Ailanthus altissima as a Source of Natural Pesticides: Comparison
Please note this is a comparison between Version 3 by Beatrix Zheng and Version 2 by Beatrix Zheng.

The extensive use of pesticides may negatively affect human health. Additionally, it is one of the main reasons for the decline of pollinators and is thus a hazard for most crops and biodiversity as a whole. Good candidates for the replacement of pesticides with ones less toxic to humans and pollinators are natural products (bioactive compounds extracted from plants), even though it should be kept in mind that some of them can be toxic too. Ailanthus altissima (Mill.), swingle, known also as tree of heaven, (Simaroubaceae) is one of the most aggressive alien invasive plants. It demonstrates a high tolerance to various habitat conditions and a potent propagation ability. This plant has a prominent ability to suppress the seed development of local vegetation.

  • biopesticides
  • essential oils
  • quassinoids
  • invasive plants’ management

1. Ethnobotanical Data about Ailanthus altissima (Mill.) Swingle

Ethnobotanical information is usually focused on the medicinal properties of plants. Therefore, information regarding the pesticide potentials of plants is valuable but scarce. For invasive plant species, ethnobotanical records are collected in their native ranges of distribution. The local human populations in these regions have established traditions in the application of such plants. The bark of Ailanthus altissima (臭椿 chou chun) was initially recorded in Xin Xiu Ben Cao, a renowned traditional Chinese medicine monograph [1]. The information within this book relates that besides the many others therapeutic effects of A. altissima, the bark of the plant was used as an insecticide [1]. A. altissima plant materials were often used in ancient China against insect predators of stored grains [2]. The traditional use of A. altissima in Chinese medicine represents the starting point for scientific research seeking evidence of such pharmacological activities, and in this particular case, its potential pesticidal effects.

2. Chemical Constituents of Ailanthus altissima and Extraction Methods

A. altissima contains various secondary metabolites such as alkaloids, terpenoids, flavonoids, essential oil, etc., with a wide range of pharmacological effects such as anti-cancer, anti-inflammatory, anti-protozoal, etc. [1][3][4][5][6][7][8][9][10][11][12][13][14][15]. For instance, extracts of A. altissima stems containing ailanthone possess antiplasmodial activity against Plasmodium falciparum P. berghei [16][17]. An interesting new discovery is the antifungal effect of the alkaloid canthin-6-one isolated from A. altissima against Fusarium oxysporum f. sp. cucumerinum [18].
Here the researchers focus on the quassinoids and essential oils as potential biopesticides since there is an indication that these groups of compounds have such effects [19][20][21][22][23][24][25][26][27][28].

3. Essential Oil of Ailanthus altissima: Composition and Extraction Overview

The qualitative and quantitative compositions of A. altissima essential oil vary considerably. This variability depends on the plant populations/ecological factors, the extractable parts, the ontogenesis stage, and the drying process. The main components are α-curcumene, α-gurjunene, γ-cadinene, α-humulene, β-caryophyllene, caryophyllene oxide, germacrene D, etc. [5][29][30][31].
The extraction methods are summarized here. The collection of the materials for A. altissima essential oil extraction may take place in the summer in Tunisia [29][30] or in September in Croatia [5]. The extraction of essential oil is a technological challenge as the researchers' own experience revealed (unpublished data). Basically, the essential oil of different plant parts (roots, stems, leaves/young and old plants, flowers, and ripe fruits, all cut into small pieces) is extracted by hydrodistillation for 3–4 h using a Clevenger-type apparatus [5][30] or a simple laboratory Quick-fit apparatus [29]. The identification of the components is performed by GC-FID and GC/MS analyses.
Additionally, the essential oil of A. altissima bark was extracted by the Soxhlet method with anhydrous diethyl ether until the distilled liquid became colorless. The solvent was evaporated under a vacuum in a rotary evaporator and the fumigant activity was tested against four major stored grain insects [32].

4. Quassinoids Extraction, Fractionation, and Isolation Overview

Quassinoids are all-chair cyclic and highly oxygenated derivatives of squalene. Biogenetically, they can be regarded as the degraded triterpenoids, which are isolated exclusively as bitter principles from plants of the Simaroubaceae family [33].
A. altissima is rich in quassinoids ( Figure 1) and the process of the identification of new quassinoids is still progressing [12]. The concentration of ailanthone, one of the main quassinoids, may range from 6.44 µg/mL to 825 µg/mL, depending on the source locality in China [34].
/media/item_content/202209/63101372a3a15diversity-14-00680-g001b.pngFigure 1. The structure of quassinoids isolated from A. altissima. The compound numbers correspond to the list in Table 1.

5. Biopesticide Potential of Ailanthus altissima and Tests’ Design

5.1. Phytotoxicity Assay of Ailanthus altissima

Essential Oil Phytotoxicity

The essential oils of A. altissima negatively affect the seed germination and early-stage development of the seedlings of the target species. The effect is dose-dependent and is greater in the light than in the dark. In addition, the phytotoxic effect depends on the origin of the essential oil, as the oil extracted from flowers is the most phytotoxic [29][30]. The caryophyllene oxide, b-caryophyllene, germacrene D, and hexahydrofarnesyl acetone presented in the essential oil may be responsible for such a phytotoxic effect [30][35][36]. Additionally, the complete inhibition of the germination of target plants is achieved after the application of 400 to 600 μg/mL hydrodistilled leaf residues [29].

Phytotoxicity of Polar Ailanthus altissima Extracts

The juglone index [37] of A. altissima has been assessed as very high (0.80–1.40 depending on the extract concentration [38][39][40]. The plant produces allelopathic substances that inhibit the seed germination and seedling growth of competing species. They are located mostly in the bark and the roots, but also occur in the leaves, seeds, and wood. The inhibitor(s) can readily be extracted from A. altissima with methanol, but not dichloromethane, indicating the plant’s polar characteristics. The experimental tests show “striking” postemergence effects, with a nearly complete mortality of all the receiver plant species [41].
The compounds of the methanolic extracts from A. altissima’s fresh leaves and some sub-fractions have strong inhibitory effects on plant growth. Some fractions show a regulatory effect on plant by inhibiting the growth of radicles at higher concentrations and enhancing their growth at lower concentrations [42]. The compounds of the aqueous extracts from A. altissima’s fresh leaves and bark negatively influence the growth of the treated seedlings of Sinapis alba L. and Brassica napus L. regardless of the dilution [43]. The aqueous extracts of A. altissima leaves have a concentration-dependent herbicidal effect on Medicago sativa L. seed germination [44].
Ailanthone is highly phytotoxic, with concentrations of 0.7 mL/L causing 50% inhibition of radicle elongation in a standardized bioassay with garden cress (Lepidium sativum L.) seeds [45]. The quassinoids (from the root bark of A. altissima), e.g., ailanthone, ailanthinone, and ailanthinol; the alkaloids such as 1-methoxycanthin-6-one; and the phenolic constituents of the leaves are potent phytotoxins [29][46][47][48][49][50][51]. A significant pre-emergence herbicide activity is found for most of the bark dichloromethane extracts, which is directly correlated with the ailanthone concentration. A remarkable combined pre- and post-emergence herbicidal activity was found for a specific fraction. These results indicate that the bark of A. altissima is a potential source for the production of natural herbicides for use in agriculture [52]. Methanol bark extract with the main component ailanthone was tested for herbicidal effects under field conditions. The results show that it was quite efficient against the weeds but also caused serious injuries to the crops. Thus, a weakness of ailanthone is its non-selectivity, but a positive feature lies in its ephemeral effects. Ailanthone is easily degradable by soil microorganisms [44][53]. It is necessary to note, however, that ailanthone is an acute toxic triterpene and should be used with caution [54].

5.2. Antifungal Activity

The antifungal activity test results are contradictory and depend on the extraction methods and reagents. The methanol and ethanol A. altissima leaves’ extracts have fungicidal activity only against Cladosporium cladosporioides of all the tested nine species belonging to Fusarium, Penicillium, Aspergillus, and Giberella—the toxic microfungi found in cereals used for livestock and human food. However, this activity is weaker compared to the Juglans regia leaves’ extracts [55]. Ethanol, methanol, and aqueous extracts of A. altissima were tested against Ceratocystis manginecans (the causal agent of Mango Sudden Death) using a poisoned food technique and the treatments result in thin, collapsed/damaged hyphae compared to the control. Phytochemical profiling of the most effective extracts revealed that 9-octadecanoic acid and I-(+)- ascorbic acid 2, 6-hexadecanoate possibly contribute to the antifungal effect [56]. Both acetone and methanol from the leaves’ extracts have activity against Candida albicans, which is higher than amphotericin B, a gold standard in antifungal therapy [9]. Although C. albicans is not a crop pathogen, the result shows that further antifungal activity is worth testing. The chloroform extract of Ailanthus excelsa stem bark shows fungistatic and fungicidal activity against Aspergillus niger, A. fumigatus, Penicillium frequentence, P. notatum, and Botrytis cinerea [57]. It is the quassinoids that have been found to have inhibitory activities against plant fungal pathogens [58].

5.3. Fumigant and Insect Repellent Activity

Essential Oil Fumigant and Insect Repellent Activity

The essential oil of A. altissima bark has a fumigant activity against some pest beetles. One possible application of A. altissima bark essential oil is for killing insects that damage stored foods or seeds, as it causes 99.3 and 81.9% mortality to Oryzaephilus surinamensis (Linnaeus) (Coleoptera: Silvanidae) and Sitophilus oryzae (Linnaeus) (Coleoptera: Curculionidae) with within 24 h, respectively [2][59][60]. In addition, Lü and his co-workers revealed that despite its weak fumigant activity against Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae) and Liposcelis paeta Pearman (Psocoptera: Liposcelididae) adults, it notably repels T. castaneum adults and L. paeta nymphaea [2][59][60]. Additionally, A. altissima bark oil possesses high fumigant activity against Lasioderma serricorne (Fabricius 1792) (Coleoptera: Anobiidae) adults with a mortality of 100% at 8 µL/L air within 48 h of exposure; thus, it is obviously a strong repellent of these pests [61]. (Z)-3-hexen-l-ol, which is one of the main components of the essential oil extracted from A. altissima stems [29], is known as a key herbivore-induced plant volatile. There is no doubting its role as an indirect defense and this compound is a good candidate for novel insect pest control strategies [62]. Additionally, caryophyllene and caryophyllene oxide, which are the main constituents of the essential oil of A. altissima leaves and samara [29], are attractive to green lacewings [63]. Green lacewing larvae are predators of many soft-bodied insect pests such as: aphids, thrips, whiteflies, leafhoppers, spider mites (especially red mites), and mealybugs, and consequently they participate in biological control [64]. Caryophyllene and caryophyllene oxide stimulate oviposition in green lacewings, which leads to increased larval predation against pest insects [63]. A. altissima contains compounds with strong acaricidal activity against the parasitic mites that cause skin disease, namely, Psoroptes cuniculi and Sarcoptes scabiei var. cuniculi [65]. It was also found to have activity towards nematodes of the Meloidogyne genus [66].

Polar Extracts’ Fumigant and Insect-Repellent Activity

The methanol extracts of A. altissima fresh leaves are practically non-toxic to the mosquito Aedes aegypti larvae [42] and the leaves are even used for feeding silkworms [67]. However, the methanolic extract of A. altissima leaves causes the malformation and mortality of the larvae of the moth Agrotis ipsilon, (Lepidoptera: Noctuidae), which are known to cause considerable damage to crops by severing young plants at the ground level. Aqueus extracts of A. altissima leaves have oviposition-deterrence effects against Spodoptera frugiperda (Smith) (Noctuidae), causing delays in the time to pupation and emergence in addition to reduced larval and pupal biomasses [68][69]. This moth is considered a noxious pest because the larvae cause massive damage to various crops; consequently, insecticide sprays are employed against it [70]. In addition, 0.5, 1, and 2% ethanol (70%) extracts of A. altissima bark and leaves have strong antifeeding activity against and significant insecticidal effects on gypsy moth (Lymantria dispar (L.)) larvae—insects known as voracious defoliating pests of deciduous trees.
The diethyl ether extract of A. altissima possesses an extremely strong repellent effect and to a certain extent a contact-killing effect on Oryzaephilus surinamensis (Linnaeus), the saw-toothed grain beetle [71]. The ethanol extract of A. altissima leaves possess strong acaricidal activity (97.4%) against the spider mite, Tetranychus urticae (Koch), a plant-feeding mite generally considered to be a pest [72]. The extract has no direct toxic effect on the pest but reduces its fertility about threefold and suppresses the development of larvae from eggs. The maximum efficiency of the extract was observed after 7–10 days when a filial generation of the spider mites started developing [73].
Quassinoids extracted both from leaves and roots have insecticidal, antifeedant, and insect-growth-regulatory activity, and ailanthone, in particular, was found to be efficient against the aphid Acyrtosiphon pisum [46]. There is a high mortality rate of aphids, pests of peas, when treated with ailanthone [74]. Methanol extracts or active substances such as ailanthone, chaparinone, glaucarubinone, and 13 (18)-dehydroglaucarubinone obtained from A. altissima leaves can be recommended for the development of new botanical insecticides targeted against the phytophagous larvae of Spodoptera littoralis, a moth referred to as the African cotton leafworm [75]. At the same time, quassinoids seems to be nontoxic for bees as they are found in propolis [46][53][76][77][78][79]. In addition, A. altissima bark-based hexane and methanol extracts do not possess any genotoxic, mutagenic, or carcinogenic effects on Saccharomyces cerevisiae, which was used as a test object to evaluate the potential harm to human health [80].

References

  1. Li, X.; Li, Y.; Ma, S.; Zhao, Q.; Wu, J.; Duan, L.; Wang, S. Traditional uses, phytochemistry, and pharmacology of Ailanthus altissima (Mill.) Swingle bark: A comprehensive review. J. Ethnopharmacol. 2021, 275, 114121.
  2. Lü, J.H.; He, Y.Q. Fumigant toxicity of Ailanthus altissima Swingle, Atractylodes lancea (Thunb.) DC. and Elsholtzia stauntonii Benth extracts on three major stored-grain insects. Ind. Crops Prod. 2010, 32, 681–683.
  3. Ohmoto, T.; Koike, K.; Sakamoto, Y. Studies on the constituents of A. altissima Swingle II. The alkaloid constituent. Chem. Pharm. Bull. 1981, 29, 390–395.
  4. Ohmoto, T.; Koike, K. Studies on the constituents of A. altissima Swingle III. The alkaloid constituents. Chem. Pharm. Bull. 1984, 32, 170–173.
  5. Mastelić, J.; Jerković, I. Volatile Constituents from the Leaves of Young and Old Ailanthus altissima (Mili.) Swingle Tree. Croat. Chem. Acta 2002, 75, 189–197.
  6. Kozuharova, E.; Lebanova, H.; Getov, I.; Benbassat, N.; Kochmarov, V. Ailanthus altissima (Mill.) Swingle—A terrible invasive pest in Bulgaria or potential useful medicinal plant? Bothalia 2014, 44, 213–230.
  7. Zhelev, I.; Georgiev, K.; Dimitrova-Dyulgerova, I. Carotenoid profile of Ailanthus altissima stem bark, in-vitro antioxidant and antineoplastic activities. World J. Pharm. Res. 2016, 5, 1816.
  8. Cho, S.K.; Jeong, M.; Jang, D.S.; Choi, J.H. Anti-inflammatory Effects of Canthin-6-one Alkaloids from Ailanthus altissima. Planta Med. 2018, 50, 527–535.
  9. Poljuha, D.; Sladonja, B.; Šola, I.; Dudaš, S.; Bilić, J.; Rusak, G.; Eloff, J.N. Phenolic composition of leaf extracts of Ailanthus altissima (Simaroubaceae) with antibacterial and antifungal activity equivalent to standard antibiotics. Nat. Prod. Commun. 2017, 12, 1934578X1701201021.
  10. Du, Y.Q.; Yan, Z.Y.; Shi, S.C.; Hou, Z.L.; Huang, X.X.; Song, S.J. Benzoic acid derivatives from the root barks of Ailanthus altissima. J. Asian Nat. Prod. Res. 2021, 23, 103–109.
  11. Du, Y.Q.; Yan, Z.Y.; Chen, J.J.; Wang, X.B.; Huang, X.X.; Song, S.J. The identification of phenylpropanoids isolated from the root bark of Ailanthus altissima (Mill.) Swingle. Nat. Prod. Res. 2021, 35, 1139–1146.
  12. Du, Y.Q.; Bai, M.; Yu, X.Q.; Lv, T.M.; Lin, B.; Huang, X.X.; Song, S.J. Quassinoids from the Root Barks of Ailanthus altissima: Isolation, Configurational Assignment, and Cytotoxic Activities. Chin. J. Chem. 2021, 39, 879–886.
  13. Wang, C.M.; Li, H.F.; Wang, X.K.; Li, W.G.; Su, Q.; Xiao, X.; Zhang, C.H. Ailanthus altissima-derived ailanthone enhances gastric cancer cell apoptosis by inducing the repression of base excision repair by downregulating p23 Expression. Int. J. Biol. Sci. 2021, 17, 2811.
  14. Duan, Z.K.; Lin, B.; Du, Y.Q.; Li, C.; Yu, X.Q.; Xue, X.B.; Huang, X.X. Monoterpenoid coumarins and monoterpenoid phenylpropanoids from the root bark of Ailanthus altissima. New J. Chem. 2021, 45, 1100–1108.
  15. Caramelo, D.; Pedro, S.I.; Marques, H.; Simão, A.Y.; Rosado, T.; Barroca, C.; Gallardo, E. Insights into the Bioactivities and Chemical Analysis of Ailanthus altissima (Mill.) Swingle. Appl. Sci. 2021, 11, 11331.
  16. Bray, D.H.; Boardman, P.; ONeill, M.J.; Chan, K.L.; Phillipson, J.D.; Warhurst, D.C.; Suffness, M. Plants as a source of antimalarial drugs 5. Activities of Ailanthus altissima stem constituents and of some related quassinoids. Phytother. Res. 1987, 1, 22–24.
  17. Okunade, A.L.; Bikoff, R.E.; Casper, S.J.; Oksman, A.; Goldberg, D.E.; Lewis, W.H. Antiplasmodial activity of extracts and quassinoids isolated from seedlings of Ailanthus altissima (Simaroubaceae). Phytother. Res. 2003, 17, 675–677.
  18. Li, Y.; Zhao, M.; Zhang, Z. Quantitative proteomics reveals the antifungal effect of canthin-6-one isolated from Ailanthus altissima against Fusarium oxysporum f. sp. cucumerinum in vitro. PLoS ONE 2021, 16, e0250712.
  19. Landrigan, P.J. Pesticides and Human Reproduction. JAMA Intern. Med. 2018, 178, 26–27.
  20. Adeyemi, J.A.; Ukwenya, V.O.; Arowolo, O.K.; Olise, C.C. Pesticides-induced Cardiovascular Dysfunctions: Prevalence and Associated Mechanisms. Curr. Hypertens. Rev. 2021, 17, 27–34.
  21. Needleman, H.L.; Gunnoe, C.; Leviton, A.; Reed, R.; Peresie, H.; Maher, C.; Barrett, P. Deficits in psychologic and classroom performance of children with elevated dentine lead levels. N. Engl. J. Med. 1979, 300, 689–695.
  22. FAO. Pollinators Vital to Our Food Supply under Threat. 2021. Available online: http://www.fao.org/news/story/en/item/384726/icode/ (accessed on 25 July 2021).
  23. Biesmeijer, J.C.; Roberts, S.P.M.; Reemer, M.; Ohlemüller, R.; Edwards, M.; Peeters, T.; Schaffers, A.P.; Potts, S.G.; Kleukers, R.; Thomas, C.D.; et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 2006, 313, 351–354.
  24. Brown, M.J.; Paxton, R.J. The conservation of bees: A global perspective. Apidologie 2009, 40, 410–416.
  25. Potts, S.; Biesmeijer, K.; Bommarco, R.; Breeze, T.; Carvalheiro, L.; Franzén, M.; González-Varo, J.P.; Holzschuh, A.; Kleijn, D.; Klein, A.-M.; et al. Status and Trends of European Pollinators. Key Findings of the STEP Project; Pensoft Publishers: Sofia, Bulgaria, 2015; p. 72.
  26. Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O.; Kunin, W.E. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 2010, 25, 345–353.
  27. Carvalheiro, L.G.; Kunin, W.E.; Keil, P.; Aguirre-Gutiérrez, J.; Ellis, W.N.; Fox, R.; Biesmeijer, J.C. Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol. Lett. 2013, 16, 870–878.
  28. Ollerton, J.; Erenler, H.; Edwards, M.; Crockett, R. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 2014, 346, 1360–1362.
  29. Albouchi, F.; Hassen, I.; Casabianca, H.; Hosni, K. Phytochemicals, antioxidant, antimicrobial and phytotoxic activities of Ailanthus altissima (Mill.) Swingle leaves. S. Afr. J. Bot. 2013, 87, 164–174.
  30. El Ayeb-Zakhama, A.; Ben Salem, S.; Sakka-Rouis, L.; Flamini, G.; Ben Jannet, H.; Harzallah-Skhiri, F. Chemical Composition and phytotoxic effects of essential oils obtained from Ailanthus altissima (Mill.) Swingle cultivated in Tunisia. Chem. Biodivers. 2014, 11, 1216–1227.
  31. Kozuharova, E.; Benbassat, N.; Berkov, S.; Ionkova, I. Ailanthus altissima and Amorpha fruticosa—Invasive arboreal alien plants as cheap sources of valuable essential oils. Pharmacia 2020, 67, 71.
  32. Lü, J.; Wu, S. Bioactivity of essential oil from Ailanthus altissima bark against 4 major stored-grain insects. Afr. J. Microbiol. Res. 2010, 4, 154–157.
  33. Zhou, L.; Wang, J.; Wang, K.; Xu, J.; Zhao, J.; Shan, T.; Luo, C. Secondary metabolites with antinematodal activity from higher plants. In Studies in Natural Products Chemistry; Elsevier: Amsterdam, The Netherlands, 2012; Volume 37, pp. 67–114.
  34. He, Q.; Xiao, H.; Li, J.; Liu, Y.; Jia, M.; Wang, F.; Zhang, Y.; Wang, W.; Wang, S. Fingerprint analysis and pharmacological evaluation of Ailanthus altissima. Int. J. Mol. Med. 2018, 41, 3024–3032.
  35. Quintana, N.; El Kassis, E.G.; Stermitz, F.R.; Vivanco, J.M. Phytotoxic compounds from roots of Centaurea diffusa Lam. Plant Signal. Behav. 2009, 4, 9–14.
  36. De Martino, L.; Formisano, C.; Mancini, E.; Feo, V.D.; Piozzi, F.; Rigano, D.; Senatore, F. Chemical composition and phytotoxic effects of essential oils from four Teucrium species. Nat. Prod. Commun. 2010, 5, 1969–1976.
  37. Szabó, L. Juglone index—A possibility for expressing allelopathic potential of plant taxa with various life strategies. Acta Bot. Hung. 1999, 42, 295–305.
  38. Csiszár, Á. Allelopathic effects of invasive woody plant species in Hungary. Acta Silv. Lignaria Hung. 2009, 5, 9–17. Available online: http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.1066.4899&rep=rep1&type=pdf (accessed on 25 July 2022).
  39. Csiszár, Á.; Korda, M.; Schmidt, D.; Šporčić, D.; Süle, P.; Teleki, B.; Tiborcz, V.; Zagyvai, G.; Bartha, D. Allelopathic potential of some invasive plant species occurring in Hungary. Allelopath. J. 2013, 31, 309–318.
  40. Novak, N.; Novak, M.; Barić, K.; Šćepanović, M.; Ivić, D. Allelopathic potential of segetal and ruderal invasive alien plants. J. Cent. Eur. Agric. 2018, 19, 408–422.
  41. Heisy, R. Allelopathic and herbicidal effects of extracts from tree of heaven (Ailanthus altissima). Am. J. Bot. 1990, 77, 662–670.
  42. Tsao, R.; Romanchuk, F.E.; Peterson, C.J.; Coats, J.R. Plant growth regulatory effect and insecticidal activity of extracts of tree of Heaven (Ailanthus altissima L.). BMC Ecol. 2002, 2, 1. Available online: https://bmcecol.biomedcentral.com/articles/10.1186/1472-6785-2-1 (accessed on 25 July 2022).
  43. Bostan, C.; Borlea, F.; Mihoc, C.; Selesan, M. Ailanthus altissima species invasion on biodiversity caused by potential allelopathy. J. Agric. Sci. 2014, 46, 95–103. Available online: http://cormoran.portiledefier.ro/wp-content/uploads/2013/02/bostan_cristian_1.pdf (accessed on 25 July 2022).
  44. Sladonja, B.; Pohulja, D.; Sušek, M.; Dudaš, S. Herbicidal effect of Ailanthus altissima leaves water extracts on Medicago sativa seeds germination. In Book of Abstracts of the 3rd Conference with International Participation Conference VIVUS; Biotechnical Centre Naklo: Naklo, Slovenia, 2014; pp. 476–481. Available online: http://civ.iptpo.hr/wp-content/uploads/publikacije/Znanstveni%20rad%20u%20zborniku%20skupa_VIVUS_2014.pdf (accessed on 25 July 2022).
  45. Heisey, R.M. Identification of an allelopathic compound from Ailanthus altissima (Simaroubaceae) and characterization of its herbicidal activity. Am. J. Bot. 1996, 83, 192–200.
  46. De Feo, V.; Mancini, E.; Voto, E.; Curini, M.; Digilio, M.C. Bioassay-oriented isolation of an insecticide from Ailanthus altissima. J. Plant Interact. 2009, 4, 119–123.
  47. Casinovi, C.G.; Ceccherelli, P.; Fardella, G.; Grandolini, G. Isolation and structure of a quassinoid from Ailanthus glandulosa. Phytochemistry 1983, 22, 2871–2873.
  48. Lin, L.-J.; Peiser, G.; Ying, B.-P.; Mathias, K.; Karasina, F.; Wang, Z.; Itatani, J.; Green, L.; Hwang, Y.-S. Identification of plant growth inhibitory principles in Ailanthus altissima and Castela tortuosa. J. Agric. Food Chem. 1995, 43, 1706–1711.
  49. De Feo, V.; De Martino, L.; Quaranta, E.; Pizza, C. Isolation of phytotoxic compounds from tree-of-heaven (Ailanthus altissima Swingle). J. Agric. Food Chem. 2003, 51, 1177–1180.
  50. De Feo, V.; Martino, L.D.; Santoro, A.; Leone, A.; Pizza, C.; Franceschelli, S.; Pascale, M. Antiproliferative effects of tree-of-heaven (Ailanthus altissima Swingle). Phytother. Res. 2005, 19, 226–230.
  51. Lebedev, V.G.; Krutovsky, K.V.; Shestibratov, K.A. Fell Upas Sits, the Hydra-Tree of Death†, or the Phytotoxicity of Trees. Molecules 2019, 24, 1636.
  52. Borchardt, J.R.; Wyse, D.L.; Sheaffer, C.C.; Kauppi, K.L.; Fulcher, R.G.; Ehlke, N.J.; Biesboer, D.D.; Bey, R.F. Antimicrobial activity of native and naturalized plants of Minnesota and Wisconsin. J. Med. Plant Res. 2008, 2, 98–110.
  53. Heisey, R.M.; Heisey, T.K. Herbicidal effects under field conditions of Ailanthus altissima bark extract, which contains ailanthone. Plant Soil 2003, 256, 85–99.
  54. Anonymous. National Center for Biotechnology Information. PubChem Database. Ailanthone, CID=72965; 2019. Available online: https://pubchem.ncbi.nlm.nih.gov/compound/Ailanthone (accessed on 1 January 2022).
  55. Balkan, B.; Balkan, S.; Aydoğdu, H.; Özcan, Ö. Antifungal activities of Ailanthus altissima Swingle and Juglans regia L. leaves against some cereal fungi. J. Appl. Environ. Biol. Sci. 2014, 8, 76–79.
  56. Jabeen, K.; Asad, S.; Zakria, M. Antifungal Evaluation and Phytochemical Identification of Selected Botanicals against Ceratocystis manginecans Causing Mango Sudden Death. J. Plant Pathol. Microbiol. 2018, 9, 465.
  57. Joshi, B.C.; Pandey, A.; Chaurasia, L.; Pal, M.; Sharma, R.P.; Khare, A. Antifungal activity of the stem bark of Ailanthus excelsa. Fitoterapia 2003, 74, 689–691.
  58. Chen, J.J.; Bai, W.; Lu, Y.B.; Feng, Z.Y.; Gao, K.; Yue, J.M. Quassinoids with Inhibitory Activities against Plant Fungal Pathogens from Picrasma javanica. J. Nat. Prod. 2021, 84, 2111–2120.
  59. Lü, J. The insecticidal activities of Ailanthus altissima extracts on several kinds of important stored-grain insects. Grain Storage 2007, 36, 17–20.
  60. Lü, J.H.; Lu, Y.J.; Hu, Y.Y. Controlling effects of three plant essential oils on Liposcelis paeta. J. Henan Agric. Sci. 2006, 5, 18.
  61. Lü, J.H.; Shi, Y.L. The bioactivitiy of essential oil from Ailanthus altissima Swingle (Sapindales: Simaroubaceae) bark on Lasioderma serricorne (Fabricius) (Coleoptera: Anobiidae). Adv. Mater. Res. 2012, 365, 428–432.
  62. Wei, J.; Kang, L. Roles of (Z)-3-hexenol in plant-insect interactions. Plant Signal. Behav. 2011, 6, 369–371.
  63. Flint, H.M.; Salter, S.S.; Walters, S. Caryophyllene: An attractant for the green lacewing. Environ. Entomol. 1979, 8, 1123–1125.
  64. Goulson, D. The Garden Jungle: Or Gardening to Save the Planet; Random House: New York, NY, USA, 2019; p. 261.
  65. Gu, X.; Fang, C.; Yang, G.; Xie, Y.; Nong, X.; Zhu, J.; Wang, S.; Peng, X.; Yan, Q. Acaricidal properties of an Ailanthus altissima bark extract against Psoroptes cuniculi and Sarcoptes scabiei var. cuniculi in vitro. Exp. Appl. Acarol. 2014, 62, 225–232.
  66. Caboni, P.; Ntalli, N.G.; Aissani, N.; Cavoski, I.; Angioni, A. Nematicidal activity of (E, E)-2, 4-decadienal and (E)-2-decenal from Ailanthus altissima against Meloidogyne javanica. J. Agric. Food Chem. 2012, 60, 1146–1151.
  67. Lucchetti, L.; Zitti, S.; Taffetani, F. Ethnobotanical uses in the Ancona district (Marche region, Central Italy). J. Ethnobiol. Ethnomed. 2019, 15, 9.
  68. Wagner, R.L.; Card, J.A. Ailanthus altissima aqueous extract deters Spodoptera frugiperda oviposition. Gt. Lakes Entomol. 2020, 53, 11. Available online: https://scholar.valpo.edu/tgle/vol53/iss1/11 (accessed on 25 July 2022).
  69. Wagner, L.R.; Leach, E.M.; Wallace, J.R. Leaf Extract from Ailanthus altissima negatively impacts life history aspects in Spodoptera frugiperda (Lepidoptera: Noctuidae). J. Kansas Entomol. Soc. 2021, 93, 140–152.
  70. Souza, J.R.; Carvalho, G.A.; Moura, A.P.; Couto, M.H.; Maia, J.B. Impact of insecticides used to control Spodoptera frugiperda (JE Smith) in corn on survival, sex ratio, and reproduction of Trichogramma pretiosum Riley offspring. Chil. J. Agric. Res. 2013, 73, 122–127.
  71. Lu, J.-H.L.; Lu, Y.J.; Tan, Y.B.; Liu, J.J.; Zhong, J.F. The controlling effects of plant extracts on Oryzaephilus surinamensis (Linnaeus). J. Henan Uni. Tech. 2006, 3, 17–20.
  72. Chermenskaya, T.D.; Stepanycheva, E.A.; Shchenikova, A.V.; Chakaeva, A.S. Insectoacaricidal and deterrent activities of extracts of Kyrgyzstan plants against three agricultural pests. Ind. Crops Prod. 2010, 32, 157–163.
  73. Stepanycheva, E.A.; Chermenskya, T.D.; Chakaeva, A.S. Effect of biologically active substances of Ailanthus altissima Mill. Swingle)(Simarubaceae) on spider mite Tetranychus urticae Koch (Akari: Tetranychidae). Agric. Chem. 2011, 4, 52–59. (In Russian)
  74. Polonsky, J.; Bhatnagar, S.C.; Griffiths, D.C.; Pickett, J.A.; Woodcock, C.M. Activity of quassinoids as antifeedants against aphids. J. Chem. Ecol. 1989, 15, 993–998.
  75. Pavela, R.; Zabka, M.; Tylova, T.; Kresinova, Z. Insecticidal activity of compounds from Ailanthus altissima against Spodoptera littoralis larvae. Pak. J. Agric. Sci. 2014, 51, 101–112. Available online: https://pakjas.com.pk/papers/2248.pdf (accessed on 25 July 2022).
  76. Fokt, H.; Pereira, A.; Ferreira, A.M.; Cunha, A.; Aguiar, C. How do bees prevent hive infections? The antimicrobial properties of propolis. Curr. Res. Technol. Educ. Top. Appl. Microbiol. Microb. Biotechnol. 2010, 1, 481–493.
  77. Connolly, J.D.; Hill, R.A. Triterpenoids. Nat. Prod. Rep. 2011, 28, 1087–1117.
  78. Slave, J. Effects of Calcium hydroxide and Quassia extract on Honey bees (Apis mellifera). In Proceedings of the 18th International Conference on Organic Fruit-Growing, Hohenheim, Germany, 19–21 February 2018; Foerdergemeinschaft Oekologischer Obstbau e.V. (FOEKO): Weinsberg, Germany, 2018; pp. 247–248.
  79. Yang, K.; Wen, X.; Ren, Y.; Wen, J. Control of Eucryptorrhynchus scrobiculatus (Coleoptera: Cuculionidae), a major pest of Ailanthus altissima (Sapindales: Simaroubaceae), using a modified square trap net. J. Econ. Entomol. 2018, 111, 1760–1767.
  80. Todorova, T.; Boyadzhiev, K.; Shkondrov, A.; Parvanova, P.; Dimitrova, M.; Ionkova, I.; Kozuharova, E.; Chankova, S. Screening of Amorpha fruticosa and Ailanthus altissima extracts for genotoxicity/antigenotoxicity, mutagenicity/antimutagenicity and carcinogenicity/anticarcinogenicity. BioRisk 2022, 17, 201–212.
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