{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T11:02:34Z","timestamp":1789383754784,"version":"build-2803163510"},"reference-count":46,"publisher":"MDPI AG","issue":"18","license":[{"start":{"date-parts":[[2026,9,13]],"date-time":"2026-09-13T00:00:00Z","timestamp":1789257600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Plants"],"abstract":"<jats:p>The root-knot nematode Meloidogyne incognita poses a major challenge to global crop production, yet sustainable management options remain limited. We evaluated a collection of Clonostachys rosea isolates for their antagonistic potential using a stepwise approach that included in vitro assays, in planta tests, and greenhouse trials. Clear strain-dependent differences in biocontrol activity were observed across the different experimental stages. In vitro, several isolates strongly inhibited egg development and suppressed second-stage juvenile (J2) motility, with the magnitude of inhibition varying among isolates, concentrations, and incubation times. Changes in motility at some intermediate concentrations indicated that inhibition was not uniformly sustained over time. In cucumber assays, several isolates reduced root galling, with stronger suppression generally observed following J2 than egg inoculation. Selected isolates were subsequently evaluated under greenhouse conditions on tomato, where 1308, 1910, and 2084 produced reductions in root galling at selected early and mid-season assessments. Although differences in galling diminished under prolonged nematode pressure, selected isolates produced harvest-specific increases in individual fruit weight, whereas cumulative fruit number and fruit weight did not differ significantly among treatments. These results indicate that effective C. rosea isolates can contribute to integrated nematode management by reducing early nematode infection and potentially supporting plant performance, even when long-term nematode suppression is limited. Our findings emphasize the importance of multi-stage screening and targeted isolate selection to identify fungal antagonists with activity across different experimental conditions.<\/jats:p>","DOI":"10.3390\/plants15182809","type":"journal-article","created":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T09:34:01Z","timestamp":1789378441000},"page":"2809","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Targeting Meloidogyne incognita with Clonostachys rosea: Strain-Dependent Biocontrol Performance and Yield Effects Under Greenhouse Conditions"],"prefix":"10.3390","volume":"15","author":[{"given":"Tobias","family":"Stucky","sequence":"first","affiliation":[{"name":"Entomology and Nematology, Plant Protection, Agroscope, M\u00fcller-Thurgau-Strasse 29, 8820 W\u00e4denswil, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"formal-analysis","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"},{"role":"visualization","vocabulary":"credit"}]},{"given":"Lara","family":"de Gianni","sequence":"additional","affiliation":[{"name":"Entomology and Nematology, Plant Protection, Agroscope, M\u00fcller-Thurgau-Strasse 29, 8820 W\u00e4denswil, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"},{"role":"data-curation","vocabulary":"credit"}]},{"given":"Jakob","family":"Egger","sequence":"additional","affiliation":[{"name":"Entomology and Nematology, Plant Protection, Agroscope, M\u00fcller-Thurgau-Strasse 29, 8820 W\u00e4denswil, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"investigation","vocabulary":"credit"}]},{"given":"J\u00fcrgen","family":"Kraus","sequence":"additional","affiliation":[{"name":"Vegetable-Production Extension, Plants and Plant Products, Agroscope, M\u00fcller-Thurgau-Strasse 29, 8820 W\u00e4denswil, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"methodology","vocabulary":"credit"},{"role":"investigation","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9945-8059","authenticated-orcid":false,"given":"Paul","family":"Dahlin","sequence":"additional","affiliation":[{"name":"Entomology and Nematology, Plant Protection, Agroscope, M\u00fcller-Thurgau-Strasse 29, 8820 W\u00e4denswil, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"},{"role":"conceptualization","vocabulary":"credit"},{"role":"methodology","vocabulary":"credit"},{"role":"validation","vocabulary":"credit"},{"role":"resources","vocabulary":"credit"},{"role":"writing-review-editing","vocabulary":"credit"},{"role":"supervision","vocabulary":"credit"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8533-1022","authenticated-orcid":false,"given":"Andrea C.","family":"Ruthes","sequence":"additional","affiliation":[{"name":"Entomology and Nematology, Plant Protection, Agroscope, M\u00fcller-Thurgau-Strasse 29, 8820 W\u00e4denswil, Switzerland"},{"name":"Mycology, Plant Protection, Agroscope, Route de Duillier 60, 1260 Nyon, Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2026,9,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1186\/s41938-018-0080-x","article-title":"Fungal and bacterial nematicides in integrated nematode management strategies","volume":"28","author":"Askary","year":"2018","journal-title":"Egypt. J. Biol. Pest Control"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"486","DOI":"10.1111\/jam.14625","article-title":"Biology and applications of Clonostachys rosea","volume":"129","author":"Sun","year":"2020","journal-title":"J. Appl. Microbiol."},{"key":"ref_3","unstructured":"de Bruijn, F.M. (2022). Clonostachys rosea to control plant diseases. Microbial Bioprotectants for Plant Disease Management, Burleigh Dodds Science Publishing. Burleigh Dodds Series in Agricultural Science."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Ayaz, M., Zhao, J.T., Zhao, W., Chi, Y.K., Ali, Q., Ali, F., Khan, A.R., Yu, Q., Yu, J.W., and Wu, W.C. (2024). Biocontrol of plant parasitic nematodes by bacteria and fungi: A multi-omics approach for the exploration of novel nematicides in sustainable agriculture. Front. Microbiol., 15.","DOI":"10.3389\/fmicb.2024.1433716"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1146\/annurev-phyto-021622-113058","article-title":"Integrated nematode management in a world in transition: Constraints, policy, processes, and technologies for the future","volume":"61","author":"Sikora","year":"2023","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Ansari, R., Rizvi, R., and Mahmood, I. (2020). Plant-parasitic nematodes and their biocontrol agents: Current status and future vistas. Management of Phytonematodes: Recent Advances and Future Challenges, Springer.","DOI":"10.1007\/978-981-15-4087-5"},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Forghani, F., and Hajihassani, A. (2020). Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Front. Plant Sci., 11.","DOI":"10.3389\/fpls.2020.01125"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"104874","DOI":"10.1016\/j.cropro.2019.104874","article-title":"Integrated control of Meloidogyne incognita in tomatoes using fluopyram and Purpureocillium lilacinum strain 251","volume":"124","author":"Dahlin","year":"2019","journal-title":"Crop Prot."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Sikora, R.A., Coyne, D., Hallmann, J., and Timper, P. (2018). Management practices: An overview of integrated nematode management technologie. Plant-Parasitic Nematodes in Subtropical and Tropical Agriculture, CAB International. [3rd ed.].","DOI":"10.1079\/9781786391247.0000"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Eisenback, J.D. (2020). Meloidogyne incognita (root-knot nematode). Invasive Species Compendium, CABI.","DOI":"10.1079\/cabicompendium.33245"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1510","DOI":"10.1021\/np0502241","article-title":"Nematicidal epipolysulfanyldioxopiperazines from Gliocladium roseum","volume":"68","author":"Dong","year":"2005","journal-title":"J. Nat. Prod."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3243","DOI":"10.1111\/j.1462-2920.2010.02296.x","article-title":"Regulation of subtilisin-like protease prC expression by nematode cuticle in the nematophagous fungus Clonostachys rosea","volume":"12","author":"Zou","year":"2010","journal-title":"Environ. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1094\/PHYTO-03-17-0091-R","article-title":"Evaluation of Clonostachys rosea for control of plant-parasitic nematodes in soil and in roots of carrot and wheat","volume":"108","author":"Iqbal","year":"2018","journal-title":"Phytopathology\u00ae"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"lxae111","DOI":"10.1093\/jambio\/lxae111","article-title":"Control of the plant-parasitic nematode Meloidogyne incognita in soil and on tomato roots by Clonostachys rosea","volume":"135","author":"Stucky","year":"2024","journal-title":"J. Appl. Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Al-Ani, L.K.T., de Freitas Soares, F.E., Sharma, A., de Los Santos-Villalobos, S., Valdivia-Padilla, A.V., and Aguilar-Marcelino, L. (2022). Strategy of nematophagous fungi in determining the activity of plant parasitic nematodes and their prospective role in sustainable agriculture. Front. Fungal Biol., 3.","DOI":"10.3389\/ffunb.2022.863198"},{"key":"ref_16","first-page":"100025","article-title":"Biological control 2.0: Use of nematophagous fungi enzymes for nematode control","volume":"4","author":"Ferreira","year":"2023","journal-title":"J. Nat. Pestic. Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1139\/W08-156","article-title":"Chitinase and \u03b2-1,3-glucanase enzyme production by the mycoparasite Clonostachys rosea f. catenulata against fungal plant pathogens","volume":"55","author":"Chatterton","year":"2009","journal-title":"Can. J. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Iqbal, M., Dubey, M., Gudmundsson, M., Viketoft, M., Funk Jensen, D., and Karlsson, M. (2018). Comparative evolutionary histories of fungal proteases reveal gene gains in the mycoparasitic and nematode-parasitic fungus Clonostachys rosea. BMC Evol. Biol., 18.","DOI":"10.1186\/s12862-018-1291-1"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"15009","DOI":"10.1038\/s41598-018-33391-1","article-title":"Functional analysis of polyketide synthase genes in the biocontrol fungus Clonostachys rosea","volume":"8","author":"Fatema","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"102279","DOI":"10.1016\/j.pmpp.2024.102279","article-title":"Unravelling the potent nematotoxic compounds from Clonostachys rosea effective against root knot nematode, Meloidogyne incognita-an in-vitro and in-silico approach","volume":"131","author":"Shravani","year":"2024","journal-title":"Physiol. Mol. Plant Pathol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2264","DOI":"10.1111\/eva.13001","article-title":"Natural variation of root lesion nematode antagonism in the biocontrol fungus Clonostachys rosea and identification of biocontrol factors through genome-wide association mapping","volume":"13","author":"Iqbal","year":"2020","journal-title":"Evol. Appl."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Mascarin, G.M., da Silva, A.V.R., da Silva, T.P., Kobori, N.N., Morandi, M.A.B., and Bettiol, W. (2022). Clonostachys rosea: Production by Submerged Culture and Bioactivity Against Sclerotinia sclerotiorum and Bemisia tabaci. Front. Microbiol., 13.","DOI":"10.3389\/fmicb.2022.851000"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1111\/j.1574-6968.2008.01228.x","article-title":"Real-time RT-PCR expression analysis of chitinase and endoglucanase genes in the three-way interaction between the biocontrol strain Clonostachys rosea IK726, Botrytis cinerea and strawberry","volume":"285","author":"Mamarabadi","year":"2008","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Duke, S.O., Kudsk, P., and Solomon, K. (2017). Perspectives on Hormesis and Implications for Pesticides. Pesticide Dose: Effects on the Environment and Target and Non-Target Organisms, American Chemical Society.","DOI":"10.1021\/bk-2017-1249"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1146\/annurev.pharmtox.43.100901.140223","article-title":"Hormesis: The dose-response revolution","volume":"43","author":"Calabrese","year":"2003","journal-title":"Annu. Rev. Pharmacol. Toxicol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1007\/3-540-33526-9_11","article-title":"Nematophagous Fungi as Root Endophytes","volume":"Volume 9","author":"Schulz","year":"2006","journal-title":"Microbial Root Endophytes. Soil Biology"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1007\/978-94-017-8730-7_5","article-title":"Biological Control of Plant-Parasitic Nematodes by Nematophagous Fungi","volume":"Volume 23","author":"Zhang","year":"2014","journal-title":"Nematode-Trapping Fungi. Fungal Diversity Research Series"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1163\/156854104323072883","article-title":"Activity of fungal culture filtrates against soybean cyst nematode and root-knot nematode egg hatch and juvenile motility","volume":"6","author":"Meyer","year":"2004","journal-title":"Nematology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"20250018","DOI":"10.2478\/jofnem-2025-0018","article-title":"Nematocidal activity of fungal filtrates on eggs and juveniles of five species of sedentary endoparasitic nematodes","volume":"57","author":"Jumbam","year":"2025","journal-title":"J. Nematol."},{"key":"ref_30","first-page":"398","article-title":"In vitro Studies on the Nematophagous fungus Clonostachys rosea (TNAU CR 01) against Meloidogyne incognita, a Root-knot Nematode","volume":"14","author":"Shaliha","year":"2022","journal-title":"Biol. Forum"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1186\/s42483-024-00257-6","article-title":"Application of fungi as biological control strategies for nematode management in horticultural crops","volume":"6","author":"Rahman","year":"2024","journal-title":"Phytopathol. Res."},{"key":"ref_32","first-page":"1","article-title":"Pochonia chlamydosporia: Advances and challenges to improve its performance as a biological control agent of sedentary endo-parasitic nematodes","volume":"45","author":"Esteves","year":"2013","journal-title":"J. Nematol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"77","DOI":"10.21307\/jofnem-2017-047","article-title":"Evaluation of Pochonia chlamydosporia and Purpureocillium lilacinum for suppression of Meloidogyne enterolobii on tomato and banana","volume":"49","author":"Silva","year":"2017","journal-title":"J. Nematol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e253451","DOI":"10.1590\/1519-6984.253451","article-title":"Efficacy of Purpureocillium lilacinum AUMC 10149 as biocontrol agent against root-knot nematode Meloidogyne incognita infecting tomato plant","volume":"84","author":"Isaac","year":"2021","journal-title":"Braz. J. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Khan, M., and Tanaka, K. (2023). Purpureocillium lilacinum for plant growth promotion and biocontrol against root-knot nematodes infecting eggplant. PLoS ONE, 18.","DOI":"10.1371\/journal.pone.0283550"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Han, Z., Ghanizadeh, H., Zhang, H., Li, X., Li, T., Wang, Q., Liu, J., and Wang, A. (2022). Clonostachys rosea promotes root growth in tomato by secreting auxin produced through the tryptamine pathway. J. Fungi, 8.","DOI":"10.3390\/jof8111166"},{"key":"ref_37","unstructured":"Alvarez Nordstr\u00f6m, S. (2014). Endophytic Growth of Clonostachys rosea in Tomato and Arabidopsis thaliana. [Master\u2019s Thesis, Swedish University of Agricultural Sciences (SLU)]."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"206","DOI":"10.1017\/S095375620300724X","article-title":"Approaches for monitoring the release of Pochonia chlamydosporia var. catenulata, a biocontrol agent of root-knot nematodes","volume":"107","author":"Atkins","year":"2003","journal-title":"Mycol. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.biocontrol.2005.12.006","article-title":"Biological control of the root-knot nematode Meloidogyne incognita by Paecilomyces lilacinus strain 251","volume":"38","author":"Kiewnick","year":"2006","journal-title":"Biol. Control"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"2288723","DOI":"10.1080\/16583655.2023.2288723","article-title":"Nematicidal action of Clonostachys rosea against Meloidogyne incognita: In-vitro and in-silico analyses","volume":"18","author":"Nagaraj","year":"2024","journal-title":"J. Taibah Univ. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"415","DOI":"10.1007\/s41348-018-0165-5","article-title":"Virulence of Meloidogyne incognita populations and Meloidogyne enterolobii on resistant cucurbitaceous and solanaceous plant genotypes","volume":"125","author":"Hallmann","year":"2018","journal-title":"J. Plant Dis. Prot."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1163\/15685411-00002751","article-title":"Identification of the tropical root-knot nematode species Meloidogyne incognita, M. javanica and M. arenaria using a multiplex PCR assay","volume":"15","author":"Kiewnick","year":"2013","journal-title":"Nematology"},{"key":"ref_43","unstructured":"(2025, December 05). Mycoscope. The Database from Agroscope\u2019s Mycoth\u00e8que. Available online: https:\/\/www.mycoscope.ch\/."},{"key":"ref_44","first-page":"141","article-title":"X Rating scheme for field evaluation of root-knot nematode infestations","volume":"24","author":"Zeck","year":"1971","journal-title":"Pflanzenschutz Nachr."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"103025","DOI":"10.1016\/j.eti.2023.103025","article-title":"Biogas digestate as potential source for nematicides","volume":"29","author":"Oldani","year":"2023","journal-title":"Environ. Technol. Innov."},{"key":"ref_46","unstructured":"R Core Team (2024). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing."}],"container-title":["Plants"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/18\/2809\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T10:05:17Z","timestamp":1789380317000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2223-7747\/15\/18\/2809"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,13]]},"references-count":46,"journal-issue":{"issue":"18","published-online":{"date-parts":[[2026,9]]}},"alternative-id":["plants15182809"],"URL":"https:\/\/doi.org\/10.3390\/plants15182809","relation":{},"ISSN":["2223-7747"],"issn-type":[{"value":"2223-7747","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,13]]}}}