Worldwide, agriculture has problems related to soil fertility, especially to pests and diseases that significantly contribute to annual losses in crop yield (FAO, 2020). The application of chemical pesticides is an effective control method for plant pests and diseases that increase agricultural production but represents a serious threat to public health and the environment (Bonner and Alavanja, 2017). This problem has affected African agricultural systems worldwide.

The African population is estimated at 1.3 billion and is expected to double by 2050 (Searchinger et al., 2019), compromising African food production systems with low productivity. Agricultural pesticides can increase crop production, improve nutrition, raise household income, facilitate local and international trade, and control mosquitoes in Africa. However, the use of pesticides in Africa has polluted freshwater sources (Nesser et al., 2016; Osoro et al., 2016), endangered wildlife (Ogada, 2014), and beneficial organisms (Vak and Koomen, 2013), and pesticide residues greater than the recommended daily intake have been found in cooked food samples (Ogah, 2012). In addition, European green agriculture standards have created trade barriers for African farmers. In this context, new safe biopesticides are needed to improve crop protection, food safety, and trade, while being locally available and sustainable (Fortuna, 2022).

Plant-based biopesticides, including compounds, extracts, and essential oils, are an important group of safer products for pest management. Their chemical composition is complex limiting the development of resistance by target pests. Therefore, plant-based biopesticides are promising and safer crop protection alternatives with unique chemical compositions and modes of action (Khursheed et al., 2022).

Species of the genus Drypetes of the Putranjivaceae family are used in traditional medicines in subSaharan Africa and Asia, and some are used against pests (Wansi et al., 2016). Drypetes gossweileri S. Moore is a medium-sized dioecious (30 m–42 m in height; bole straight, up to 120 cm in diameter) species found in the Democratic Republic of Congo (DRC), Gabon, Equatorial Guinea, Central African Republic, and Cameroon. The bark is used as an analgesic for venereal diseases, urethral problems, reptile-repellent, fish poisoning, anthelminthic, vermifugal, and antifilarial (Wansi et al., 2016), and to protect stored food against pests (Aba et al., 2013). The essential oil of D. gossweileri is known for its antimycobacterial (Moni et al., 2018), antimicrobial (Moni et al., 2018; Graf and Stappen, 2022), and antifungal activities (Ghislaine et al., 2013).

Phyochemical studies of D. gossweileri extracts have shown the presence of friedelanes, oleananes, diterpenoids, and phenylethanoids (Wansi et al., 2016). Glucosinolates (GSLs) such as 4-hydroxybenzyl-glucosinolate and benzyl glucosinolate have been identified in the bark of D. gossweileri (Montaut et al., 2017). The essential oil (EO) from this plant species contains isothiocyanates (ITCs), benzyl isothiocyanate (Ndoye Foe et al., 2016), and benzyl cyanide (Agnaniet et al., 2003) as major components, which originate from hydrolysis of their precursor GSLs. Glucosinolates (GSL, β-thioglucoside-N-hydroxysulfates) are the precursors of isothiocyanates and are converted to ITCs after plant tissue damage by the action of the enzyme myrosinase. Glucosinolates and isothiocyanates are widely recognized as defensive compounds against generalist herbivores, are involved in host plant recognition by specialist predators (Hopkins et al., 2009), and have nematicidal properties (Wu et al., 2011; Ntalli and Caboni, 2017). Most of these compounds have been associated with many beneficial effects on human health, such as anticancer, antibacterial, antidiabetic, anti-obesity, antifungal, antioxidant, and antimutagenic activities (Di Gioia et al., 2020).

As part of an ongoing project exploring the pesticidal potential of African medicinal plants for local farmers, we assessed the essential oil obtained from D. gossweileri sourced from the Kisangani region in the Democratic Republic of the Congo (DRC). This study aimed to determine its efficacy as a biopesticide against various insect pests (Rhopalosiphum padi, Myzus persicae, and Spodoptera littoralis) and a phytoparasitic nematode (Meloydogine javanica) of economic importance. The moth S. littoralis (Egyptian cotton leafworm) feeds on a wide range of horticultural crops (Muñoz-Rodríguez et al., 2018). The aphid M. persicae affects many plant species with a particular affinity for Brassicaceae crops (Kim and Jander, 2007). The cereal aphid R. padi is a major pest of cereals (Greenslade et al., 2016). The root-knot nematode, M. javanica, which is present in temperate and tropical regions, is the most destructive nematode because of the formation of galls in the host roots. In the DRC, M. javanica attacks several crops (beans, soybeans, and tomatoes), contributing to more than 5% of crop loss (Chaudhary et al., 2019; Alekcevetch et al., 2021).

In this work, the phytochemical composition of D. gossweileri essential oil from the Kisangani region (DRC) has been studied along with its bioactivity against S. littoralis, M. persicae, R. padi, and M. javanica. We also tested the phytotoxicity of this EO on ryegrass (Lolium perenne) and tomato (Solanum lycopersicum) plants. The most significant effect was nematicidal activity. Molecular docking was used to study the major EO involved in this nematicidal effect.

The essential oil yield from D. gossweileri leaves was 0.55%. Yields of 0.2% and 0.29% have been previously reported for bark essential oils (Eyele Mvé-Mba et al., 1997). The composition of the essential oil of D. gossweileri leaves from Kisangani was largely dominated by benzyl isothiocyanate followed by benzyl cyanide. Similar results have been reported for the composition of D. gossweileri stem bark EO from Cameroon (Ndoye Foe et al., 2016), with benzyl isothiocyanate as the main compound, followed by benzyl cyanide. However, benzyl cyanide (73.7%) was the main compound in the D. gossweileri bark EO from Gabon (Agnaniet et al., 2003). Benzyl isothiocyanate has been reported in bark essential oil (Eyele Mvé-Mba et al., 1997; Voundi et al., 2015). These variations may be related to plant origin, plant parts used, or the distillation process that causes thermal degradation of glucosinolates (GL). Previous studies showed the presence of 4-hydroxybenzyl (12.5%) and benzyl GL (87.5%) in the bark and 4-hydroxybenzyl GL in the seeds of D. gossweileri (Montaut et al., 2017).

In this study, D. gossweileri leaf essential oil, rich in benzyl ITC, was used as an insect antifeedant with effective doses that varied with the insect species and feeding adaptation (lower effect against the polyphagous S. littoralis: 29 μg/cm², and M. persicae: 15 μg/cm², and stronger against the oliphagous R. padi: 8 μg/cm²). Similarly, previous studies have shown that two generalist (S. frugiperda and Trichoplusia ni) lepidopterans were adapted to feed on allyl and benzyl isothiocyanate-containing crucifers because these compounds are metabolized by glutathione transferase present in the generalist and absent in the specialist insect species (Anticarsia gemmatalis) (Wadleigh and Yu, 1988). Isothiocyanates (ITCs), released from Brassicaceae plants after hydrolysis of glucosinolates, are known for their negative effects on insect herbivores (Hopkins et al., 2009) and have been proposed for isothiocyanate-based biofumigation, being aliphatic isothiocyanates stronger fumigants than the aromatic ones because of their lower volatility (Matthiessen and Shackleton, 2005). Therefore, the lower volatility of benzyl isothiocyanate could be advantageous for formulation purposes.

The essential oil of D. gossweileri, rich in benzyl isothiocyanate, was lethal to M. javanica J2. At MLC concentrations and below (0.03 mg/mL–0.015 mg/mL) this oil strongly inhibited egg hatching in vitro, and in soil treatment (in vivo) caused strong suppression (100%–98%) of nematode egg masses, egg production, infection frequency and multiplication rate in tomato plants. Glucosinolates and isothiocyanates (such as benzyl isothiocyanate) have been reported in the literature as having nematicidal properties (Wu et al., 2011). Soil biofumigation with ITC-producing Brassiccaceae has been proposed for the control of Meloidogyne species in the context of Integrated Pest Control Management strategies (Ntalli and Caboni, 2017). Essential oil from the seeds of Carica papaya showed in vitro nematicidal activity against Caenorhabditis elegans and M. incognita, with benzyl isothiocyanate being responsible for the activity (Nagesh et al., 2002). Benzyl isothiocyanate showed strong in vitro nematicidal activity against M. incognita J2 (LD_{50 =} 15.21 μM) (Lazzeri et al., 2004). The infectivity of treated (0.01 mM) M. incognita juveniles on soybean (Glycine max) was significantly reduced, and egg production was almost eliminated by 0.03 mM benzyl isothiocyanate (Zasada et al., 2009). Reproduction and infectivity of M. incognita were suppressed when juveniles (J2) were exposed to 0.03 mM benzyl isothiocyanate for 2 h prior to inoculation with either C. annuum or G. max (Masler et al., 2010). However, the mode of nematicidal action of these isothiocyanates remains unknown.

It has been suggested that isothiocyanate interacts with cellular proteins and amino acids through oxidation reactions. Potassium ion homeostasis is reported in the literature to be a key factor in the maintenance of many vital functions in living beings. Indeed, the transport of this ion across the biological membrane is coupled to that of the chloride ion and ensured by cation-chloride protein co-transporters. It is involved in the change of the cellular response to the neuromodulator gamma amino butyric acid (GABA), which is the basis for the transition from a depolarizing effect to a hyperpolarizing effect, with the consequent inhibition of neurotransmission (Lesage et al., 2000). This bioelectric phenomenon, necessary for neuron maturation, was exploited in this study as a pharmacological target of the compounds contained in the essential oil of D. gossweileri. Thus, in the present study, we demonstrated through molecular modeling that the bioactive compounds of this essential oil form a thermodynamically stable complex with the protein receptor KCC3 (ΔG <0) in the same order of importance as that of the positive control (thiirane). In addition, all these compounds (as well as the positive control) formed a hydrogen bond with the receptor at the protein C subunit, demonstrating the synergistic effect of the bioactive compounds of this essential oil. Thus, the interaction of these compounds with the KCC 3 receptor would result in the inhibition of neuronal maturation (synaptic inhibition) via modification of the electrochemical properties of the biological membrane and thus the membrane transport of chloride ions, hence the increase in neuronal excitability, which could justify the (neuro) toxic effects observed in nematodes under our experimental conditions. The mechanism proposed in this study is derived from the principles of previous experiments with C. elegans, a nematode used as an experimental model/system in molecular biology to understand cell differentiation phenomena (Leung et al., 2008). Thus, neuronal maturation in C. elegans under the physiological action of GABA via the co-transporter KCC is a fundamental property common to all nematodes (including M. javanica). This biological property, being well preserved in this taxonomic group during ontological evolution, allows us to extrapolate the knowledge on GABA receptors to root-knot nematode species (M. javanica) as a pharmacological target of interest, under the postulate of the uniformity of biological processes that are the basis of cell function.

Molecular docking-based understanding of the bioactivity of EOs is a novel tool for the selection of natural products and discovery of biopesticidal leads. For example, in silico analysis suggested a higher binding capacity of geraniol, β-terpineol, citronellal l-limonene, γ-terpinene to ODR1 (odorant response gene 1) complex due to extensive H-bonding, hydrophobic, and p-alkyl interactions among a selection of target proteins (cytochrome c oxidase subunit 1, AChE, Hsp90, ODR1, ODR3, neuropeptide GPCR, and CLAVATA3/ESR (CLE)-related) of the nematode M. incognita, which was confirmed in vitro (Kundu et al., 2021). Therefore, in vitro/in vivo effects and computational bioefficacy analyses of EO chemical profiles can provide useful insights into the potential of EOs as bionematicides.

In light of our results, mustard EO from the leaves of the medicinal plant D. gossweileri, characterized by benzyl isothiocyanate (BITC), could be used as a safe alternative to synthetic chemical products. Therefore, ITCs are potentially toxic to humans. Specifically, BITC has been shown to cause genotoxicity, chromosomal aberrations, and DNA damage (Masutomi et al., 2001). BITC was orally administered (200 mg/kg daily for 4 weeks) to rats, with alterations in hematological parameters. However, BITC has been proposed as an anticancer agent and is considered safe for consumption (Dinh et al., 2021). Therefore, essential (mustard) oils from tropical forests are credible alternatives to synthetic chemical products. The Democratic Republic of Congo, a sanctuary of medicinal plants, is therefore a source of biologically active chemical compounds that can be exploited as biopesticides. To prevent deforestation and reduce human pressure on natural forests, large-scale cultivation (domestication) of this wild plant should be considered in a project to create a productive ecosystem for a sustainable supply of raw materials. Indeed, in the context of biodiversity loss linked to human activities and environmental factors (climate change), safeguarding natural resources must involve the implementation of efficient management and conservation strategies. A processing unit for this medicinal and aromatic plant can also facilitate socioeconomic development through an industrial agronomic initiative. The domestication of wild plants helps fight deforestation and climate change by creating a carbon sink to reduce greenhouse gases, as recommended by the Kyoto Protocol (Atangana et al., 2014).

The aim of the present study was to determine the chemical composition of the essential oil of a tropical plant, D. gossweileri S. Moore, and to evaluate its insecticidal and nematicidal effects against insect pests (S. littoralis, M. persicae, and R.padi), and the root-knot nematode M. javanica. GC/MS analysis of the essential oil of D. gossweileri indicated the presence of benzyl isothiocyanate as the major component followed by small amounts of benzyl cyanide, benzyl isocyanate, benzyl chloride, and α-pinene. ITC found in the EO is derived from the hydrolysis of the parent glucosinolate present in the leaf tissue. This mustard essential oil showed significant species-dependent insect antifeedant effects, strong in vitro and in vivo nematicidal activity, and low phytotoxicity against tomato plants. The major EO components (benzyl isothiocyanate, benzyl cyanide, and benzyl isocyanate) are believed to act by inhibiting the KCl cotransporter.

Mustard EO from the leaves of the medicinal plant D. gossweileri could be used as a safe alternative to synthetic chemical pesticides (insecticides and nematicides applied to the soil). Further research is needed to develop productive agroforestry systems for the sustainable production of D. gossweileri oil-based medicinal and biopesticidal ingredients along with optimized formulations.

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/supplementary material.

JM: Investigation, Formal Analysis, Writing – original draft. MA: Formal Analysis, Investigation, Supervision, Writing – review & editing. EK: Investigation, Writing – original draft, Methodology. NK: Investigation, Methodology, Writing – original draft. DDT: Investigation, Writing – original draft, Formal Analysis. KN: Investigation, Methodology, Writing – original draft. DTT: Investigation, Writing – original draft, Methodology. OO: Investigation, Methodology, Writing – original draft. AG-C: Investigation, Writing – original draft, Funding acquisition, Resources, Supervision, Writing – review & editing. PM: Conceptualization, Investigation, Methodology, Resources, Supervision, Validation, Writing – original draft, Writing – review & editing.