Utilization of plant secondary metabolites for plant protection

Abstract

In the past two decades, the need for a new concept in agriculture has emerged. The new “Greener revolution” should rely on the implementation of sustainable practices in crop production and the achievement of increased yields under the conditions of reduction of water, fertilizer, and pesticide use. The utilization of plant secondary metabolites is viewed by many authors as а possible alternative to synthetic chemicals. Bioactive botanical compounds can be obtained from plants in the form of extracts, essential oils (EO), or both. There are four main groups of plant secondary metabolites depending on their chemical structure: terpenes, phenolics, nitrogen-, and sulfur-containing compounds. A growing body of publications is devoted to the pesticidal properties of various secondary metabolites obtained from plants. The botanical families Meliaceae, Rutaceae, Asteraceae, Annonaceae, Labiatae, and Canellaceae include the most valuable species that are rich in secondary metabolites. The strong fumigant properties of the EOs from many plant species make them attractive in different Integrated Post-Harvest Pest Management systems. Suitable carriers for EOs delivery can be designed using nanoencapsulation. On a worldwide scale, the main botanical insecticides that are commercially available at present are Pyrethrum, Azadirachtin from Neem, and EOs from various plant species. Among the botanicals with considerable antimicrobial activity, there are some successfully authorized and developed commercial phenolics, terpenes, and alkaloids. Among the proven active substances are cinnamaldehyde, l-glutamic acid and gamma-aminobutyric acid, Jojoba oil, еssential oils, and others.

Keywords:

• Essential oils
• botanical pesticides
• post-harvest pest control
• biopesticide market

Introduction

Agricultural crop production is essential for the survival and well-being of the world’s human population, which is forecast to increase to about 9 billion by 2050. This is expected to lead to a global environmental change. To attain maximum productivity, intensive farming relies on the input of a high level of agrochemicals, together with mechanization [1]. The twentieth-century Green Revolution brought agricultural intensification by means of fertilization, irrigation, pesticide application, and crop breeding [2]. Many positive effects have been achieved: reduction of labor, increment of crop yield, and food security. On the other hand, productivity expansion has led to adverse consequences like topsoil depletion, groundwater contamination, increased production costs, and the decline of family farms [3]. The characteristic globalization of the agri-food systems has also negatively impacted dietary diversification, resulting in a rise in micronutrient deficiencies on a worldwide scale. Other negative consequences include a higher frequency of economic shocks, most strongly resonating in poorer regions, the opacity of food origin and quality assessment, the collapse of biodiversity, and the degradation of different ecosystems, including the marines, accompanied by environmental damages [4]. For example, various detrimental effects of agricultural intensification have become apparent in India after the adoption of a few high-yielding varieties of rice instead of landraces. These effects include a general loss of agro-biodiversity, a change in the water usage landscape, and a huge rise in agrochemical application and its effect on soil, water resources, and the edible biota of rice fields [5].

In the past two decades, it has become apparent that there is expanding awareness among environmentalists about the need for a new concept in agriculture. The new “Greener revolution” should entail the implementation of sustainable practices in crop production and increased yields at the same time, under the conditions of reduction of water, fertilizer, and pesticide use [2, 6]. There are roughly 2000 pesticides in commercial use worldwide, and this quantity is expected to grow continuously [7]. Conventional agrochemicals for plant disease control are related to various problems like negative effects on the environment and human health, as well as acquired resistance to widely used chemical products in plant pathogen populations [8]. Pesticides possess high biological toxicity and complex distribution in the ecosystem, spreading to air by means of wind, to water by means of runoff and leaching, and thereby to humans, animals, and plants [9]. Deleterious loss in the biodiversity of various aquatic and terrestrial non-target organisms due to chemical plant protection products is also evident and addressed in many publications. Furthermore, the Environmental Risk Assessment of Pesticides for registration in the European Union may be suffering from important drawbacks, thus contributing to the decline in biodiversity [10, 11]. Pesticides based on natural substances, together with RNA interference-based technologies, are viewed by many authors as a possible alternative to synthetic chemicals [12, 13]. The active substances can be derived from animals, plants, and microorganisms like bacteria, cyanobacteria, and microalgae. One of the most common microbial pesticides are those based on Bacillus thuringiensis (Bt) and Trichoderma spp [14, 15]. Botanical pesticides can be obtained from all plant parts and utilized in the form of plant extracts, essential oils (EOs) or both, depending on the targeted bioactive compounds [16]. They are usually extracted with organic solvents and then concentrated, formulated, and evaluated for efficacy under laboratory, controlled, or field conditions. Most commonly, the promising plant species are selected on the basis of ethnobotanic studies and allelopathy data [15]. Then, bioassay-guided fractionation of crude extracts, which consists of systematic separation of extracted components based on the differences in their physicochemical properties, takes place. The next steps include assessing the targeted activity, followed by another round of separation and evaluation. As a result, the active components are separated from the crude extract. This approach can be used for medicinal purposes as well as for botanical-based pesticides [17].

In this review, we attempt to summarize the current literature about the possibilities for the employment of plant secondary metabolites in plant protection. We take into consideration the processes of the selection of effective extracts, the main secondary metabolites in plants and their potency against the main pest groups. We dwell upon the recent achievements and challenges in the novel types of formulations and applications of botanicals in pest and disease control. We also glance at the botanical-based fungicides on the world market and their future perspectives.

Important secondary metabolites in plants and their action

Secondary metabolites in plants play a huge role in their innate defense against pathogens, pests, and abiotic stress factors [18]. Since they are natural products, they are biodegradable, less toxic to humans, and participate in a wide range of activities. There are four main groups of plant secondary metabolites depending on their chemical structure: terpenes, phenolics, nitrogen-, and sulfur-containing compounds [19].

Terpenes are structurally the most diverse class of secondary metabolites. They are formed structurally by branching different numbers of isoprene units, and they may or may not contain oxygen (terpenoids and terpenes) [20]. Terpenes in plants could play both an ecological and physiological role: allelopathy, insecticidal activity, the attraction of pollinators, plant hormones (abscisic acid, gibberellins), etc. [21]. Terpenoids such as monoterpenoids and sesquiterpenoids, which are primary components of EOs, are highly volatile. EOs often function as insect toxins, and many protect against fungal or bacterial attacks. For example, mint plants (Mentha spp.) produce large quantities of the monoterpenoids menthol and menthone [22]. It has been proven that these substances have a fungicidal effect against Alternaria alternata [23]. Details are presented in Table 1. Menthol showed an antibacterial effect on Xanthomonas campestris and Pseudomonas syringae strains [24].

Table 1. Recent studies on the effect of plant extracts and oils on important agricultural pathogens.

Plant source	Pathogens, disease	Extract, concentration, active compounds	Best results, conditions	References
Melia azedarach and Ficus carica	Cucumber mosaic virus (CMV) in cucumber seedlings	Ethanolic (100 ppm) and aquatic extracts (1000 ppm)	80–90% decrease up of symptoms to 15 days after their treating/greenhouse conditions	[55]
Satureja khuzistanica	CMV in test plant Vigna unguiculata	Hydro–ethanolic extract, 2–4%	66–78% disease reduction/greenhouse conditions	[56]
		EO nanoemulsion, 2%) /carvacrol, para-cymene, beta-caryophyllene, and beta-pinene	59% disease reduction/greenhouse conditions
Rumex nepalensis	Alternaria solani (early blight in potato)	Aqueous extracts of aerial parts	60% reduction of fungal mycelial growth (FMG)/in vitro. 71.43% preventive control of disease/in vivo	[57]
Mentha arvensis	Alternaria alternata (leaf blight in tomato plants)	EO, 40 μL/mL (menthol, menthone)	93.6% reduction of FMG and 90.6% inhibition of conidia germination/in vitro Over 80% increasing the plant grought metrics (height, fresh and dry weight)/in vivo	[23]
Origanum vulgare	Botrytis cinerea (gray mold disease)	EO, 0.5 mg/mL, carvacrol, thymol, β-caryophyllene	100% inhibition of FMG/in vitro	[58]
Syzygium aromaticum	Botrytis cinerea (grey mould in strawberry)	EO, 12 mL/L, eugenol	Significantly inhibition the infection on detached strawberry leaves/in vitro	[59]
Mentha x piperita, Syzygium aromaticum, and Cinnamomum zeylanicum	Rhizoctonia solani, Sclerotinia sclerotiorum, Fusarium oxysporum, and F. solani (root rot and wilt of marigold) Calendula officinalis L.	EOs, 1 mL/L	70–100% reduction of FMG/in vitro	[60]
		EOs, 3 mL/L for seed soaking and 1.5 mL/L for foliar spraying)	Significantly disease reduction/greenhouse conditions
Foeniculum vulgare	Fusarium oxysporum f. sp. lycopersici (tomato fusarium wilt)	EO, 500 μL/mL, trans-anethole, L-fenchone, estragole and limonene	42.85% disease severity reduction/in vivo	[61]
	Fusarium culmorum, F. poae, Botrytis cinerea (Fusarium disease of pea)	EO, 200 ppm	100% inhibition of FMG/in vitro	[62]
		EO, 500 ppm	40% disease reduction/n vivo
Mentha longifolia	Aspergillus flavus, Aspergillus niger, Fusarium culmorum	EO, 500 and 250 μL/mL, menthone, eucalyptol	100% inhibition of FMG/in vitro	[63]
Origanum bilgeri	Clavibacter michiganensis subsp. michiganensis (Cmm), Xanthomonas axonopodis pv. vesicatoria (Xav) and Pseudomonas syringae pv. tomato (Pst).	EOs, 7.5 μL dose/petri dish, carvacrol, borneol, and p-cymen	100% microbial growth inhibition/in vitro	[64]
Origanum syriacum L.	Rhizobium radiobacter	EO, 10 μL dose/petri dish, carvacrol, p-cymene,γ-terpinene	37.67 mm inhibition zone/in vitro	[65]
	Pseudomonas savastanoi pv.savastanoi		44.67 mm inhibition zone/in vitro
	P.savastanoi pv.nerii		16.67 mm inhibition zone/in vitro

FMG, fungal mycelial growth; EO, essential oil.

Phenols consist of at least one aromatic ring linked to one or more hydroxyl groups. Important subgroups of phenols are simple phenols, tannins, lignins, flavonoids, coumarins, and stilbenes [25]. Phenolic compounds act on insects directly as toxins that disrupt their growth and development [26]. Flavones, flavonoids, and flavonols are phenolic structures with one carbonyl group. They are synthesized by plants in response to microbial infection and are often found effective in vitro as antimicrobial substances against a wide array of microorganisms [27]. Coumarins and stilbenes have antimicrobial and germination inhibitor properties [21, 28].

Nitrogen-containing secondary metabolites include alkaloids, amines, non-protein amino acids, cyanogenic glucosides, and peptides. Fabaceae plants can produce more nitrogen-containing secondary metabolites because of their ability to fix atmospheric nitrogen. The nitrogen-containing defense compounds often accumulate in seeds [29].

About 20% of plant species produce alkaloids. They are toxic to insects by affecting their nervous system, DNA replication, protein synthesis, enzyme activity, etc. [25, 26, 30]. Alkaloids have insecticidal, acaricidal, fungicidal, antiviral, and herbicidal properties [31]. For example, the alkaloids caffeine and theobromine (isolated from coffee (Coffea arabica), tea (Camellia sinensis) and cocoa (Theobroma cacao)) are toxic to both insects and fungi. They are also reported to inhibit the germination of seeds from other plants (allelopathy) [22, 26].

Sulfur-containing secondary metabolites are of two types: glucosinolates, which are present in Brassicaceae, and alliins, found in members of the Allium genus. Both glucosinolate–myrosinase and alliin–alliinase pathways seem to be evolved for herbivore defense [25]. When herbivores injure plant cells, glucosinolates are metabolized into toxic substances, such as nitriles, thiocyanates, and isothiocyanates [26].

Application of essential oils and plant extracts for pest and disease control in agriculture

There are a number of plant species whose extracts and essential oils possess insecticidal, acaricidal, nematocidal, fungicidal, and bactericidal properties. These natural plant protection products have a number of advantages and are being increasingly used in organic farming [32]. Most plants produce a rich complex of secondary metabolites, so their extracts may have more than one effect. At the end of the last century, the species of the families Meliaceae, Rutaceae, Asteraceae, Annonaceae, Labiatae, and Canellaceae were indicated as the most promising source of botanicals [33]. The author points out the necessary prerequisites for successful commercialization of botanical pesticides. They need to be safe for plant and animal life and biodegradable plants to be readily available or capable of cultivation and to have determined procedures for isolation or syntheses of the active component(s) [33].

Plant extracts with activity against arthropod pests

The most widely used botanical insecticide worldwide is pyrethrum, although it is difficult to determine precisely the amounts used [34]. Pyrethrins are extracted from the perennial plant Dalmatian pyrethrum (Tanacetum cinerariifolium (Trevir.) Sch. Bip. syn.: Chrysanthemum cinerariifolium (Trevis.) Vis., Pyrethrum cinerariifolium Trevis), Asteraceae family. The species is cultivated for the production of monoterpene esters called pyrethrins, which possess insecticidal properties [35]. For the needs of plant protection, the flowers of the plant are used, where the concentration of biologically active substances is greatest during mass flowering. Natural pyrethrins, similarly to their synthetic pyrethroid derivatives, can be used directly against insects, or applied as a spray or dust [36]. Shawkat et al. [37] have found that the C. cinerariaefolium flower extract can be used as a control agent against Tribolium castaneum. Between 100 and 60% mortality of the insects has been reached in treatments with the flower extract at concentrations from 40% to 20%, respectively [37]. The use of botanical pesticides such as pyrethrin fits into the goals of sustainable agriculture for the reduction of the spread of pests and diseases without altering the natural balance [38].

Another highly aromatic plant species that is used in medicine and plant protection is garlic (Allium sativum). Its major organosulfur compounds are ajoenes, allicin, alliin, allyl sulfide, and 1,2-vinyldithiin [39]. Nwachukwu and Asawalam [40] have found that freshly prepared garlic juice containing allicin possesses insecticidal properties against Sitophilus zeamais. Increasing the concentration of aqueous extracts, using underground and aerial parts of nettle (Urtica dioica) plus grinding garlic bulbs into powder can increase their efficacy as biological pesticides. According to Fatima et al. [41], garlic extract can be used for control of Tetranychus evansi in tomato crops. Garlic extract (25 g fresh weight in 10 L of water) applied to the soil and plants was found effective against aphids, Lepidoptera larvae, whiteflies, weevils, and mites [39, 42].

The essential oils of Artemisia absinthium L. and Tanacetum vulgare L. were found lethal to Tetranychus urticae Koch. to a variable extent. A chemical analysis of T. vulgare extract revealed that beta-thujone is the main contributing compound [43]. Elisovetskaya and Nastas [44] have proved the high insecticidal activity of hellebore extract (Veratrum lobelianum Bernh.) against the imago and larvae of Leptinotarsa decemlineata Say, I-III instar of Heliothis armigera Hbn., Mamestra brassicae L., and Acyrtho siphonpisum Harr. The extract was confirmed to exhibit repellent activity against Galleria mellonella larvae. A single treatment with 0.1% extract of V. lobelianum (water–alcohol solution, 7.5 L/ha, 40 g/L active substance) was reported to be sufficient for the reduction of the density of L. decemlineata first generation [44].

The hot taste of Capsicum annuum L. (Solanaceae) is due to the presence of capsaicinoids, found only in the genus Capsicum, which are biosynthesized in the fruit placenta by condensation of vanillylamine and fatty acids. Fatima et al. [41] have found that the extract of Capsicum frutescens has the potential to control Tetranychus evansi in tomato cultivation.

Another established biological insecticide in agriculture is nicotine, a major alkaloid in tobacco plants (Nicotiana spp., Solanaceae). It is used against many insects, including aphids, thrips, and whiteflies [45]. Nicotine is a nonsystemic insecticide that interacts with the cholinergic acetylcholine nicotinic receptor (nAch) in the nerve cells of insects. Tobacco leaf powder snuff at 3% w/w was found effective against cowpea weevil (Callosobruchus maculatus L.) studied on stored cowpea (Vigna unguiculata L.) grains [39]. Both the crude extract and the isolated alkaloids of Chelidonium majus, Papaveraceae have shown high insecticidal activity against Lymantria dispar larvae by affecting their nutrition [46].

Plant extracts with nematocidal activity

Plant-parasitic nematodes are emerging as one of the most destructive groups of plant pathogens in the world, and their control is extremely difficult [47]. The activity of natural nematocides is usually expressed as a paralysis effect on second-stage juveniles, or as egg hatch arrest [48]. Among the plants possessing nematocidal properties is Tagetes patula L., a species of the Asteraceae family originating from Mexico and Guatemala. It has a great number of varieties, and is widely cultivated as an easy-to-grow plant. A methanol–water (1:1, w/v) extract of fresh horseradish (Armoracia rusticana, Brasicaceae) roots was tested in vitro for nematocidal activity against second-stage juvenile Meloidogyne incognita. The most abundant compound in the extract, allylisothicyanate, induced paralysis with an EC₅₀ of 52.6 ± 45.6 and 6.6 ± 3.4 mg/L after 1 h and 3 days of incubation [49]. Garlic straw was found effective by Gong et al. [50] in reducing root-knot nematode damage on tomatoes, thereby increasing crop productivity.

Plant extracts with activity against plant pathogens

Equisetum arvense L. extract has been approved for use in horticulture, ornamentals, viticulture cereals, and other cultures as an EU agricultural pesticide in organic production since 2016 [51]. A synergistic effect was found between horsetail (E. arvense L.) aqueous extract and chitosan (1:1), which were tested against important grapevine trunk diseases. Tests were performed in vitro against eight species of Botryosphaeriaceae and in vivo in grafted plants artificially inoculated with Neofusicoccum parvum and Diplodia seriata. Strong inhibition of both mycelial growth and plant damage was observed [52]. Trebbi et al. [53] found that E. arvense macerate has the potential to be an alternative treatment for Phytophthora infestans in the organic production of tomatoes (S. lycopersicum). In a three-year experiment under field conditions, foliar spraying of tomato plants with horsetail macerate and copper (Cu) fungicides (as a control) was regularly applied. The authors established that the Cu-fungicides and horsetail macerate treatments were both equally effective at significantly reducing late blight disease and increasing yield in tomatoes compared to the untreated control [53]. In another study, Tagetes patula L. water extract from dry flowers was found to effectively control early blight (Alternaria solani) with 61.53% reduction of disease (%RD), wilt (Fusarium oxysporum f. sp., lycopersici (18.42% RD), bacterial fruit spot (Pseudomonas syringae (27.41% RD), and sunburn (26.44% RD) on tomato plants [54]. These properties of T. patula are a good alternative to existing synthetic pesticides. More examples of plant extracts and oils that are active against important agricultural pathogens are given in Table 1.

Fumigant toxicity of essential oils against pests and diseases of stored products

The constant market demand for fresh fruit and vegetables of high quality and the growing awareness of the toxic potential of fungicide residues have brought to the forefront the development of new alternative approaches for disease control. They include the use of physical means, biocontrol agents, and natural compounds [66]. Pests and diseases on the major crops at each step of the supply chain (i.e. harvest, storage, transit, and commercialization) cause losses that are estimated to reach between 25% and 50% of the total production, depending on the level of the storage facilities. The pathogens responsible for the microbial decay during the storage of fresh fruit, nuts, and grains are the object of postharvest pathology science [66]. Practically, all postharvest diseases of fruit and vegetables are caused by fungi and bacteria. However, no less harm is caused by the multitude of insects which have adapted to develop in stored grain and constitute a constant threat to the quality of grain and its products [67].

The minimizing of post-harvest food losses and the development of effective postharvest management practices are crucial for global food security and availability [68, 69]. The traditional strategies for pest and disease management during storage and prevention include the extensive use of fungicides and insecticides [67, 70]. Integrated pest management (IPM) postharvest prevention and management strategies rely on a combination of different biological, physical, and chemical tools. When a significant insect infestation is detected, the most commonly used practice is fumigation [71]. Fumigation is a vital part of integrated pest management. An agent widely used in the past was methyl bromide, but this insecticide was phased out for grain storage use in 2005 for environmental reasons [72]. In the past few years, multiple publications have focused on the fumigant properties of the plant EOs, which would allow them to find a place in different Integrated Pest Management systems. This potential is based on their ability to interfere with the basic metabolic, biochemical, physiological, and behavioral functions of insects [73]. EOs and their constituents are fast-acting neurotoxins in insects, likely interacting with multiple receptor types [74]. It has been found that the biocidal activity of EOs against some adult dipteran insects can be increased by up to 100% for certain EO mixtures compared to individual EOs [73].

A recent review summarizes the literature exploring the insecticidal effect of EOs on six economically important pests in stored grain [75]. Among the essential oils investigated in 42 articles, the most promising against Lasioderma serricorne have proved to be the EOs of Artemisia argyi and Mentha haplocalyx (DL50 of 6.42 μg/adult and 16.5 μg/adult, respectively). Against Liposcelis bostrychophila, there was strong repellent activity of Ligusticum pteridophyllum EO at the concentration of 3.15 nL/cm² after 2 h of exposure, and CL₅₀ for Artemisia rupestris EO was determined to be 418.48 μg/cm² in a contact test. Artemisia anethoides EO exhibited 100% repellency at concentrations of 78.63 and 15.73 nL/cm² after 24 h of exposure, and Elshotzia ciliate EO displayed a toxic effect at concentrations of 7.79 mg/adult and 24.87 mg/larva against Tribolium castaneum [75]. EO from garlic cloves was found toxic to all stages of Tribolium castaneum and to the imago of Sitophilus zeamais. Complete destruction of T. castaneum eggs was achieved at a concentration of garlic oil 4.4 mg/cm² in a bioassay by filter paper impregnation method [76]. A major constituent of cinnamon essential oils, cinnamaldehyde (CA), was reported to exhibit antifungal and antibacterial activity against many mammalian and plant pathogens [77]. Pan et al. [78] have found that by deploying a specific antifungal mechanism, CA can inhibit the conidial viability of Fusarium solani at a concentration of 0.075 g/L. The study demonstrated that CA vapor of 0.3 g/L in the air can completely control F. solani development in sweet potatoes during storage for 10 days at 28 °C [78].

Effective formulations of secondary metabolites for applications as plant protection agents

There are several important obstructions which impede the wide applications of EOs in the food and agriculture sectors. They are unstable and degrade easily if they are not protected from external factors. The oxidation processes lead to the deterioration of their qualities and the generation of toxic products [79]. Formulations of botanical pesticides must be developed to overcome such main problems as water immiscibility of crude oils and instability of plant extracts aqueous solutions [80]. A step forward towards the development of a promising eco-friendly technology in crop protection was demonstrated by Khandelwal et al. [81] and Purkait et al. [80]. The former has proved the effectiveness of insecticidal formulation prepared from extracts of leaves of Azadirachta indica, Datura stramonium, Cascabela thevetia, and seeds of Annona squamosa against ballworm larvae in in-vitro experiments [81]. Purkait et al. [80] have obtained Emulsifiable Concentrate (EC) formulations that are suitable for seed oils. The formulations contained 40% seed extracts combined with 50% biodegradable solvents and 10% emulsifier blends and displayed bioefficacy comparable with the synthetic insecticides against Brevicoryne brassicae L, Aphis gossypii G., and Bemisia tabaci G. [80].

Designing suitable carriers for EO delivery by using nanoencapsulation is considered an efficient way to overcome the outlined restrictions [79]. Nanotechnology is an interdisciplinary field that deals with materials scaling in size to less than 100 nm, characterized by a large surface-to-volume ratio and unique physical and chemical properties [82]. In agriculture, nanomaterials can be applied as nanofertilizers and as pesticide carriers [83]. This innovative technique allows safe and precise delivery of agrochemicals, thus reducing the losses during the application stage. In recent years, the development of carrier systems has focused towards the reduction of pesticide concentrations [84].

In a recent review, Adeyemi et al. [85] summarize the trends and developments in the formulation of EOs based on polymeric nanoparticles (PNPs). The most appreciated advantages of the PNPs are their functionalization accessibility, easy integration into biological matrices, stability, and active ingredient transport to the target site with specified concentration and extended activity period. The authors provide a detailed classification of the PNPs according to their structural organization, absorptivity, and formulations. Biodegradable PNPs, which are well-tolerated and have no serious side effects, remain the most attractive candidates for efficient delivery. They are basically products of living organisms such as green plants, animals, bacteria, and fungi, like polysaccharides (pectin, cellulose, chitosan, etc.) and protein sources (albumin, gelatin, soy protein, hydrolysate, etc.) [85]. Like biopriming, which is the incorporation of biocontrol agents or biofertilizers in the seed, priming with plant extracts can improve uniform seed germination and increase the crop’s tolerance to pests and diseases [86]. Coating of durum wheat seeds with thyme oil increased their germination rate and enhanced seedling growth development. Furthermore, thyme oil enhanced the cultivar avoidance strategy by inducing root elongation and reducing the loss of shoot and root dry matter in response to progressive water/nutrient stress. This approach is suggested as a promising alternative for the enhancement of drought resistance in wheat [87].

Botanical-based biopesticides on the world market—overview

The regulation of natural substances as biopesticides applies only to the biochemicals that have a nontoxic mode of action. Other natural products are regulated as chemical pesticides because they either have a toxic mode of action, or are modified synthetically and, therefore, are no longer naturally identical [88].

There is a growing number of reports focused on the bioactivity of plant-based compounds on pests; however, the botanicals currently used in agriculture are far less [89]. At present, biopesticides based on animals, plants, and bacteria comprise about 5% of the total crop protection market worldwide, and the tendency is to grow by almost 10% every year. Compared to the USA, where over 200 products are available, Europe lags behind with 60 registered analogous biological pesticides [90]. For instance, bioinsecticides based on EOs have entered the European market in the past 5–6 years, while in the USA, such products have been used for over a decade [74]. This is due to several factors, like the high demand for organic products in the USA and the easy registration procedures for biopesticides [91].

The huge botanical insecticide market potential of the European Union is still insufficiently developed despite the existing high consumption of organic foods and the traditions for the use of plant-based medicines in Europe [92]. This is due mainly to the heavy legislation procedures, which are the same as those for synthetic pesticides. However, the European Commission recently recognized that it is necessary to expand the range of approved active substances that are non-chemical, low-risk or basic and, at the same time, are available to farmers, thereby reducing their dependence on the most dangerous active substances. Support has also been claimed for research projects to expand the scope of alternative pest control strategies, tools and technologies [93].

Nowadays, the USA, the EU, China, and Latin America are making extensive use of bioinsecticides derived from plant EOs or their chemical constituents. On a worldwide scale, the major botanical insecticides currently in commercial use are Pyrethrum, Azadirachtin from Neem, and EOs from various plant species. The majority of pyrethrum used in North America and Europe has been for non-agricultural use in homes and gardens, against wood-destroying pests and in public health. Nevertheless, the use of pyrethrins in plant protection has grown recently [94]. Among the botanicals with considerable antimicrobial activity that were successfully authorized and developed commercially are phenolics, terpenes, and alkaloids. Generally, they are perceived as chemicals with less or no negative impact compared to synthetic antifungal agents, including residual effects and induced resistance [91]. Their low or little toxicity suggests greater chances of success for the development of botanical fungicides by using plant-derived metabolites. Among the proven active substances are cinnamaldehyde, l-Glutamic acid, gamma-aminobutyric acid, Jojoba oil, EOs, and others [95].

Conclusions

Plants have evolved to synthesize a huge variety of secondary metabolites to cope with herbivores. The use of plants rich in active antimicrobial substances has been the foundation for traditional medicine systems and this has been extensively documented. Additionally, plants have been used in plant protection for thousands of years. The use of the multidisciplinary nanobiotechnology approach could facilitate the incorporation of plant secondary metabolites in different sustainable agricultural systems by providing suitable delivery formulations. More efforts should be put into the creation of novel, stable formulations of plant secondary metabolites with proven pesticidal activity. The loosened legislation and registration processes for plant-based pesticides could also prompt progress in the integration of botanical pesticides in sustainable plant protection.

Author contributions

All authors contributed significantly to the work and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. AL and LG made substantial contributions to the conception and design of the work. AL, LG, and VA were involved in project management, literature search, data acquisition, interpretation, drafting, and reviewing of the manuscript. LG and VA were involved in visualization. All authors read and approved the final manuscript.

Disclosure statement

No potential conflict of interest was reported by the authors.

Data availability statement

Data sharing is not applicable to this article as no new data were created or analyzed in this study.

Additional information

Funding

This work was supported by Operational Program Science and Education for Smart Growth 2014–2020, co-financed by the European Union through the European Structural and Investment Funds, Grant BG05M2OP001-1.002-0012 Sustainable utilization of bioresources, and waste of medicinal and aromatic plants for innovative bioactive products.