Bioscience Journal | 2022 | vol. 38, e38048 | ISSN 1981-3163 1 Vanessa Alves GOMES¹ , Carolina Alves GOMES² , Fabíola de Jesus SILVA³ , Márcio Santos SOARES4 , Everaldo Antonio LOPES5 1 Plant Protection/PhD in Agronomy, São Paulo State University, Botucatu, São Paulo, Brazil. 2 Crop Production/MSc in Agronomy, Federal University of Viçosa, Rio Paranaíba, Minas Gerais, Brazil. 3 Plant Pathology/PhD in Agronomy, Federal University of Lavras, Lavras, Minas Gerais, Brazil. 4 Department of Chemestry, Federal University of Viçosa, Rio Paranaíba, Minas Gerais, Brazil. 5 Department of Crop Production, Federal University of Viçosa, Rio Paranaíba, Minas Gerais, Brazil. Corresponding author: Vanessa Alves Gomes Email: vavvgomes@gmail.com How to cite: GOMES, V.A. et al. Extracts and purified substances of Cabralea canjerana inhibit hatching and extracts of Schinus terebinthifolius kill juveniles of meloidogyne incognita. Bioscience Journal. 2022, 38, e38048. https://doi.org/10.14393/BJ-v38n0a2022-53994 Abstract Nematicidal substances have been identified from plants and are potentially useful for the management of plant-parasitic nematodes. Cabralea canjerana, (Meliaceae) and Schinus terebinthifolius (Anacardiaceae) produce bioactive compounds during their secondary metabolism and little is known about the effect of such substances on plant-parasitic nematodes. In the present study, we assessed the effect of aqueous and ethanolic extracts of C. canjerana and S. terebinthifolius at 1% (m:v) and purified substances from C. canjerana (gedunin, ocotillone, cabraleadiol, a mixture of ocotillone + cabraleadiol and a mixture of shoreic acid + eichlerianic acid) on hatching and mortality of Meloidogyne incognita juveniles. Aqueous extracts of C. canjerana fruits and seeds reduced hatching by 70.3 to 95.7%. Aqueous extracts of S. terebinthifolius fruits killed 42.8 to 77.1% of juveniles. The purified substances of C. canjerana inhibited the hatching of M. incognita from 57 to 90% and did not increase the mortality of juveniles. Therefore, C. canjerana extracts and its purified substances reduce M. incognita hatching and aqueous extracts of S. terebinthifolius kill J2 of this nematode. Keywords: Botanical nematicides. Brazilian pepper tree. Plant extracts. Mortality. Root-knot nematode. 1. Introduction Root-knot nematodes are one of the main plant-pathogens worldwide, causing losses ranging from 20% to 100%, depending on population density, cultivar susceptibility, nematode species, soil texture, and environmental conditions (Nicol et al. 2011). In Brazil, Meloidogyne incognita (Kofoid and White) Chitwood and M. javanica (Treub) Chitwood are widespread over the country, damaging cash, and staple crops (Ferraz et al. 2010). The efficient management of RKN depends on the combination of different control strategies, including crop rotation, genetic resistance, physical methods, biological control and nematicides (Charchar et al. 2007; Neves et al. 2007; Silva and Pereira 2008; Jones et al. 2017; Gomes et al. 2020). Nematicidal substances can be produced by plants during their secondary metabolism and such substances may be useful for managing plant-parasitic nematodes (Ferraz et al. 2010). Essential oils, crude extracts, isolated compounds, and volatile organic compounds of several plant species have been reported to suppress or kill root-knot nematodes under greenhouse and field conditions. EXTRACTS AND PURIFIED SUBSTANCES OF Cabralea canjerana INHIBIT HATCHING AND EXTRACTS OF Schinus terebinthifolius KILL JUVENILES OF MELOIDOGYNE INCOGNITA https://orcid.org/0000-0003-0372-8083 https://orcid.org/0000-0002-6441-9543 https://orcid.org/0000-0002-1734-6521 https://orcid.org/0000-0002-8992-4693 https://orcid.org/0000-0002-5458-2312 Bioscience Journal | 2022 | vol. 38, e38048 | https://doi.org/10.14393/BJ-v38n0a2022-53994 2 Extracts and purified substances of Cabralea canjerana inhibit hatching and extracts of Schinus terebinthifolius kill juveniles of meloidogyne incognita Plant-origin compounds may kill active forms of nematodes, inhibit hatching, impair nematode movement, interfere with root location, or even activate plant defense mechanisms (Ferraz et al. 2010). A plethora of chemicals from plants may have nematicidal properties, including phenolic compounds, alkaloids, tannins, fatty acids, terpenes, among others (Neves et al. 2008; Gardiano et al. 2011; Mateus et al. 2014; Barros et al. 2019; Gomes et al. 2020; Silva et al. 2020a; Silva et al. 2020b). Cabralea canjerana belongs to the Meliaceae, the same family of the nematicidal plants: Neem (Azadirachta indica) and Chinaberry (Melia azedarach). A number of bioactive triterpenes and limonoids have been isolated from C. canjerana (Soares et al. 2004; Braga et al. 2006; Soares et al. 2006; Cazal et al. 2009). Schinus terebinthifolius belongs to the Anacardiaceae family and is grown as an ornamental plant. This species is rich in polyphenols, which are unevenly distributed in leaves, fruits, seeds, and bark (Feuereisen et al. 2017). Despite the richness of bioactive compounds found in C. canjerana and S. terebinthifolius, little is known about the potential of these plants as sources of nema ticidal substances. Thus, this work aimed to evaluate the nematicidal potential of extracts of C. canjerana and S. terebinthifolius and purified substances of C. canjerana against M. incognita. 2. Material and Methods Nematode inoculum The nematode M. incognita race 3 was multiplied and kept in roots of potted tomato (cv. Santa Clara) in the greenhouse. Nematode eggs were extracted by the technique of Hussey and Barker (1973), modified by Boneti and Ferraz (1981). Hatching chambers were prepared to obtain second-stage juveniles (J2) (Southey 1970). The concentration of eggs and juveniles was adjusted using Peters slide under an inverted microscope. Plant extracts preparation The aqueous and ethanolic extracts of C. canjerana and S. terebinthifolius were evaluated for their ability to inhibit hatching and kill M. incognita J2 in laboratory experiments. Leaves, branches, fruits, and seeds of C. canjerana and leaves and fruits of S. terebinthifolius were dried in a forced-air oven for 72 h at 45 °C (Table 1). The dried material was ground in a Willey mill to pass through a 1.27-mm mesh. The resulting crushed plant material (hereafter “plant powder”) was stored in hermetically sealed jars until use. Aqueous and ethanolic extracts were prepared for the extraction of secondary metabolites from plants. To obtain the aqueous extract, 1 g of plant powder was added in a beaker containing 100 mL of deionized water and kept in a water bath at 65 °C for 90 min. Then, the material was filtered through Whatman number 1 filter and a 0.45-μm nitrocellulose membrane. The filtrates were kept in amber glasses and stored in a refrigerator. To prepare ethanolic extracts, 1 g of plant powder was added to 100 mL of ethanol (96° GL), followed by grinding with a domestic blender for 1 minute at low speed. The grinding process was performed three times. The extracts were filtered through Whatman number 1 filter and a 0.45-μm nitrocellulose membrane and stored in a refrigerator. The final concentration of the extracts was 1% (m:v). Table 1. Plant used for preparing aqueous and ethanol extracts. Aqueous extracts Ethanolic extracts Cabralea canjerana Schinus terebinthifolius Cabralea canjerana Schinus terebinthifolius Leaves Leaves Leaves Leaves Branches Fruits Branches Fruits Fruits Fruits Seeds Seeds Nematicidal effect of aqueous and ethanolic extracts of Cabralea canjerana and Schinus terebinthifolius To investigate the anti-hatching activity of the extracts, 100 µL of egg suspension containing 30 eggs were placed in a well of ELISA plate. The cells were then filled with 100 μL of aqueous or ethanolic extract Bioscience Journal | 2022 | vol. 38, e38048 | https://doi.org/10.14393/BJ-v38n0a2022-53994 3 GOMES, V.A. et al. and 100 μL of phosphate saline buffer (16.0 g NaCl; 4.2 g Na2HPO4.7H2O; 0.4 g KH2PO4 and 0.4 g KCl pH 7.0). In the controls, the extracts were replaced by 100 μL of distilled water or ethanol (96° GL). The number of eggs and eventual J2 per cell was evaluated soon after the beginning of the experiment, with the aid of a light microscope with inverted objectives. The plates were then sealed with film paper and kept in an incubator at 27 ºC. Every 24 h, over a period of five days, the number of hatched juveniles was evaluated. In the experiments to evaluate the nematicidal effect of extracts on J2, the procedures were similar to hatching experiments. However, the inoculum was composed of 30 J2 and the numbers of mobile and immobile J2 were evaluated shortly after 5 days. After this period, immobile J2 were considered dead. The experiments with aqueous and ethanolic extracts were carried out twice, in a completely randomized design (CRD) in a 5 x 2 (control; leaf, branches, seeds or fruit extracts of C. canjerana x water or ethanol) or 3 x 2 (control; leaf or fruit extracts of S. terebinthifolius x water or ethanol) factorial scheme. Each treatment was repeated 10 times. Nematicidal effect of purified substances of Cabralea canjerana Cabraleadiol, eichlerianic acid, gedunin, ocotillone, and shoreic acid were extracted from C. canjerana according to Soares et al. (2006). Seed extracts were initially fractionated using the microcrystalline Cellulose-D stationary phase column chromatography technique and solvents in increasing order of polarity as eluents (hexane, CH2Cl2, AcOEt, and MeOH). This stationary phase was chosen because the extract had high polarity and a silica column could retain some secondary metabolites of interest in the study. 59 fractions were collected, which were grouped according to their similarities by comparison by CDDA, yielding 11 subfractions. Fruit extracts with greater mass than seed extracts were analyzed by the 1H NMR spectrum, which revealed the presence of triterpenes. Assuming that triterpenes were masking the signals of other more polar metabolites, 88.3 g of the extract was fractionated through a liquid-liquid partition. At the end of the partition, four extracts were obtained. These extracts were submitted to a liquid-liquid extraction with 120 mL of solution. The ethanolic fruit extract was fractionated in hexane, dichloromethane, ethyl acetate, or methanol and the substances were extracted according to Soares et al. (2006). The ethanolic seed extract was subjected to column chromatography using microcrystalline cellulose, where the mobile phase was composed of hexane/dichloromethane/ethyl acetate in increasing polarity order, resulting in eleven fractions. The chemical identification of the substances was performed according to Sarria et al. (2014). Two milligrams of each substance were diluted in a 3-μL solution containing 50% of water, 50% of ethanol, and one drop of Tween 20. The potential of gedunin, ocotillone, cabraleadiol, the mixtures of ocotillone + cabraleadiol, and a mixture of shoreic and eichlerianic acids in inhibiting hatching and killing second-stage juveniles of M. incognita was investigated following the same procedures as described for aqueous and ethanolic extracts. A solution containing water 50%, ethanol 50%, Tween 20, and without C. canjerana substances was used as control. The experiments with purified compounds of C. canjerana were carried out twice in a CRD with 10 replicates. Statistical Analysis The experiments were carried out in a completely randomized design (CRD) in a 5x2 and 3x2 factorial scheme. Data of all experiments were subjected to analysis of variance and means were compared by Tukey test (p = 0.05) using the statistical package R version 3.1.1 (R Core Team 2016). 3. Results and Discussion The effect of C. canjerana and S. terebinthifolius extracts on M. incognita hatching varied due to the interaction between the extracts and the solvents in both experiments (Tables 2 and 3). Aqueous extracts of leaves, branches, fruits, and seeds of C. canjerana reduced hatching in both experiments (Table 1). No ethanol extract of C. canjerana reduced hatching (Table 2). Aqueous extracts of C. canjerana fruits and seeds reduced hatching by 70.3 to 95.7% (Table 2). Bioscience Journal | 2022 | vol. 38, e38048 | https://doi.org/10.14393/BJ-v38n0a2022-53994 4 Extracts and purified substances of Cabralea canjerana inhibit hatching and extracts of Schinus terebinthifolius kill juveniles of meloidogyne incognita Aqueous extracts of leaves and fruit of S. terebinthifolius reduced hatching by more than 97% in the experiment 1 but had no effect in the experiment 2 (Table 3). No ethanolic extract of S. terebinthifolius reduced nematode hatching in both experiments. For both the plants, nematode hatching was lower when ethanol was used as solvent. Table 2. Effect of aqueous and ethanolic extracts of Cabralea canjerana on hatching of second-stage juveniles (J2) of Meloidogyne incognita race 3. Hatching (%) Extract Experiment 1 Experiment 2 Aqueous Ethanolic Aqueous Ethanolic Leaves 13.6Ab 13.8Aa 2.4Ac 0.6Aa Branches 15.5Ab 3.5Bb 15.0Ab 2.3Ba Fruits 6.5Ac 0.4Bb 5.9Ac 0.5Ba Seeds 4.2Ac 0.0Bb 3.6Ac 0.7Aa Control 21.9Aa 0.8Bb 83.7Aa 2.16Ba Means followed by the same uppercase letter in the row and lowercase in the column do not differ from each other by the Tukey test (p = 0.05). Table 3. Effect of aqueous and ethanolic extracts of Schinus terebinthifolius on hatching of second stage juveniles (J2) of Meloidogyne incognita race 3. Hatching (%) Extract Experiment 1 Experiment 2 Aqueous Ethanolic Aqueous Ethanolic Leaves 2.0Ab 1.2Aa 96.1Aa 1.2Ba Fruits 1.1Ab 1.1Aa 97.6Aa 2.0Ba Control 84.5Aa 2.16Ba 29.2Ab 0.8Ba Means followed by the same uppercase letter in the row and lowercase in the column do not differ from each other by the Tukey test (p = 0.05). The effect of C. canjerana and S. terebinthifolius extracts on mortality of J2 varied due to the interaction between types of extracts and solvents in both experiments (Tables 4 and 5). No aqueous extract of C. canjerana increased mortality of J2 (Table 4). In general, ethanolic extracts of C. canjerana and ethanolic control caused high mortality of juveniles. Aqueous extracts of S. terebinthifolius fruits killed 42.8 to 77.1% of juveniles (Table 5). Ethanolic extracts of S. terebinthifolius did not increase the mortality of J2 in comparison to ethanolic control (Table 5). Table 4. Effect of aqueous and ethanolic extracts of Cabralea canjerana on mortality of the second stage juveniles (J2) of Meloidogyne incognita race 3. Mortality (%) Extract Experiment 1 Experiment 2 Aqueous Ethanolic Aqueous Ethanolic Leaves 22.4Ab 33.8Ac 12.5Bc 54.5Aa Branches 54.2Aa 53.4Abc 34.5Bb 68.4Aa Fruits 17.0Bb 75.5Aa 13.3Bc 69.9Aa Seeds 49.0Aa 60.6Bab 29.2Bbc 66.9Aa Control 45.5Ba 72.4Aab 58.3Ba 72.5Aa Means followed by the same uppercase letter in the row and lowercase in the column do not differ from each other by the Tukey test (p = 0.05). Table 5. Effect of aqueous and ethanolic extracts of Schinus terebinthifolius on mortality of second-stage juveniles (J2) of Meloidogyne incognita race 3. Mortality (%) Extract Experiment 1 Experiment 2 Aqueous Ethanolic Aqueous Ethanolic Leaves 26.2Bb 71.5Aa 31.1Bb 72.2Ab Fruits 42.8Ba 85.9Aa 77.1Aa 79.8Aab Control 11.7Bb 84.7Aa 7.3Bc 92.6Aa Means followed by the same uppercase letter in the row and lowercase in the column do not differ from each other by the Tukey test (p = 0.05). Bioscience Journal | 2022 | vol. 38, e38048 | https://doi.org/10.14393/BJ-v38n0a2022-53994 5 GOMES, V.A. et al. All the purified substances of C. canjerana and mixtures inhibited hatching of M. incognita race 3 in both experiments, with no difference between them (Table 6). The inhibition ranged from 57 to 90%. However, no substance increased mortality of M. incognita J2 (Table 6). Table 6. Effect of purified substances of Cabralea canjerana on hatching and mortality of second-stage juveniles (J2) of Meloidogyne incognita race 3. Means followed by the same uppercase letter in the row and lowercase in the column do not differ from each other by the Tukey test (p = 0.05). Plants from the Meliaceae family produce several biocidal compounds. The nematicidal effect of extracts, essential oil, seed cake, and purified substances of neem (Azadirachta indica) has been widely reported (Silva and Pereira 2008; Ferraz et al. 2010; Oka 2010). Cabralea canjerana, a neglected species from the Meliaceae family, is rich in limonoids and triterpenes (Braga et al. 2006). Extracts of this plant have antifungal and insecticidal properties (Lopes et al. 2008; Smaniotto et al. 2010; Magrini 2011; Mata and Lomonaco 2013). Here, we observed that aqueous extracts of fruit and seeds and purified substances of C. canjerana reduce hatching and did not cause significant mortality of M. incognita J2. It is likely that the extracts and the purified substances have nematostatic rather than nematicidal activity on M. incognita. The lower mortality of nematodes exposed to aqueous extracts and purified substances of C. canjerana in comparison to the control can be a result of this nematostatic activity. After five days, the nematodes immobilized by the extracts and purified substances had higher body energy than those in water (control). As a result, the nematodes in the water remained moving, wasting energy, and, because of this, died sooner (Silva et al. 2018; Silva et al. 2019). The extracts of S. terebinthifolius had no activity on inhibiting hatching and aqueous extracts of this plant cause mortality of second-stage juveniles. Little is known about the properties of this plant in reducing plant-parasitic nematodes. In one of the few studies, Schwengber et al. (2017) reported the effect of the essential oil of this plant against Pratylenchus zeae in the greenhouse. Borges et al. (2018) also related to the suppression of root-knot nematode by S. terebinthifolius essential oil. It is likely that nematicidal compounds of S. terebinthifolius are concentrated in the essential oils. Further studies are required to elucidate which compounds found in aqueous extracts and essential oils and if the concentration of the aqueous extracts higher than 1% may provide a nematicidal effect against M. incognita (Silva et al. 2020a; Silva et al. 2020b). The ethanolic extracts were highly toxic against J2 but similar to control with ethanol only. However, ethanolic extracts did not reduce hatching in comparison to aqueous extracts. Such results support previous works that demonstrated the strong effect of ethanol solutions against plant-parasitic nematodes, especially on second-stage juveniles (Silva et al. 2017; Pedroso et al. 2019; Fujita et al. 2020). Ethanol may kill J2 (Silva et al. 2017). To better understanding the effect of C. canjerana substances on J2 and eggs of root-knot nematodes, researchers must consider diluting the compounds just in water and Tween 20. Botanical nematicides may be additional control tools in integrated management of plant-parasitic nematodes (Jardim et al. 2018; Silva et al. 2018; Gomes et al. 2020; Silva et al. 2020a; Silva et al. 2020b). The nematicidal potential of extracts and essential oils of a plethora of plant species have not been studied yet. Some plants can be sources of substances that may ultimately be active ingredients of plant -based nematicides. Here, we found that C. canjerana extracts and purified substances inhibit hatching of M. incognita J2, while S. terebinthifolius extracts kill the active forms of the nematode. These results should stimulate further research to evaluate whether formulations containing these extracts and compounds can be useful for the management of root-knot nematode under field conditions (Borges et al. 2018). Substance Hatching (%) Mortality (%) Experiment 1 Experiment 2 Experiment 1 Experiment 2 Gedunin 12.4b 19.1b 17.9b 18.5b Ocotillone 9.2b 6.1b 71.3a 76.0a Cabraleadiol 7.1b 9.8b 39.1b 39.9b Ocotillone + Cabraleadiol 12.5b 8.5b 31.3b 27.4b Shoreic acid + Eichlerianic Acid 4.1b 5.0b 35.1b 26.5b Control 42.5a 44.9a 70.5a 77.3a Bioscience Journal | 2022 | vol. 38, e38048 | https://doi.org/10.14393/BJ-v38n0a2022-53994 6 Extracts and purified substances of Cabralea canjerana inhibit hatching and extracts of Schinus terebinthifolius kill juveniles of meloidogyne incognita 4. Conclusions Cabralea canjerana aqueous extracts of fruits and seeds reduce Meloidogyne incognita race 3 hatching and aqueous extracts of seeds cause mortality of second-stage juveniles (J2) this nematode. All Purified substances of C. canjerana reduce M. incognita race 3 hatching and all purified, except ocotillone, kill J2 of this nematode. Schinus terebinthifolius aqueous extracts of fruits cause mortality of J2 of M. incognita race 3. Authors' Contributions: Gomes, V.A.: Definition of the theme, execution of activities and writing of the text. Gomes, C.A.: Assistance with laboratory activities. Silva, F.J.: Assistance in data analysis and interpretation. Soares, M.S.: Assistance in the production of extrac ts and purified substances. Lopes, L.A.: Definition of the theme and revision of the text. Conflicts of Interest: The authors declare no conflicts of interest. Ethics Approval: This study has been reviewed by all authors and all are in agreement. The study has not been tested in animals and humans. The study has not been published elsewhere. Acknowledgments: This research was supported by the FAPEMIG. E.A. Lopes thanks CNPq (Research Productivity Grant 306267/2018 -7). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Brazil - Finance Code 001. References BARROS, A.F., et al. Nematicidal screening of essential oils and potent toxicity of Dysphania ambrosioides essential oil against Meloidogyne incognita in vitro and in vivo. Journal of Phytopathology. 2019, 167, 380-389. https://doi.org/10.1111/jph.12803 BONETI, J.I.S. and FERRAZ, S. Modificação do método de Hussey and Barker para extração de ovos de Meloidogyne exigua de raízes de cafeeiro. Fitopatologia Brasileira. 1981, 6(3), 553. BORGES, D.F., et al. Nematicidal potential of essential oils of Ageratum fastigiatum, Callistemon viminalis and Schinus terebinthifolius. Bioscience Journal. 2018, 34(6), 90-96. https://doi.org/10.14393/BJ-v34n6a2018-39879 BRAGA, P.A.C., et al. Dammarane triterpenes from Cabralea canjerana (Vell.) Mart (Meliaceae): their chemosystematic significance. Biochemical, Systematics and Ecology. 2006, 34(4), 282-290. https://doi.org/10.1016/j.bse.2005.10.012 CAZAL, C.M., et al. Avaliação da atividade antitumoral de triterpenos damaranos de Cabralea canjerana. In: Reunião Anual da Sociedade Brasileira de Química- SBQ; Anais.. 2009, Fortaleza. CHARCHAR, J.M., et al. Efeito da rotação de culturas no controle de Meloidogyne spp. em cenoura na Região Norte do Estado de Minas Gerais. Nematologia Brasileira. 2007, 31(3), 173-179. FERRAZ, S., et al. Manejo sustentável de fitonematoides. 1st ed. Viçosa: Editora UFV, 2010. FEUEREISEN, M.M., et al. Pressurized liquid extraction of anthocyanins and biflavonoids from Schinus terebinthifolius Raddi: A multivariate optimization. Food chemistry. 2017, 214, 564-571. https://doi.org/10.1016/j.foodchem.2016.07.002 FUJITA, K., et al. Anaerobic soil disinfestation using diluted ethanol increases phosphorus availability in arable Andosols. Biology and Fertility of Soils. 2020, 2020, 1-15. GARDIANO, C.G., et al. Efeito de extratos aquosos de espécies vegetais sobre a multiplicação de Rotylenchulus reniformis Linford & Oliveira. Arquivos do Instituto Biológico. 2011, 78(4), 553-556. GOMES, V.A., et al. Activity of papaya seeds (Carica papaya) against Meloidogyne incognita as a soil biofumigant. Journal of Pest Science. 2020, 93, 783-792. https://doi.org/10.1007/s10340-020-01192-z HUSSEY, R.S. and BARKER, K.R.A. Comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Disease Reporter. 1973, 57(12), 1025-1028. JARDIM, I.N., et al. (E)-cinnamaldehyde from the essential oil of Cinnamomum cassia controls Meloidogyne incognita in soybean plants. Journal of Pest Science. 2018, 91, 479-487. https://doi.org/10.1007/s10340-017-0850-3 JONES, J.G., et al. Evaluation of nematicides for southern root-knot nematode management in lima bean. Crop Protection. 2017, 96, 151-157. https://doi.org/10.1016/j.cropro.2017.02.015 LOPES, E.M.C., et al. Screening for antifungal, DNA-damaging and anticholinesterasic activities of Brazilian plants from the Atlantic Rainforest: Ilha do Cardoso State Park. Revista Brasileira de Farmacognosia. 2008, 18, 655-660. https://doi.org/10.1590/S0102-695X2008000500002 https://doi.org/10.1111/jph.12803 https://doi.org/10.14393/BJ-v34n6a2018-39879 https://doi.org/10.1016/j.bse.2005.10.012 https://doi.org/10.1016/j.foodchem.2016.07.002 https://doi.org/10.1007/s10340-020-01192-z https://doi.org/10.1007/s10340-017-0850-3 https://doi.org/10.1016/j.cropro.2017.02.015 https://doi.org/10.1590/S0102-695X2008000500002 Bioscience Journal | 2022 | vol. 38, e38048 | https://doi.org/10.14393/BJ-v38n0a2022-53994 7 GOMES, V.A. et al. MAGRINI, F.E. Atividade biológica de extratos de Cabralea canjerana sobre Anastrepha fraterculus e Spodoptera frugiperda. Rio Grande do Sul: Universidade de Caxias do Sul, 2011. Dissertação de mestrado. MATA, R.F.F. and LOMONACO, C. Toxicidade, deterrência e repelência de extratos aquosos de Cabralea canjerana ssp. polytricha (A. Juss.) Penn. (Meliaceae) sobre o curuquere-da-couve Ascia monuste orseis (Godart) (Lepidoptera: Pieridae). Revista Árvore. 2013, 37(2), 261-268. https://doi.org/10.1590/S0100-67622013000200018 MATEUS, M.A.F., et al. Extratos aquosos de plantas medicinais no controle de Meloidogyne incognita (Kofoid e White, 1919) Chitwood, 1949. Bioscience Journal. 2014, 30(3), 730-736. NEVES, W.S., et al. Ação nematicida de óleo, extratos vegetais e de dois produtos à base de capsaicina, capsainoides e alil isotiocianato sobre Juvenis de Meloidogyne javanica (Treub) Chitwood. Nematologia Brasileira. 2008, 32(2), 93-100. NEVES, W.S., et al. Biofumigação do solo com espécies de brássicas para o controle de Meloidogyne javanica. Nematologia Brasileira. 2007, 31(3), 195-201. NICOL, J.M., et al. Current nematode threats to world agriculture. IN: JONES, J., GHEYSEN, G. and FENOLL, C. (Eds.). Genomics and molecular genetics of plant – nematodes interactions. Switzerland: Springer Science, 2011. pp. 21-43. OKA, Y. Mechanisms of nematode suppression by organic soil amendments—a review. Applied Soil Ecology. 2010, 44(2), 101- 115. https://doi.org/10.1016/j.apsoil.2009.11.003 PEDROSO, L.A., et al. Nematicidal activity of ethanol solutions on soybean cyst nematode Heterodera glycines. Nematology. 2019, 22(1), 111- 121. https://doi.org/10.1163/15685411-00003288 R CORE TEAM. R: The comprehensive R archive network. Vienna: R Foundation for Statistical Computing, 2016. Available from: https://cran.r- project.org/ SCHWENGBER, R.P., et al. Óleo essencial das folhas e frutos de Schinus terebinthifolius Raddi no controle de Pratylenchus zeae. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR. 2017, 20(3), 153-159. https://doi.org/10.25110/arqvet.v20i3.2017.6692 SARRIA, A.L.F., et al. Effect of triterpenoids and limonoids isolated from Cabralea canjerana and Carapa guianensis (Meliaceae) against Spodoptera frugiperda (J. E. Smith). Biosciences Zeitschrift für Naturforschung C. 2014, 66(5), 254-250. https://doi.org/10.1515/znc-2011-5-607 SILVA, M.F., et al. Medicinal plant volatiles applied against the root-knot nematode Meloidogyne incognita. Crop Protection. 2020a, 130(4), 1050-1057. https://doi.org/10.1016/j.cropro.2019.105057 SILVA, M.F., et al. Volatile emissions of watercress (Nasturtium officinale) leaves and passion fruit (Passiflora edulis) seeds against Meloidogyne incognita. Pest Management Science. 2020b, 76(4), 1413-1421. https://doi.org/10.1002/ps.5654 SILVA, J.C.P., et al. Performance of volatiles emitted from different plant species against juveniles and eggs of Meloidogyne incognita. Crop Protection. 2019, 116, 196-203, 2019. https://doi.org/10.1016/j.cropro.2018.11.006 SILVA, J.C.P., et al. Plant volatiles reduce the viability of the root-knot nematode Meloidogyne incognita either directly or when retained in water. Plant Disease. 2018, 102(11), 2170-2179. https://doi.org/10.1094/PDIS-01-18-0143-RE SILVA, J.C., et al. Toxicity of ethanol solutions and vapours against Meloidogyne incognita. Nematology. 2017, 19(3), 271-280. https://doi.org/10.1163/15685411-00003046. ISSN 1568-5411 SILVA, G.S. and PEREIRA, A.L. Efeito da incorporação de folhas de nim ao solo sobre o complexo Fusarium x Meloidogyne em quiabeiro. Summa Phytopathologica. 2008, 34(4), 368-370. https://doi.org/10.1590/S0100-54052008000400015 SMANIOTTO, L., et al. Bioatividade da Cabralea canjerana (Vell.) Mart. (Meliaceae) no controle de adultos de Acanthoscelides obtectus (Coleoptera, Bruchidae) em laboratório. Revista Biotemas. 2010, 23(2), 31-35. https://doi.org/10.5007/2175-7925.2010v23n2p31 SOARES, M.S., et al. Metabólitos secundários dos frutos de Cabralea canjerana, uma contribuição à quimiosistemática do gênero. In: Reunião Anual da Sociedade Brasileira de Química; Anais... 2006, 29, Águas de Lindóia. SOARES, M.S., et al. Triterpeno e limonoides isolados dos frutos de Cabralea canjerana. In: XXVI Reunião Anual sobre Evolução, Sistemática e Ecologia Micromoleculares; Anais... 2004, 26, 23-24, Niterói. SOUTHEY, J.F. Laboratory methods for work with plant and soil nematodes. 5th ed. London: Ministery of Agriculture, Fischeries and Food, 1970. https://doi.org/10.1590/S0100-67622013000200018 https://doi.org/10.1016/j.apsoil.2009.11.003 https://doi.org/10.1163/15685411-00003288 https://cran.r-project.org/ https://cran.r-project.org/ https://doi.org/10.25110/arqvet.v20i3.2017.6692 https://doi.org/10.1515/znc-2011-5-607 https://doi.org/10.1016/j.cropro.2019.105057 https://doi.org/10.1002/ps.5654 https://doi.org/10.1016/j.cropro.2018.11.006 https://doi.org/10.1094/PDIS-01-18-0143-RE https://doi.org/10.1163/15685411-00003046.%20ISSN%201568-5411 https://doi.org/10.1590/S0100-54052008000400015 https://doi.org/10.5007/2175-7925.2010v23n2p31 Bioscience Journal | 2022 | vol. 38, e38048 | https://doi.org/10.14393/BJ-v38n0a2022-53994 8 Extracts and purified substances of Cabralea canjerana inhibit hatching and extracts of Schinus terebinthifolius kill juveniles of meloidogyne incognita Received: 22 April 2020 | Accepted: 30 August 2021 | Published: 12 August 2022 This is an Open Access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.