strong inhibition of juveniles’ penetration in the tomato roots. Soil treatment with A. absinthium hydrolate (60% and 20% concentrations) significantly reduced the reproductive capacity of root-knot nematode and the infection frequency. The main component of the hydrolate, responsible for the nematicidal activity, was identified as (5Z)-2,6-dimethylocta-5,7-dien-2,3-diol [97].
    Kalaiselvi et al. [98] showed that essential oils of A. nilagirica plants collected from high and low altitude have different composition and different nematicidal activity against Meloidogyne incognita (LC50/48h of 5.75 and 10.23 μg/mL, respectively). α-thujone, α-myrcene, and linalyl isovalerate were the main components of high-altitude A. nilagirica volatile oil, while the low-altitude plants produced an oil composed mostly of camphor, caryophyllene oxide, eucalyptol, humulene epoxide II, α-humulene, and β-caryophyllene. Experiments carried out in vivo by soil irrigation with the essential oil revealed that both volatile oils significantly reduced the infection of tomato plant (number of nematode juveniles and eggs) and enhanced plant growth (fresh weight of aerial parts and roots) at 20 µg/mL. Again, the effect was greater for the oil originated from high-altitude A. nilagirica. Moreover, the ethanol extract of flowering parts of A. nilagirica (1 mg/mL) exhibited nematicidal activity against Meloidogyne incognita, as reported by an earlier study [99].
    Various hypotheses have been advanced as explanations for the nematicidal effects of essential oils: disruption of cell membrane permeability and obstruction of its functions, irreversible modifications of proteins structures from the nematode surface induced by aldehydes, inhibition of acetylcholinesterase with build-up of neurotransmitter in the central nervous system of the nematode followed by convulsion, paralysis, and death [11]. Research on A. nilagirica essential oil ascribe the nematicidal action to an increased generation of intracellular reactive oxygen species, activation of signaling pathway of apoptosis, and DNA damage prompting cell death [98].
    In addition to the essential oils and their volatile compounds, few other substances from Artemisia genus have been tested for their activity against plant nematodes. Thirteen chemical compounds (apigenin, bonanzin, nepetin, dihydroluteolin, scopoletin, isoscopoletin, benzoic acid, β-sitosterol, γ-sitosterol, betulinic acid, friedelin, linoleic acid, and a long chain ketone) isolated from Artemisia elegantissima and Artemisia incisa were tested in vitro and in vivo for nematicidal activity against M. incognita. All phytochemicals significantly inhibited egg hatching and induced high mortality of second-stage juveniles at the tested concentrations (0.1, 0.2, and 0.3 mg/mL). Isoscopoletin was even more effective than the positive control carbofuran. In addition, application of the compounds as a root drench (0.1 mg/mL) on potted tomato plants caused a marked reduction of galls, galling index, and egg masses on plant roots, numbers of juveniles in the rhizosphere soil, and also improved tomato plant growth parameters (shoot and root length and weight). Isoscopoletin and apigenin were the most active compounds [100].

    2.5. Herbicidal Activity

    One of the most influential groups of plant secondary metabolites is the allelochemicals. They are released into the environment in order to affect the germination, growth, behavior, survival, and reproduction of competing plants, which is a process better known as allelopathy. They are produced mainly in the plant’s roots, seeds, flowers, and leaves, and their synthesis depends on the changes of the climate conditions as well as exposure to biotic or abiotic stress. Allelochemicals activity can be harmful or beneficial for the growth and survival of target species [101]. The destructive effect of allelochemicals is crucial for defending plants against herbivores and providing an advantage in the competition for resources [102]. In agroecosystems, allelopathy can influence weed management, and plant allelochemicals could be employed as bioherbicides in order to reduce the negative impact of chemical herbicides on the environment [103].
    The allelopathic properties of Artemisia species are well known [104][105][106][107][108][109][110], so it was expected that numerous studies would investigate their herbicide potential on various weeds. Most researchers focused on the volatile oils, and only a few dealt with aqueous or alcoholic extracts (Table 3). The phytotoxic effect of essential oils is owed to multiple mechanisms of action: inhibition of cell division, decrease of mitochondrial respiration, reduction of photosynthetic pigments and photosynthesis, generation of radical oxygen species in excess and oxidative impairment, destruction of waxy cuticular layer, inhibition of enzymes activity, water uptake, and alteration of gibberellic acid content [102][111][112]. Most of these actions are correlated with the presence of oxygenated monoterpenes. For example,1,8-cineole and camphor inhibit DNA synthesis, cell proliferation, and elongation [113].
    Table 3. Phytotoxic activity of Artemisia compounds and extracts.
    Artemisia
    Species
    Extract * or Compound Tested Weed/Target Plant Observed Effect Reference
    A. absinthium
    aerial parts
    essential oil
    (cis-epoxyocimene, (−)-cis-chrysanthenol, chrysanthenyl acetate, linalool and β-caryophyllene)
    Lolium perene Suppression of root and leaf growth
    No effect on seed germination
    [18]
    Lactuca sativa Suppression of root and leaf growth
    No effect on seed germination
    A. absinthium
    fresh aerial parts
    essential oil
    (β-thujone, chamazulene)
    Sinapis arvensis Complete inhibition of seed germination and seedling growth at 2 µL/mL [114]
    A. absinthium
    leaves
    aqueous extract
    1:10 w/v
    Parthenium hysterophorus Inhibition of seed germination, shoot and root growth, reduction of chlorophyll and carotenoid content, at 25, 50, 75, and 100%
    Enhanced malondialdehyde levels, phenolic content and increased activity of antioxidative enzymes, at 25, 50, 75, and 100%
    [105]
    A. absinthium
    shoot and root
    aqueous extract Chenopodium album Decreases growth criteria (root and shoot length and fresh weight, number of leaves) at 1–100 mg/mL
    No effect on seed germination
    Increased peroxidase and superoxide dismutase activity in root
    [115]
    A. afra
    leaves
    aqueous extract Triticum aestivum No effect on seed germination [116]
    Brassica napus Complete inhibition of seed germination
    Medicago sativa Increased germination rate
    resistant and non-resistant Lolium spp. Significant inhibition of seed germination
    A. annua
    flower heads
    essential oil
    (1,8-cineole, trans-sabinyl acetate, artemisia ketone, camphor α-pinene)
    Amaranthus retroflexus In vitro, complete inhibition of seed germination, at 10 and 100 µg/L
    In vivo, plant death, at the cotyledon stage (100 mg/L) and true leaf stage (1000 mg/L)
    [117]
    Setaria viridis In vitro, complete inhibition of seed germination, at 100 µg/L
    In vivo, plant death, at the cotyledon stage (100 mg/L) and true leaf stage (1000 mg/L)
    A. annua
    aerial parts
    artemisinin
    arteannuin B
    artemisinic acid
    Secale cereale, Hordeum vulgare, Artemisia annua, Portulaca oleracea, Amaranthus blitun, Lactuca sativa, Raphanus sativus Inhibition of seed germination
    Inhibition of shoot and root growth
    [118]
    A. annua artemisinin Lactuca sativa Inhibition of root and shoot elongation, reduced cell division and cell viability in root tips, at 10 µM
    Reduced chlorophyll a and b levels
    Increased malondialdehyde and proline levels, at 1 µM
    [119]
    A. annua artemisinin Arabidopsis thaliana Reduction of fresh biomass, chlorophyll a, b, and leaf mineral contents at 40–160 μM
    Reduction of photosynthetic efficiency, yield, and electron transport rate, calcium and nitrogen levels at 80 and 160 μM
    Elevated lipid peroxidation (malondialdehyde contents) at 80 and 160 μM
    [120]
    A. arborescens
    shoot
    sesamin
    ashantin
    Agrostis stolonifera,
    Lactuca sativa
    Growth inhibition at 1 mg/mL [107]
    sesamin Lemna paucicostata Growth inhibition IC50 = 401 μM
    ashantin Lemna paucicostata Growth inhibition IC50 = 224 μM
    A. arborescens
    leaf litter
    crude methanol extract Lactuca sativa, Raphanus sativus, Amaranthus retroflexus, Cynodon dactylon Inhibition of seed germination
    ED50 = 1.61–3.05 mg/mL
    Inhibition of root growth
    ED50 = 1.22–3.14 mg/mL
    [121]
    hexane, chloroform,
    and ethyl acetate fractions
    Inhibition of seed germination
    ED50 = 1.19–6.25 mg/mL
    Inhibition of root growth
    ED50 = 0.92–3.98 mg/mL
    A. arborescens
    aerial part
    crude methanol and aqueous extracts Lactuca sativa Inhibition of seed germination and root growth
    ED50 = 0.5–2.8 mg/mL
    [122]
    ethyl acetate, n-hexane,
    chloroform, n-butanol fractions
    Inhibition of seed germination and root growth
    ED50 = 0.4–5.4 mg/mL
    A. argyi
    leaves
    water extract (caffeic acid, schaftoside, 4-caffeoylquinic acid, 5-caffeoylquinic acid, 3,5-dicaffeoylquinic acid and 3-caffeoylquinic acid) Brassica pekinensis, Lactuca sativa, Oryza sativa Inhibition of germination, root and stem growth, and biomass (at 50, 100, and 150 ng/mL) [108]
    Brassica pekinensis, Lactuca sativa, Oryza sativa, Portulaca oleracea, Oxalis corniculata, Setaria viridis Inhibition of germination and growth in pot experiment (A. argyi powder mixed into sand soil at the ratio 100:0, 100:2, 100:4, and 100:8)
    A. campestris
    leaves
    essential oil
    (β-pinene, 1, 8-cineole, p-cymene, myrcene)
    Daucus carota, Cicer arietinum, Phaseolus vulgaris, Triticum sativum Reduces seed germination at 1000–2000 ppm
    Enhances seed germination at 100 ppm
    Delays the germination of D. carota seeds
    [123]
    A. dracunculus
    aerial parts
    essential oil Medicago minima, Rumex crispus, Taraxacum officinale No effect on seed germination at 0.3–1.2 mg/L [124]
    A. dracunculus leachate Lactuca sativa Radicle growth inhibition [125]
    A. fragrans
    aerial parts
    essential oil
    (α-thujone, camphor, 1,8-cineole, β-thujone)
    Convolvulus arvensis Important reduction in the shoot, root, and plant length, shoot and root fresh weight, shoot and root dry weight
    Inhibited seed germination
    Significant decrease of photosynthetic pigments and antioxidant enzymes
    Increased production of H2O2 and malondialdehyde content, and membrane leakage
    [126]
    A. fragrans
    roots, leaves, and flowers
    methanol extracts Raphanus raphanistrum Inhibition of root growth at 1000 ppm
    Inhibition of seed germination at 7500 ppm
    [56]
    A. frigida volatile organic compounds
    (1,8-cineole, camphene, (E)-3-hexen-1-ol acetate, α-terpineol, β-terpineol)
    Melitotus suaveolens, Sorghum sudanense, Elymus dahuricus, Agropyron cristatum Significantly decreases the seed germination and seedling growth [127]
    A. judaica
    aerial parts
    essential oil
    (piperitone, 3-bornanone)
    Lactuca sativa Reduced seed germination, shoot and root growth at 250–1000 µL/L [36]
    A. lavandulaefolia
    leaves
    aqueous extract Lactuca sativa, Artemisia princeps, Achyranthes japonica, Oenothera odorata, Plantago asiatica, Aster yomena, Elsholzia ciliata, Raphanus sativus Inhibition of root growth
    Inhibition of seed germination
    [128]
    essential oil
    (1,8-cineole, α-terpineol, α-terpinene, camphor, azulene, 2-buten-1-ol)
    A. monosperma
    aerial parts
    aqueous extract Phaseolus vulgaris Stimulation of seed germination at 1% and 2% concentration
    Inhibition of seed germination at 3% and 4% concentration
    Inhibition of amylase and protease activity
    [129]
    A. monosperma
    aerial parts
    aqueous extract Medicago polymorpha Reduction of germination percentage, plumule and radicle growth, and seedling dry weight [130]
    crude plant powder mixed with clay loam soil Inhibitory effects on leaf area index,
    total photosynthetic pigments, total available carbohydrates and total protein, in pot culture bioassay
    A. scoparia
    fresh leaves
    essential oil
    (β-myrcene, (+)-limonene, (Z)-β-ocimene, γ-terpinene)
    Avena fatua, Cyperus rotundus, Phalaris minor Important reduction in germination, seedling growth, and dry matter at 0.07–0.7 mg/mL [131]
    A. scoparia
    fresh leaves
    essential oil
    (p-cymene, β-myrcene, (+)-limonene)
    Achyranthes aspera, Cassia occidentalis, Parthenium hysterophorus, Echinochloa crus-galli, Ageratum conyzoides Inhibition of seed germination, root and shoot growth at 10, 25, and 50 µg oil/g sand
    Chlorosis, necrosis and complete wilting of plants 1 to 7-days after spraying with oil (2%, 4%, and 6%, v/v)
    Significant decline in chlorophyll content and cellular respiration, electrolyte leakage
    [132]
    A. sieversiana
    fresh aerial parts
    essential oil
    (α-thujone, eucalyptol)
    Amaranthus retroflexus, Medicago sativa, Poa annua, Pennisetum alopecuroides Inhibition of root and shoot growth
    IC50 = 1.89–4.69 mg/mL
    [133]
    α-thujone IC50 = 1.55–6.21 mg/mL
    eucalyptol IC50 = 1.42–17.81 mg/mL
    α-thujone and eucalyptol mixture IC50 = 0.23–1.05 mg/mL
    A. terrae-albae
    aerial parts
    essential oil
    (α-thujone, β- thujone, eucalyptol, camphor)
    Amaranthus retroflexus Reduces root and shoot growth at 1.5 μg/mL
    Completely inhibits seed germination at 3 μg/mL
    [134]
    Poa annua Reduces root and shoot growth at 1.5 μg/mL
    Completely inhibits seed germination at 5 μg/mL
    A. verlotiorum
    flower heads
    essential oil
    (chrysanthenone,
    1,8-cineole, β-pinene, camphor
    2,6-dimethyl phenol, β-caryophyllene)
    Amaranthus retroflexus In vitro, complete inhibition of seed germination, at 10 and 100 µg/L
    In vivo, plant death, at the cotyledon stage (100 mg/L) and true leaf stage (1000 mg/L)
    [117]
    Setaria viridis In vitro, inhibition of seed germination, at 10 and 100 µg/L
    In vivo, plant death, at the cotyledon stage (1000 mg/L) and true leaf stage (1000 mg/L)
    A. vulgaris
    aerial parts
    aqueous extract Amaranthus retroflexus Inhibition of seed germination, radicle, and hypocotyl length at 7.5% to 10% w/v, in Petri dish bioassays
    Inhibition of seedling emergence and plant growth, in pot culture bioassays
    [104]
    Zea mays Stimulation of radicle and mesocotyl growth at 7.5% to 10% w/v, in Petri dish bioassays
    Stimulation of plant biomass, in pot culture bioassays
    A. vulgaris
    leaves and flowers
    essential oil Agrostemma githago, Amaranthus retroflexus, Cardaria draba, Chenopodium album, Echinochloa crus-galli, Reseda lutea, Rumex crispus, Trifolium pratense Inhibition of root and shoot growth and reduction of germination rate (at 2, 5, 10 and 20 μL/plate) [135]
    A. vulgaris
    root
    aqueous extracts Triticum aestivum
    (winter wheat)
    Inhibition of shoot and root growth by all concentrations (1:6250 to 1:10) [136]
    Brassica napus spp. oleifera var. biennis
    (winter oilseed rape)
    Significant inhibition of germination at the 1:10 concentration
    A. vulgaris
    aerial parts
    Significant inhibition of root growth at 1:10 concentration
    Stimulation of shoot growth
    * To highlight the active compounds, the major constituents of the volatile oils were noted in parentheses.
    Artemisia fragrans essential oil inhibited seed germination and growth of Convolvulus arvensis at 1–4% concentration in a Petri dish and pot experiment. It significantly reduced the level of photosynthetic pigments (chlorophyll a, chlorophyll b, and carotenoids) and of antioxidant enzymes (catalase, peroxidase, ascorbate peroxidase, superoxide dismutase), as well as enhancing the production of hydrogen peroxide and malondialdehyde. It seems that volatile oil compounds—mostly oxygenated monoterpenes—inhibited the electron transport chain and affected the process of photosynthesis, leading to an increased production of oxygen reactive species. In turn, these intensified the lipid peroxidation of the cell membrane followed by electrolyte leakage [126].
    Oxygenated monoterpenes were the major ingredients of Artemisia sieversiana essential oil (α-thujone 64.46% and eucalyptol 10.15%) that suppressed seedling growth of Amaranthus retroflexus, Medicago sativa, Poa annua, and Pennisetum alopecuroides. The experiment showed that the mixture of the major constituents, in the same ratio as found in the oil, was more phytotoxic compared to each individual compound, indicating a possible synergistic effect of α-thujone and eucalyptol [133].
    Although oxygenated monoterpenes were the major constituents of A. judaica essential oils obtained by hydro-distillation and microwave-assisted extraction, the oil extracted by hydro-distillation exhibited greater phytotoxicity on Lactuca sativa seed germination and plant growth [36], showing that the extraction method impacts the phytotoxic activity of volatile oils.
    Major constituents of A. terrae-albae essential oil were tested on seed germination, root and shoot growth of Poa annua and Amaranthus retroflexus. The phytotoxic effect of α-thujone, eucalyptol, camphor, and the mixture of these compounds was inferior to that of the essential oil, which suggests that probably other volatile components are causing the herbicidal activity of the oil [134]. α-Terpinen and β-pinene, compounds of A. lavandulaefolia essential oil, exhibited strong phytotoxic activity on seed germination test against eight target plants (Table 3), whereas β-caryophyllene and myrcene only inhibited Achyranthes japonica seed germination [128].
    Artemisia scoparia essential oil inhibits germination and plant growth through the production of oxidative stress related to membrane disruption, increased lipid peroxidation, and buildup of hydrogen peroxide. It also interferes in cellular respiration and photosynthesis processes [132].
    Field experiments in Triticum aestivum used pre-emergence application of Artemisia vulgaris aqueous extract (20% w/v) together with chlorsulfuron. This treatment permitted lowering the dose of the herbicide up to 80%, while manifesting an inhibitory effect of 70% against Lolium multiflorum [137]. Another field trial demonstrated that A. argyi water extract markedly suppressed the growth of weeds in Chrysanthemum morifolium field with no adverse effect on the growth of C. morifolium. The investigations showed that A. argyi inhibited weed growth and germination through inhibition of chlorophyll synthesis and photosynthesis [108]. Conversely, field treatment of Triticum turgidum L. subsp. durum Desf. with A. absinthium aqueous extract exerted a stimulating effect on weed presence and reduced wheat growth and yield [106].
    The sensitivity of different weed species to a certain herbicide varies greatly. Among eight weeds tested in a study, Amaranthus retroflexus, Echinochloa cruss-galli, and Reseda lutea were more susceptible to the action of A. vulgaris essential oil, compared to Rumex crispus, Agrostemma githago, Trifolium pretense, Chenopodium album, and Cardaria draba, which were more resistant [135]. Similarly, Parthenium hysterophorus and Ageratum conyzoides were more vulnerable to the inhibitory effect of Artemisia scoparia volatile oil, in comparison with Cassia occidentalis, under laboratory conditions. In another test, Echinochloa crus-galli and Parthenium hysterophorus were more affected by post-emergence application of the oil [132].
    The phytotoxicity of isolated compounds from Artemisia annua was evaluated against two monocots and five dicots (Table 3). The suppression of germination and seedling growth varies in the order: artemisinin>arteannuin B>artemisinic acid. Raphanus sativus was the most resistant to the action of tested compounds, followed by Secale cereale. The weaker activity of arteannuin B and artemisinic acid—molecules without an endoperoxide bridge—implies that the moiety is important for the phytotoxic effect [118]. Artemisinin reduces many physiological and biochemical processes in the target plant and affects mitosis by inhibiting microtubules formation [120][138].
    The incorporation of artemisinin into soil inhibited the growth of above-ground lettuce plants, with EC50 = 2.5 mg/Kg sandy soil, but the germination was not arrested up to 100 mg/Kg soil [139]. Furthermore, adding A. annua leaves containing 0.81–0.22% artemisinin in soil led to the inhibition of Zea mays growth [140]. Artemisinin is phytotoxic in concentrations comparable to those of commercial herbicides and has a good activity in soil [110].
    In vivo tests proved that artemisinin is a potent suppressor of photosynthetic activity through the formation of a highly reactive artemisinin-metabolite that is able to inhibit the photosynthetic electron flow [141]. Other investigations showed that artemisinin enhances the generation of radical oxygen species and lipid peroxidation, which leads to cell death and arrest of mitotic phases in Lactuca sativa seedlings [119]. When added to the culture medium of Arabidopsis thaliana seedlings, artemisinin (1, 2, 5, 20, 100 µM) reduced the root gravitropic responses, elongation of primary and lateral roots, root hairs density, and length. Furthermore, artemisinin diminished starch grain and auxin concentrations and affected auxin redistribution in root tips [142].

    2.6. Activity on Non-Target Organisms

    Since biopesticides and bioherbicides are of natural origin, they are considered to be less harmful to the environment and the health of applicators and consumers. Usually, plant-based formulations are mixtures of compounds, and they do not consist of a single substance, which should prevent resistance in target organisms. In addition, some phytochemicals are rapidly degraded in nature, so there is no risk of their accumulation in the environment, as is the case with chemical pesticides. Consequently, plant-based pesticides and herbicides are regarded as generally safe. Still, these products can affect the non-target organism directly or indirectly by influencing biodiversity and species interactions, so it is imperative to assess their safety [13][143].
    Little information is available regarding the ecotoxicity of Artemisia compounds and extracts. Pino-Otin et al. [13] evaluated the toxicity of hydrolate and organic extracts from A. absinthium on three aquatic ecotoxicity indicator organisms: an invertebrate (Daphnia magna), a marine bacterium (Vibrio fisheri), and a unicellular freshwater alga (Chlamydomonas reinhardtii). The wormwood hydrolate, a by-product of essential oil extraction, is a promising biopesticide with nematicidal effect due to (5Z)-2,6-dimethylocta-5,7-dien-2,3-diol [97]. A. absinthium hydrolate caused acute toxicity on non-target organisms: D. magna (LC50 = 0.236%) > V. fisheri (LC50 = 1.85%) > C. reinhardtii (LC50 = 16.49%). Moreover, the wormwood ethanol extract was highly toxic to D. magna (LC50 = 0.093 mg/L). However, the effect of wormwood hydrolate on a river microbial community, composed mainly of Proteobacteria, was negligible, causing only small changes in metabolic diversity and a slight inhibition of bacterial growth. It is possible that natural freshwater microbial populations are more resistant to 2,6-dimethylocta-5,7-diene-2,3-diol action because of the modified bioavailability of compounds in the river water and particular sensitivity of the various microbial species [13].
    The same A. absinthium hydrolate was tested on non-target soil organisms: natural microbial communities, the earthworm Eisenia fetida, and the plant Allium cepa. The hydrolate was toxic in low concentrations: it caused substantial inhibition of onion root growth (LC50 = 3.87% v/v), high mortality of the earthworm E. fetida (LC50 = 0.07 mL/g), and decreased bacterial metabolism (LC50 = 25.72% v/v after 1 day of exposure). All these effects were exhibited at inferior concentrations than those needed to contain the target organism. Probably, 2,6-dimethylocta-5,7-diene-2,3-diol is able to penetrate biological membranes and thus affect the survival and metabolic processes of soil organism from different trophic levels [13].
    The methanol extracts of Artemisia fragrans manifested significant toxicity in the brine shrimp (Artemia salina) lethality assay, with ED50 = 19.7 ppm for the root extract and ED50 = 11.99 ppm for flowers and leaves extract [56]. In another study, the aqueous extracts from Artemisia ordosica leaves were tested on two algae from the biological soil crusts, Chlorella vulgaris and Nostoc spp. The less concentrated extract (1 g/L) stimulated C. vulgaris growth but did not significantly affect Nostoc spp., indicating that C. vulgaris might utilize the sugars and other carbon sources in the extract to promote self-growth. The highly concentrated extract (5 and 10 g/L) inhibited the growth of both algae [109].
    The safety profile of the Artemisia nilagirica essential oil was determined in terms of mammalian toxicity on male mice (Mus musculus) and millet (Eleusine coracana) seeds viability. The essential oil showed low toxicity on mice (LD50 = 7528.10 µL/kg) and no effect on millet seed germination. Thus, the oil is suitable as a food preservative for both consumption and sowing purposes [40]. More so, Artemisia nilagirica essential oil did not cause any significant changes in the physicochemical and sensory properties of table grapes when applied by fumigation on the fruits [39].
    Artemisia absinthium essential oil, a potential biopesticide, was evaluated for toxicity against non-target organisms: the honey bee (Apis mellifera) and tomato plant (Solanum lycopersicum). Honeybee toxicity (EC50 = 0.26 mg/cm2) is reached at lower concentrations of A. absinthium oil than the ones necessary for controlling the leaf miner Tuta absoluta (EC50 = 0.5 mg/cm2), but not at rates needed to control the whitefly Trialeurodes vaporariorum (EC50 = 0.08 mg/cm2). A similar phenomenon was noted for the phytotoxic effect on tomato; seed germination and root growth were inhibited at oil concentrations needed to control the leaf miner, but not the whitefly [66].
    Investigations to date have shown that biopesticides derived from Artemisia are most likely to have some toxicity toward non-target organisms, and further studies are needed to assess the risk in natural communities in order to ensure the safe use of biopesticides in agricultural practices.
    Choosing the right formulation can reduce toxicity as well as increase the stability and effectiveness of Artemisia biopesticides. For instance, terpenoids are lipophilic, volatile, and thermolabile compounds that are easily oxidized or hydrolyzed, so they can be affected during extraction, storage, and transport. Furthermore, after application onto plants, they volatilized quickly and start degrading, leading to short persistence and low efficacy in the field. These drawbacks can be overcome by a suitable formulation through encapsulation or nanoparticles synthesis. A product formulation is a homogeneous and stable mixture of components put together according to a specific procedure with the purpose of increasing the biological activity, stability, persistence, and efficiency, while decreasing the toxicity of the product. The selected formulation depends on the intended use and mode of application, the targeted phytopathogen, and the degradation factors present in the ecosystem [16].

    The entry is from 10.3390/molecules26103061

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