Use of Schinus molle (Anacardiaceae) as a means of biological control against Trialeurodes vaporariorum (Aleyrodidae)

Amina Belhadji1,

Imane Abdelli2, 3,

Faiçal Hassani1

1 Laboratory of Ecology and Management of Natural Ecosystems, Faculty of SNV-STU, University of Tlemcen, BP 119, Imama, 13000 Tlemcen, Algeria

2 Laboratory of Natural and Bioactive Products (LASNABIO) Department of Chemistry, Faculty of Sciences, Abou Bekr Belkaïd University, BP119 Tlemcen 13000, Algeria

3 Graduate School of Applied Sciences Tlemcen, Algeria

Greenhouse whiteflies, Trialeurodes vaporariorum, are very small sucker-whipper-type pests of the family Aleyrodidae. They cause considerable damage to greenhouse crops in the first order and show resistance to chemical insecticides. In this context, we dedicated this study to the control of this pest through the active ingredients extracted from the leaf and fruit part of the pepper tree, Schinus molle by inhibiting the  chemosensory protein responsible mainly for capturing external stimuli in these polyphagous insects. By applying molecular modeling methods, including molecular docking, using software Molegro Virtual Docker version 2012.5.5.0, we tested the bioinsecticide potency of seven inhibitors. The  results obtained show that the  molecule beta-elemol is the best chemosensory protein inhibitor with a score of -82.6648 Kcal/mol and that it forms strong bonds with the active site amino acids of the protein.

Keywords: Trialeurodes vaporariorum, Schinus molle, chemosensory protein, molecular modeling, inhibitor, bioinsecticide


It is the law of nature that any living being will be the target of one or more enemies at one point in its life cycle (Suty, 2010; Yarou et al., 2017). Vegetable products are an essential component of our daily diet (James et al., 2010). They are, unfortunately, attacked by many types of insects, so the losses are considerable. This work contributes to the knowledge of the greenhouse whitefly, T. vaporariorum, commonly known as whitefly. T.  vaporariorum is a polyphagous insect (Malausa et al., 1988) of the sucker-whipper type ( of the order Hemiptera in the family Aleyrodidae. The greenhouse whitefly today seems to be cosmopolitan. It is found mainly in greenhouses and glass buildings. T.  vaporariorum attacks vegetables, fruits, ornamental plants (Bellmann, 2006), and even weeds (; it weakens them and stops their growth (Alford, 2012). Chemical insecticides are one of the  most widely used pests control methods (Regnault-Roger  et  al., 1997). However, greenhouse whiteflies are resistant to these insecticides, and chemical control is therefore inefficient ( The intensive use of insecticides has consequences for the  health of consumers: numerous studies report association between insecticides and carcinogenic diseases (prostate cancer, hematopoietic cancers), endocrine disruption, allergies, neurological and neurobehavioral effects, and effects on fertility and development (Inserm, 2013; Yarou et al., 2017). Insecticides also have negative impacts on the environment (surface and groundwater contamination, soil contamination, air contamination). The level of this impact depends on the degree of exposure resulting from their dispersions and concentrations in the environment and their ecotoxicological characteristics (Periquet et al., 2004; Yarou  et  al., 2017). Because of these risks to consumer health, the negative effect on the environment, and the  high cost of insecticides (Champ et al., 1977; White, Leesch, 1995; Subramanyam, Hagstrum, 1995), current research is moving towards biological control methods. Biological control is the use of living organisms or their products to control other organisms considered to be harmful. There are two categories of methods or means of biological control: means without recourse to auxiliaries and those who resort to them. The  biopesticide-based means of plant origin (James et al., 2010) had existed for a long time, but they were neglected with the advent of synthetic chemistry, mainly in the second half of the twentieth century. The use of biopesticides has many advantages: they restrict or eliminate the  use of chemical insecticides, are less toxic, reduce the risks of developing resistance, offer consumers healthy products, maintain the biodiversity of biotopes, and degrade rapidly, reduce the risk of pollution (Rochefort et al., 2006). The self-defence of plants lies in the subtle chemistry of their toxins: if a plant is not attacked by an insect, this is due to its chemical defence. Many herbs that we use in our recipes and herbal teas produce volatile insect-repellent products. Today, we have more than 2000 plant species that can keep pests away (Pintureau, 2009). The pepper tree, S. molle, of the family Anacardiaceae is an example of an insect-repellent aromatic tree due to its chemical compounds in leaves and fruits. The purpose of our work was to test theoretically the bioefficacy of the active principles of S. molle on greenhouse whiteflies, T. vaporari­orum, by molecular modeling methods.


Preparation of inhibitors

Our work consisted in studying the  interaction of the chemosensory protein (CSP) with a series of molecules extracted from the essential oils of the leaf part and fruit of the pepper tree, S.  molle. The  following inhibitors were studied: alpha-phellandrene, beta-elemol, limonene, beta-phellandrene, beta-eudesmol, alpha-eudesmol, and alpha-pinene. These inhibitors were chosen according to the  most important yield in each part of the plant, leaf or fruit. The chemical structure of the seven inhibitors was obtained from the PubChem database (Tables 1 and 2). In this study, we drew the seven inhibitors with the software Chem-Draw, v. and then saved them in the mol format. Then, we optimised these inhibitors with the  software HyperChem, v. 8.0.10 and saved them in the mol format. Regarding molecular docking, we did it using software Molegro Virtual Docker, v. 2012.5.5.0 with the aim of finding the best conformation between the chemosensory protein 1N8U and the  seven inhibitors, that is, we conducted a search for the most stable protein-inhibitor complex with the lowest energy level.

Table 1. Chemical structures of the essential oil compounds of S. molle fruits (

Chemical compounds Chemical structures
Beta-elemol img
Alpha-eu-desmol img

Table 2. Chemical structures of the essential oil compounds of S.  molle leaves (

Chemical compounds Chemical structures
Alpha-phellandrene img
Limonene img
Beta-phellandrene img
Beta-eudesmol img
Alpha-pinene img

Protein preparation

In our study, we downloaded the  chemosensory protein under access code 1N8U from the database Protein Data Bank with a resolution of 1.8 Å (Fig. 1), which is within the interval of 1.5-2.5 Å. It is composed of a single polypeptide chain with 112 amino acids (Table 3) (


Fig. 1. Three-dimensional structure of the CSP with the PDB code 1N8U (

We chose molecular modeling as a method for this study. This method is a bioinformatic tool that allows the  study of biological phenomena at the atomic scale. Today, molecular modeling is increasingly used to study chemical reactions and protein dynamics (Hercend, 2012). It aims to predict the structure and reactivity of molecules. ( The principle of molecular modeling consists in specifying, from calculations, the position of atoms in space and calculating the energy of the generated structure. The closest possible representation of reality will correspond to a  structure of lower energy. Molecular modeling involves theoretical calculation methods including molecular mechanics and molecular docking.

Table 3. Crystallographic data of the chemosensory protein 1N8U (

Protein 1N8U
Co-crystallization inhibitor img
Molecular weight (KDa) 11.69
Polymer 1
Chain A
Chain type Polypeptide (L)
Length of the sequence 112 amino acids
Resolution (Å) 1.8


Molecular docking. Using software Molegro Virtual Docker, v.2012.5.5.0, we have performed molecular docking between the  chemosensory protein under access code 1N8U and the seven inhibitors in cavity 1 (we chose this cavity because it represents the largest active site) to compare the stability of complexes trained (Fig. 2).


Fig. 2. Complexes formed after molecular docking

The score values of the first poses that designate the  conformations that best represent the seven inhibitors are given in Table 4.

The results of molecular docking led us to the following rankings:


From the score ranking we can conclude that the  1N8U-beta-elemol complex is the  most stable as it represents a  better affinity with the lowest energy level compared to the others. The  molecule bromo-dodecanol inhibitor of co-crystallization deactivates the function of the 1N8U protein. We note that there is not a big difference between the score values of the bromo-dodecanol (-103.714 Kcal/mol) and beta-elemol (-82.6648 Kcal/mol). So beta- elemol also deactivates the protein and inhibits it. We consider it a  good bioinsecticide against the polyphagous T. vaporariorum and that the fruits of S. moll have a good bioninsecticide power.

Table 4. Molecular docking scores

Inhibitors Score (Kcal/mol)
Alpha-phellandrene –63.6504
Beta-elemol –82.6648
Limonene –72.0394
Beta-phellandrene –68.7278
Beta-eudesmol –71.4398
Alpha-eudesmol –71.8688
Alpha-pinene –60.4802
Co-crystallisation inhibitor –103.714

Determination of interactions. We determined the  different amino acid interactions of cavity 1 of the 1N8U protein and the seven inhibitors using two software packages, Molegro Virtual Docker, v.2012.5.5.0 and BIOVIA Discovery Studio Visualizer, v. Figure 3 shows the interactions established by the Molegro Virtual Docker software:

The interactions established with the  BIOVIA Discovery Studio Visualizer software are represented in Fig. 4.


Fig. 3. Interactions between the amino acids in cavity 1 and the seven inhibitors. --- steric bonds; --- hydrogen bonds


Fig. 4. Hydrogen interactions between the  amino acids of cavity 1 and beta-elemol.
hydrogen bonds

The results of the interactions are represented in Table 5:

Based on the results in the table above, we observed that:

-  the  inhibitors formed steric interactions with the amino acids of cavity 1 of CSP 1N8U, apart from alpha-phellandrene, which did not form any interaction.

- beta-elemol formed two hydrogen bonds with glycine (GLY54) and glutamic acid (GLU63) of cavity 1.

- alpha-eudesmol formed a hydrogen bond with threonine (THR5).

As for the distances of the hydrogen bonds, we have as a rule:

• 2.5 Å < D < 3.1 Å => strong interaction;

• 3.1 Å < D < 3.55 Å => medium interaction;

• D > 3.55 Å => weak interaction (Imberty et al., 1991).

We then noticed that:

-  the  two hydrogen bonds between beta-elemol and the two amino acids GLY54, GLU63 belong to the range of strong interactions;

- the hydrogen bond formed between alpha-eudesmol and the THR5 amino acid belongs to the range of mean interactions.

We conclude that beta-elemol formed two steric bonds and two strong hydrogen bonds, which confirms its good complementarity with the 1N8U protein and the formation of a stable complex.

Cultivated plants would suffer considerable pre-harvest losses due to pests, diseases, and competitors. People must therefore protect their agricultural production, with respect to the  environment and without harming public health. Whiteflies cause very serious damage to the crops they attack. Adults and larvae sting and suck sap from the leaves, which eventually fade. Over time, the growth stunts and leaves fall. As is the  case with aphids, the  larvae of the  white fly also secrete a  sweet and sticky substance (honeydew) that causes the appearance and development of a fungus called sooty mold. The leaves of the plants are then covered with a  black or brown powder thus blocking photosynthesis; they turn yellow and die. In this context, the use of the pepper tree, S. molle (Anacardiaceae), as a means of biological control against T. vaporariorum (Aleyrodidae), pest of crops in greenhouses, was investigated. To this end, we applied molecular modeling methods, to theoretically, study the bioefficacy of the active principles extracted from the leaves and fruits of S. molle on the polyphagous T. vaporariorum; by inhibiting the  chemosensory protein: mainly responsible for capturing external stimuli in these harmful insects and facilitating communication between adults for reproduction. Benabdelkader (2012) showed that the insecticidal effectiveness of an essential oil is due to the nature and chemical structure of its constituents. Thus, Aiboud (2011) demonstrated a very interesting insecticidal activity with regard to the  fertility of female Calloso­bruchus maculates (Aiboud, 2011). Delimi et al. (2013) reported that the essential oil extracted from the  white wormwood, Artemisia herba alba, is considered a disruptive insecticide for reproduction. The  disruptive effect of some vegetable oils has been found by many studies. Thus our study on the effect of the essential oil of S. molle just confirms its disruptive effect on the  adults of T.  vaporariorum (Aleyrodidae). Senouci (2016) contributed to the  use of essential oils of medicinal plants: Marrubium vul­garis and Pistacia lentiscus (Anacardiaceae) as a means of fight against the pests of the olive tree. Our study confirms the insecticidal power of the Anacardiaceae family, of which S. molle is a part (Senouci, 2016). Bouayad Alam (2015) proved the  bio-insecticidal power of essential oils of some aromatic plants (Bouayad Alam, 2015) on another pest of greenhouse plants, Tuta absoluta. Agarwal  et  al. (2001) demonstrated the  toxicity and repellency of the 1,8-cineol compound in eucalyptus against Callosobruchus maculatus, Rhyzopertha domi­nica (Coleoptera: Bostrychidea), and Sarocladi­um oryzae. The recurrence rate of repellency of this chemotype towards these three insect pests ranged from 65% to 74% (Agarwal et al., 2001). Yarou et al. (2017) added that the use of pesticide plants was proving to be an ancestral practice in Africa. Indeed, many plants are known and used for their biocidal activities (toxic, repellent, anti-appetizing) towards a wide range of pests (Yarou et al., 2017). Our results are in agreement with those reported by many authors who highlighted the effectiveness of many essential oils applied as bio-insecticide. The remarkable insecticidal potential of S.  molle is due to the  presence of beta-elemol, which is present in its fruits and proves that it has the  bio-insecticidal power on the  greenhouse whitefly. Biocidal plants can be used as foliar extracts (Mochiah et al., 2011; Dela et al., 2014) or in combination with other crops (Asare-Bediako  et  al., 2014; Baidoo  et  al., 2012). We can thus propose our farmers replace the hitherto-used insecticides to fight the greenhouse whitefly T. vaporariorum with the essential oil of the pepper tree, S. mole, in biological fight or integrated fight, thus protecting our health and our environment.

Table 5. Distances and interactions between the amino acids of cavity 1 and the inhibitors

Inhibitors Steric bonds Hydrogen bonds
Amino acids Distance (À) Amino acids Distance (À)
Alpha-phellandrene HIS46 3.16 / /
Beta-elemol TYR4 3.02 GLY54 2.93
GLU42 2.74 GLU63 2.65
Limonene GLU 42 2.85 / /
Alpha-phellandrene / / / /
Beta-eudesmol GLU42 2.76 /
LEU43 3.00
Alpha-eudesmol LEU43 3.02 THR5 3.28
GLU42 2.90
GLN62 3.19 /
Alpha-pinene HIS46 2.99
LEU43 3.19 /
LEU43 3.14
TYR4 3.04


The purpose of our study was to test theoretically, by using molecular modeling methods, the  inhibitory activity of seven molecules extracted from the leaf and fruit parts of the pepper tree, S.  molle (Anacardiaceae), according to their highest yield with the  chemosensory protein in greenhouse whiteflies, T.  vaporari­orum (Aleyrodidae). Chemosensory protein is responsible for the  detection, transport of stimuli from the  external environment, and their solubilisation in the aqueous environment that surrounds the sensory neurons. The molecular docking with Molegro Virtual Docker v.2012.5.5.0 allowed us to evaluate the affinity between the  seven inhibitors and the  chemosensory protein with the PDB 1N8U code, and to retain the beta-elemol molecule as the best inhibitor of the  chemosensory protein with the  best score of -82.6648  Kcal/mol. The  results of the visualisation of the interactions between the seven inhibitors and the amino acids of the active site of the protein show that beta-elemol formed two strong hydrogen bonds and two steric bonds, which confirms the good complementarity between beta-elemol and the chemosensory protein and the formation of the most stable complex. Finally, after conducting an overview of the disadvantages of chemical insecticides on human health and the environment, the results obtained in the present led us to judge the molecule beta-elemol extracted from fruit of S. molle as nontoxic and it has no effects on human health. As a result, these results led us to propose this molecule as a possible new inhibitor of the  chemosensory protein and to confirm the bioinsecticidal power of S. molle fruit for the control of this harmful insect.

Received 22 August 2021

Accepted 3 November 2021


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* Corresponding author. Email:

Amina Belhadji, Imane Abdelli, Faiçal Hassani



Siltadarzinis baltasparnis (Trialeurodes vaporario­rum) yra labai mazas Aleyrodidae seimos vabzdys. Jis daro didelę zalą siltnamio augalams ir yra atsparus cheminiams insekticidams. Tyrimas skirtas sio kenkėjo kontrolei naudojant is pipirmedzio Schinus molle lapų ir vaisių dalių isgautas veikliąsias medziagas, kurios slopina polifaginių vabzdzių chemosensorinį baltymą, fiksuojantį isorinius dirgiklius. Taikydami molekulinio modeliavimo metodus, įskaitant molekulinę jungtį, naudojome programinę įrangą „Molegro Virtual Docker" (versija 2012.5.5.0) ir isbandėme septynių inhibitorių bioinsekticidinį stiprumą. Tyrimas rodo, kad esant -82,6648  Kcal/mol rezultatui, molekulė beta-elemolis sudaro stiprius rysius su baltymo veikliosios vietos aminorūgstimis ir yra geriausias chemosensorinio baltymo inhibitorius.

Raktazodziai: Trialeurodes vaporariorum, Schi­nus molle, chemosensorinis baltymas, molekulinis modeliavimas, inhibitorius, bioinsekticidas