{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,24]],"date-time":"2026-03-24T15:10:19Z","timestamp":1774365019162,"version":"3.50.1"},"reference-count":37,"publisher":"MDPI AG","issue":"13","license":[{"start":{"date-parts":[[2023,6,25]],"date-time":"2023-06-25T00:00:00Z","timestamp":1687651200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia (FCT\/MCTES)","doi-asserted-by":"publisher","award":["2022.00359.CEECIND"],"award-info":[{"award-number":["2022.00359.CEECIND"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia (FCT\/MCTES)","doi-asserted-by":"publisher","award":["UIDB\/00100\/2020"],"award-info":[{"award-number":["UIDB\/00100\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia (FCT\/MCTES)","doi-asserted-by":"publisher","award":["UIDP\/00100\/2020"],"award-info":[{"award-number":["UIDP\/00100\/2020"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001871","name":"Funda\u00e7\u00e3o para a Ci\u00eancia e a Tecnologia (FCT\/MCTES)","doi-asserted-by":"publisher","award":["IMS\u2014LA\/P\/0056\/2020 (CQE)"],"award-info":[{"award-number":["IMS\u2014LA\/P\/0056\/2020 (CQE)"]}],"id":[{"id":"10.13039\/501100001871","id-type":"DOI","asserted-by":"publisher"}]},{"name":"national funds","award":["2022.00359.CEECIND"],"award-info":[{"award-number":["2022.00359.CEECIND"]}]},{"name":"national funds","award":["UIDB\/00100\/2020"],"award-info":[{"award-number":["UIDB\/00100\/2020"]}]},{"name":"national funds","award":["UIDP\/00100\/2020"],"award-info":[{"award-number":["UIDP\/00100\/2020"]}]},{"name":"national funds","award":["IMS\u2014LA\/P\/0056\/2020 (CQE)"],"award-info":[{"award-number":["IMS\u2014LA\/P\/0056\/2020 (CQE)"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>Control of the pinewood nematode (PWN), the causal agent of pine wilt disease, can be achieved through the trunk injection of nematicides; however, many pesticides have been linked to environmental and human health concerns. Essential oils (EOs) are suitable alternatives due to their biodegradability and low toxicity to mammals. These complex mixtures of plant volatiles often display multiple biological activities and synergistic interactions between their compounds. The present work profiled the toxicity of eight EOs against the PWN in comparison to their 1:1 mixtures, to screen for successful synergistic interactions. Additionally, the main compounds of the most synergistic mixtures were characterized for their predicted environmental fate and toxicity to mammals in comparison to emamectin benzoate, a commercial nematicide used against PWN. The mixtures of Cymbopogon citratus with Mentha piperita and of Foeniculum vulgare with Satureja\u00a0montana EOs showed the highest activities, with half-maximal effective concentrations (EC50) of 0.09 and 0.05 \u00b5L\/mL, respectively. For these, complete PWN mortality was reached after only ca. 15 min or 2 h of direct contact, respectively. Their major compounds had a higher predicted affinity to air and water environmental compartments and are reported to have very low toxicity to mammals, with low acute oral and dermal toxicities. In comparison, emamectin benzoate showed lower nematicidal activity, a higher affinity to the soil and sediments environmental compartments and higher reported oral and dermal toxicity to mammals. Overall, uncovering synergistic activities in combinations of EOs from plants of different families may prove to be a source of biopesticides with optimized toxicity against PWNs.<\/jats:p>","DOI":"10.3390\/plants12132438","type":"journal-article","created":{"date-parts":[[2023,6,26]],"date-time":"2023-06-26T02:40:23Z","timestamp":1687747223000},"page":"2438","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["First Report on the Synergistic Interaction between Essential Oils against the Pinewood Nematode Bursaphelenchus xylophilus"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2817-7943","authenticated-orcid":false,"given":"Jorge M. S.","family":"Faria","sequence":"first","affiliation":[{"name":"INIAV, I.P., National Institute for Agrarian and Veterinary Research, I.P., Quinta do Marqu\u00eas, 2780-159 Oeiras, Portugal"},{"name":"MED, Mediterranean Institute for Agriculture, Environment and Development & CHANGE\u2014Global Change and Sustainability Institute, Institute for Advanced Studies and Research, \u00c9vora University, P\u00f3lo da Mitra, Ap. 94, 7006-554 \u00c9vora, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9466-2536","authenticated-orcid":false,"given":"Tom\u00e1s","family":"Cavaco","sequence":"additional","affiliation":[{"name":"INIAV, I.P., National Institute for Agrarian and Veterinary Research, I.P., Quinta do Marqu\u00eas, 2780-159 Oeiras, Portugal"},{"name":"Instituto Superior de Agronomia (ISA), Universidade de Lisboa, 1349-107 Lisboa, Portugal"}]},{"given":"Diogo","family":"Gon\u00e7alves","sequence":"additional","affiliation":[{"name":"INIAV, I.P., National Institute for Agrarian and Veterinary Research, I.P., Quinta do Marqu\u00eas, 2780-159 Oeiras, Portugal"},{"name":"Centro de Qu\u00edmica Estrutural, Institute of Molecular Sciences, Departamento de Qu\u00edmica e Bioqu\u00edmica, Faculdade de Ci\u00eancias, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal"}]},{"given":"Pedro","family":"Barbosa","sequence":"additional","affiliation":[{"name":"MED, Mediterranean Institute for Agriculture, Environment and Development & CHANGE\u2014Global Change and Sustainability Institute, Institute for Advanced Studies and Research, \u00c9vora University, P\u00f3lo da Mitra, Ap. 94, 7006-554 \u00c9vora, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6035-6656","authenticated-orcid":false,"given":"Dora Martins","family":"Teixeira","sequence":"additional","affiliation":[{"name":"HERCULES Laboratory, \u00c9vora University, Largo Marqu\u00eas de Marialva 8, 7000-809 \u00c9vora, Portugal"},{"name":"Science and Technology School, \u00c9vora University, Rua Rom\u00e3o Ramalho n\u00ba 59, 7000-671 \u00c9vora, Portugal"}]},{"given":"Cristina","family":"Moiteiro","sequence":"additional","affiliation":[{"name":"Centro de Qu\u00edmica Estrutural, Institute of Molecular Sciences, Departamento de Qu\u00edmica e Bioqu\u00edmica, Faculdade de Ci\u00eancias, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6883-5288","authenticated-orcid":false,"given":"Maria L.","family":"In\u00e1cio","sequence":"additional","affiliation":[{"name":"INIAV, I.P., National Institute for Agrarian and Veterinary Research, I.P., Quinta do Marqu\u00eas, 2780-159 Oeiras, Portugal"},{"name":"GREEN-IT Bioresources for Sustainability, Instituto de Tecnologia Qu\u00edmica e Biol\u00f3gica, Universidade Nova de Lisboa (ITQB NOVA), Av. da Rep\u00fablica, 2780-157 Oeiras, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2023,6,25]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Jaiswal, D.K., Gawande, S.J., Soumia, P.S., Krishna, R., Vaishnav, A., and Ade, A.B. (2022). Biocontrol Strategies: An Eco-Smart Tool for Integrated Pest and Diseases Management. BMC Microbiol., 22.","DOI":"10.1186\/s12866-022-02744-2"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1235773","DOI":"10.1126\/science.1235773","article-title":"The Consequence of Tree Pests and Diseases for Ecosystem Services","volume":"342","author":"Boyd","year":"2013","journal-title":"Science"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1163\/156854199508757","article-title":"First Report of Bursaphelenchus Xylophilus in Portugal and in Europe","volume":"1","author":"Mota","year":"1999","journal-title":"Nematology"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Zhao, B.G., Futai, K., Sutherland, J.R., and Takeuchi, Y. (2008). Pine Wilt Disease, Springer.","DOI":"10.1007\/978-4-431-75655-2"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"946","DOI":"10.1111\/mpp.12057","article-title":"Top 10 Plant-Parasitic Nematodes in Molecular Plant Pathology","volume":"14","author":"Jones","year":"2013","journal-title":"Mol. Plant Pathol."},{"key":"ref_6","unstructured":"Kamata, N. (2008). Pine Wilt Disease, Springer."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.ibiod.2013.08.024","article-title":"Wood Penetration Ability of Hydrogen Cyanide and Its Efficacy for Fumigation of Anoplophora glabripennis, Hylotrupes bajulus (Coleoptera), and Bursaphelenchus xylophilus (Nematoda)","volume":"86","author":"Stejskal","year":"2014","journal-title":"Int. Biodeterior. Biodegrad."},{"key":"ref_8","first-page":"126","article-title":"Efficacy of Four Nematicides against the Reproduction and Development of Pinewood Nematode, Bursaphelenchus Xylophilus","volume":"47","author":"Bi","year":"2015","journal-title":"J. Nematol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1080\/13102818.2023.2166869","article-title":"Plant Extracts and Trichoderma Spp: Possibilities for Implementation in Agriculture as Biopesticides","volume":"37","author":"Lyubenova","year":"2023","journal-title":"Biotechnol. Biotechnol. Equip."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Malik, S. (2019). Essential Oil Research, Springer International Publishing.","DOI":"10.1007\/978-3-030-16546-8"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/S1226-8615(08)60289-7","article-title":"Nematicidal Activity of Plant Essential Oils against Bursaphelenchus Xylophilus (Nematoda: Aphelenchoididae)","volume":"9","author":"Kong","year":"2006","journal-title":"J. Asia. Pac. Entomol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Faria, J.M.S., Barbosa, P., Vieira, P., Vicente, C.S.L., Figueiredo, A.C., and Mota, M. (2021). Phytochemicals as Biopesticides against the Pinewood Nematode Bursaphelenchus Xylophilus: A Review on Essential Oils and Their Volatiles. Plants, 10.","DOI":"10.3390\/plants10122614"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1002\/ps.2070","article-title":"Synergistic and Antagonistic Interactions of Terpenes against Meloidogyne incognita and the Nematicidal Activity of Essential Oils from Seven Plants Indigenous to Greece","volume":"67","author":"Ntalli","year":"2011","journal-title":"Pest Manag. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3989","DOI":"10.3390\/molecules17043989","article-title":"Essential Oils in Combination and Their Antimicrobial Properties","volume":"17","author":"Juliani","year":"2012","journal-title":"Molecules"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1627","DOI":"10.1002\/etc.5620150929","article-title":"Evaluating the Environmental Fate of a Variety of Types of Chemicals Using the EQC Model","volume":"15","author":"Mackay","year":"1996","journal-title":"Environ. Toxicol. Chem."},{"key":"ref_16","unstructured":"National Library of Medicine (2023, March 29). PubChem, Available online: https:\/\/pubchem.ncbi.nlm.nih.gov\/."},{"key":"ref_17","unstructured":"University of Hertfordshire (2023, March 29). PPDB: Pesticide Properties DataBase. Available online: http:\/\/sitem.herts.ac.uk\/aeru\/ppdb\/en\/."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.phytochem.2013.06.005","article-title":"Bioactivity against Bursaphelenchus Xylophilus: Nematotoxics from Essential Oils, Essential Oils Fractions and Decoction Waters","volume":"94","author":"Faria","year":"2013","journal-title":"Phytochemistry"},{"key":"ref_19","first-page":"35","article-title":"Nematicidal Activity of Monoterpenoids against the Pine Wood Nematode (Bursaphelenchus xylophilus)","volume":"15","author":"Choi","year":"2007","journal-title":"Russ. J. Nematol."},{"key":"ref_20","unstructured":"Trent University (2023, March 29). Level I Model. Available online: https:\/\/www.trentu.ca\/cemc\/resources-and-models\/level-i-model."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1163\/156854105775142946","article-title":"Nematicidal Activity of Plant Essential Oils and Components from Garlic (Allium sativum) and Cinnamon (Cinnamomum verum) Oils against the Pine Wood Nematode (Bursaphelenchus xylophilus)","volume":"7","author":"Park","year":"2005","journal-title":"Nematology"},{"key":"ref_22","first-page":"8","article-title":"Nematicidal Activity of Essential Oils and Volatiles Derived from Portuguese Aromatic Flora against the Pinewood Nematode, Bursaphelenchus xylophilus","volume":"42","author":"Barbosa","year":"2010","journal-title":"J. Nematol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"12312","DOI":"10.3390\/molecules171012312","article-title":"Bioassays against Pinewood Nematode: Assessment of a Suitable Dilution Agent and Screening for Bioactive Essential Oils","volume":"17","author":"Barbosa","year":"2012","journal-title":"Molecules"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"9471","DOI":"10.1038\/s41598-019-45908-3","article-title":"Combinations of Plant Essential Oil Based Terpene Compounds as Larvicidal and Adulticidal Agent against Aedes aegypti (Diptera: Culicidae)","volume":"9","author":"Sarma","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/j.indcrop.2014.06.030","article-title":"Acute, Synergistic and Antagonistic Effects of Some Aromatic Compounds on the Spodoptera littoralis Boisd. (Lep., Noctuidae) Larvae","volume":"60","author":"Pavela","year":"2014","journal-title":"Ind. Crop. Prod."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"3835","DOI":"10.1007\/s00436-015-4614-9","article-title":"Acute Toxicity and Synergistic and Antagonistic Effects of the Aromatic Compounds of Some Essential Oils against Culex Quinquefasciatus Say Larvae","volume":"114","author":"Pavela","year":"2015","journal-title":"Parasitol. Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/j.vetpar.2017.06.008","article-title":"Synergistic Interaction of Ten Essential Oils against Haemonchus Contortus In Vitro","volume":"243","author":"Katiki","year":"2017","journal-title":"Vet. Parasitol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1163\/15685411-bja10014","article-title":"Synergism of Citral from Cymbopogon Citratus Essential Oil and Undecan-2-One against Meloidogyne incognita","volume":"22","author":"Barros","year":"2020","journal-title":"Nematology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1163\/156854107780739018","article-title":"Nematicidal Activity of Onion (Allium cepa) Oil and Its Components against the Pine Wood Nematode (Bursaphelenchus xylophilus)","volume":"9","author":"Shin","year":"2007","journal-title":"Nematology"},{"key":"ref_30","unstructured":"WHO (2023, March 29). Evaluations of the Joint FAO\/WHO Expert Committee on Food Additives (JECFA). Available online: https:\/\/apps.who.int\/food-additives-contaminants-jecfa-database\/Home."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2493","DOI":"10.1016\/j.fct.2008.04.006","article-title":"Toxicity and Gastric Tolerance of Essential Oils from Cymbopogon Citratus, Ocimum Gratissimum and Ocimum Basilicum in Wistar Rats","volume":"46","author":"Fandohan","year":"2008","journal-title":"Food Chem. Toxicol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1146\/annurev.ento.51.110104.151146","article-title":"Botanical Insecticides, Deterrents, and Repellents in Modern Agriculture and an Increasingly Regulated World","volume":"51","author":"Isman","year":"2006","journal-title":"Annu. Rev. Entomol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1111\/jen.13039","article-title":"Carvone and Citral, Two Promising Compounds for Controlling the Honey Bee Ectoparasitic Mite, Varroa Destructor","volume":"146","author":"Sabahi","year":"2022","journal-title":"J. Appl. Entomol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1007\/s00425-015-2257-9","article-title":"In Vitro Co-Cultures of Pinus Pinaster with Bursaphelenchus Xylophilus: A Biotechnological Approach to Study Pine Wilt Disease","volume":"241","author":"Faria","year":"2015","journal-title":"Planta"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1111\/j.1744-7348.1965.tb07864.x","article-title":"A Comparison of Some Quantitative Methods of Extracting Small Vermiform Nematodes from Soil","volume":"55","author":"Whitehead","year":"1965","journal-title":"Ann. Appl. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1017\/S0890037X00023253","article-title":"Log-Logistic Analysis of Herbicide Dose-Response Relationships","volume":"9","author":"Seefeldt","year":"1995","journal-title":"Weed Technol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Faraone, N., Hillier, N.K., and Cutler, G.C. (2015). Plant Essential Oils Synergize and Antagonize Toxicity of Different Conventional Insecticides against Myzus persicae (Hemiptera: Aphididae). PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0127774"}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/13\/2438\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:00:11Z","timestamp":1760126411000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/12\/13\/2438"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,25]]},"references-count":37,"journal-issue":{"issue":"13","published-online":{"date-parts":[[2023,7]]}},"alternative-id":["plants12132438"],"URL":"https:\/\/doi.org\/10.3390\/plants12132438","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,25]]}}}