{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T03:03:44Z","timestamp":1788404624695,"version":"build-2803163510"},"reference-count":45,"publisher":"MDPI AG","issue":"20","license":[{"start":{"date-parts":[[2023,10,21]],"date-time":"2023-10-21T00:00:00Z","timestamp":1697846400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Research Centre for Agricultural Technologies (Agritech)"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Commercial formulations of beneficial microbes have been used to enrich the rhizosphere microbiome of tomato plants grown in pots located in a glasshouse. These plants have been subjected to attacks by soil-borne parasites, such as root-knot nematodes (RKNs), and herbivores, such as the miner insect Tuta absoluta. The development of both parasites and the symptoms of their parasitism were restricted in these plants with respect to plants left untreated. A mixture, named in the text as Myco, containing plant growth-promoting rhizobacteria (PGPR), opportunistic biocontrol fungi (BCF), and arbuscular mycorrhizal fungi (AMF) was more effective in limiting pest damage than a formulation containing the sole AMF (Ozor). Therefore, Myco-treated plants inoculated with RKNs were taken as a model for further studies. The PGPR contained in Myco were not able to reduce nematode infection; rather, they worsened symptoms in plants compared with those observed in untreated plants. Therefore, it was argued that both BCF and AMF were the microorganisms that colonized roots and stimulated the plant immune system against RKNs. Beneficial fungi colonized the roots by lowering the activities of the defense supporting enzymes endochitinases and \u03b2-1,3-glucanase. However, as early as three days after nematode inoculation, these enzyme activities and the expression of the encoding pathogenesis-related genes (PR-2, PR-3) were found to be enhanced in roots with respect to non-inoculated plants, thus indicating that plants had been primed against RKNs. The addition of paclobutrazol, which reduces salicylic acid (SA) levels in cells, and diphenyliodonium chloride, which inhibits superoxide generation, completely abolished the repressive effect of Myco on nematode infection. Inhibitors of copper enzymes and the alternative cyanide-resistant respiration did not significantly alter resistance induction by Myco. When Myco-treated plants were subjected to moderate water stress and inoculated with nematodes, they retained numbers of developed individuals in the roots similar to those present in regularly watered plants, in contrast to what occurred in roots of untreated stressed plants that hosted very few individuals because of poor nutrient availability.<\/jats:p>","DOI":"10.3390\/ijms242015416","type":"journal-article","created":{"date-parts":[[2023,10,21]],"date-time":"2023-10-21T12:59:01Z","timestamp":1697893141000},"page":"15416","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":10,"title":["Resistance to Plant Parasites in Tomato Is Induced by Soil Enrichment with Specific Bacterial and Fungal Rhizosphere Microbiome"],"prefix":"10.3390","volume":"24","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2472-1289","authenticated-orcid":false,"given":"Sergio","family":"Molinari","sequence":"first","affiliation":[{"name":"Institute for Sustainable Plant Protection, IPSP-Bari Unit, Department of Biology, Agricultural and Food Sciences, DISBA, National Council of Research, CNR, 70126 Bari, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2636-3419","authenticated-orcid":false,"given":"Paola","family":"Leonetti","sequence":"additional","affiliation":[{"name":"Institute for Sustainable Plant Protection, IPSP-Bari Unit, Department of Biology, Agricultural and Food Sciences, DISBA, National Council of Research, CNR, 70126 Bari, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,10,21]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Liu, H., Carvalhais, L.C., Crawford, M., Singh, E., Dennis, P.G., Pieterse, C.M., and Schenk, P.M. (2017). Inner plant values: Diversity, colonization and benefits from endophytic bacteria. Front. Microbiol., 8.","DOI":"10.3389\/fmicb.2017.02552"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.proenv.2015.07.270","article-title":"Nematodes: A threat to sustainability of agriculture","volume":"29","author":"Singh","year":"2015","journal-title":"Procedia Environ. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1002\/bies.20717","article-title":"Parasitism genes and host range disparities in biotrophic nematodes: The conundrum of polyphagy versus specialisation","volume":"30","author":"Blok","year":"2008","journal-title":"BioEssays"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1146\/annurev-phyto-080516-035623","article-title":"Interplay between innate immunity and the plant microbiota","volume":"55","author":"Hacquard","year":"2017","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Poveda, J., Abril-Urias, P., and Escobar, C. (2020). Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Front. Microbiol., 11.","DOI":"10.3389\/fmicb.2020.00992"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Molinari, S., and Leonetti, P. (2019). Bio-control agents activate plant immune response and prime susceptible tomato against root-knot nematodes. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0213230"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1007\/s00299-017-2109-0","article-title":"Induction of SA-signaling pathway and ethylene biosynthesis in Trichoderma harzianum-treated tomato plants after infection of the root-knot nematode Meloidogyne incognita","volume":"36","author":"Leonetti","year":"2017","journal-title":"Plant Cell Rep."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.soilbio.2013.01.013","article-title":"Mycorrhiza-induced resistance against the root\u2013knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato","volume":"60","author":"Vos","year":"2013","journal-title":"Soil Biol. Biochem."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Molinari, S., Akbarimotlagh, M., and Leonetti, P. (2022). Tomato root colonization by exogenously inoculated arbuscular mycorrhizal fungi induces resistance against root-knot nematodes in a dose-dependent manner. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23168920"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1080\/03235401003633774","article-title":"Interaction between Pseudomonas fluorescens and Meloidogyne javanica on tomato plant as influenced by the different levels of phosphorus","volume":"44","author":"Mahmood","year":"2011","journal-title":"Arch. Phytopathol. Plant Prot."},{"key":"ref_11","first-page":"5","article-title":"Pseudomonas fluorescens induced systemic resistance in tomato against Meloidogyne javanica","volume":"42","author":"Sankari","year":"2012","journal-title":"Indian J. Nematol."},{"key":"ref_12","unstructured":"Lumsden, R.D., and Vaughn, J.L. (1993). Pest Management: Biotechnology-Based Technologies, American Chemistry Society."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Susi\u010d, N., \u017dibrat, U., Sinkovi\u010d, L., Von\u010dina, A., Razinger, J., Knapi\u010d, M., Sedlar, A., \u0160irca, S., and Geri\u010d Stare, B. (2020). From genome to field\u2014Observation of the multimodal nematicidal and plant growth-promoting effects of Bacillus firmus I-1582 on tomatoes using hyperspectral remote sensing. Plants, 9.","DOI":"10.3390\/plants9050592"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1016\/j.tplants.2020.03.014","article-title":"Microbiome-mediated stress resistance in plants","volume":"25","author":"Liu","year":"2020","journal-title":"Trends Plant Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1394","DOI":"10.1016\/j.molp.2020.09.017","article-title":"The soil-borne identity and microbiome-assisted agriculture: Looking back to the future","volume":"13","author":"Bakker","year":"2020","journal-title":"Mol. Plant."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Molinari, S. (2021). Factors determining the variability of performance of bio-control agents against root-knot nematodes in vegetable plants. Agronomy, 11.","DOI":"10.3390\/agronomy11081602"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1291","DOI":"10.1016\/j.sjbs.2019.05.004","article-title":"Bacillus subtilis: A plant-growth promoting rhizobacterium that also impacts biotic stress","volume":"26","author":"Hashem","year":"2019","journal-title":"Saudi J. Biol. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.biocontrol.2013.01.014","article-title":"Rhizospheric biological weapons for growth enhancement and Meloidogyne incognita management in Withania somnifera cv. Poshita","volume":"65","author":"Shilpi","year":"2013","journal-title":"Biol. Control"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1111\/mpp.12085","article-title":"Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes","volume":"15","author":"Molinari","year":"2014","journal-title":"Mol. Plant Pathol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1093\/pcp\/pci231","article-title":"Colonization by the arbuscular mycorrhizal fungus Glomus versiforme induces a defense response against the root-knot nematode Meloidogyne incognita in the grapevine (Vitis amurensis Rupr.), which includes transcriptional activation of the class III chitin","volume":"47","author":"Li","year":"2006","journal-title":"Plant Cell Physiol."},{"key":"ref_21","first-page":"1","article-title":"New developments in understanding the role of salicylic acid in plant defence","volume":"2","author":"Molinari","year":"2007","journal-title":"CABI Rev."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2182","DOI":"10.1016\/S0021-9258(17)33675-X","article-title":"In vivo inhibition of superoxide dismutase in mice by diethyldithiocarbammate","volume":"251","author":"Heikkila","year":"1976","journal-title":"J. Biol. Chem."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1007\/s00425-014-2115-1","article-title":"Endogenous salicylic acid accumulation is required for chilling tolerance in cucumber (Cucumis sativus L.) seedlings","volume":"240","author":"Dong","year":"2014","journal-title":"Planta"},{"key":"ref_24","first-page":"1118","article-title":"The reactive oxygen species are involved in resistance response of wheat to the Russian wheat aphid","volume":"163","author":"Moloi","year":"2006","journal-title":"J. Plant Pathol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1038\/nature21417","article-title":"Root microbiota drive direct integration of phosphate stress and immunity","volume":"543","author":"Castrillo","year":"2017","journal-title":"Nature"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"E4284","DOI":"10.1073\/pnas.1717308115","article-title":"Drought delays development of the sorghum root microbiome and enriches for monoderm bacteria","volume":"115","author":"Xu","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"347","DOI":"10.1146\/annurev-phyto-082712-102340","article-title":"Induced systemic resistance by beneficial microbes","volume":"52","author":"Pieterse","year":"2014","journal-title":"Annu. Rev. Phytopathol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1080\/03235408.2013.816102","article-title":"Biological control of root-knot nematode (Meloidogyne javanica) disease by Pseudomonas fluorescens (Chao)","volume":"47","author":"Norabadi","year":"2014","journal-title":"Arch. Phytopathol. Plant Prot."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1077062","DOI":"10.3389\/fpls.2022.1077062","article-title":"Biocontrol of Meloidogyne spp. in Solanum lycopersicum using a dual combination of Bacillus strains","volume":"13","author":"Amora","year":"2023","journal-title":"Front. Plant Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"012019","DOI":"10.1088\/1755-1315\/757\/1\/012019","article-title":"Biocontrol of Meloidogyne spp. on tomato plants by selected Bacillus spp.","volume":"757","author":"Habazar","year":"2021","journal-title":"IOP Conf. Ser. Earth Environ. Sci."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"947","DOI":"10.1016\/j.pt.2021.05.007","article-title":"Can microorganisms assist the survival and parasitism of plant-parasitic nematodes?","volume":"37","year":"2021","journal-title":"Trends Parasitol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"S12","DOI":"10.1134\/S1062359021150036","article-title":"Commonalities of molecular response in tomato plants against parasitic nematodes","volume":"48","author":"Bozbuga","year":"2021","journal-title":"Biol. Bull. Russ. Acad. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Aita, B.C., Heinz, B.B., Alves, E.A., Mezadri, E.T., Spannemberg, S.S., Romagna, I.S., Karsburg, P.A., Junges, E., Kuhn, R.C., and Mazutti, M.A. (2021). Cell-wall degrading enzymes for the control of Meloidogyne javanica. Biotech. Res. Inn. J., 4.","DOI":"10.4322\/biori.2019120"},{"key":"ref_34","first-page":"523","article-title":"Activity and differential induction of chitinase isozymes in soybean cultivars resistant or susceptible to root-knot nematodes","volume":"29","author":"Qtu","year":"1997","journal-title":"J. Nematol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2860","DOI":"10.1111\/pce.13632","article-title":"Beneficial microbes going underground of root immunity","volume":"42","author":"Yu","year":"2019","journal-title":"Plant Cell Environ."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1038\/nature22009","article-title":"Plant signalling in symbiosis and immunity","volume":"543","author":"Zipfel","year":"2017","journal-title":"Nature"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1002\/ps.4063","article-title":"Systemic acquired resistance activation in Solanaceous crops as a management strategy against root-knot nematodes","volume":"72","author":"Molinari","year":"2016","journal-title":"Pest Manag. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"123","DOI":"10.3109\/07388551.2012.731684","article-title":"Plant hormones as signals in arbuscular mycorrhizal symbiosis","volume":"34","author":"Miransari","year":"2014","journal-title":"Crit. Rev. Biotechnol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/S1360-1385(02)02366-X","article-title":"Function of the alternative oxidase: Is it still a scavenger?","volume":"7","author":"Moore","year":"2002","journal-title":"Trends Plant Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1007\/s42729-021-00684-w","article-title":"Assessing the potential role of compost, PGPR, and AMF in improving tomato plant growth, yield, fruit quality, and water stress tolerance","volume":"22","author":"Tahiri","year":"2022","journal-title":"J. Soil Sci. Plant Nutr."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"4808","DOI":"10.1093\/jxb\/erad249","article-title":"The role of arbuscular mycorrhizal symbiosis in improving plant water status under drought","volume":"74","author":"Abdalla","year":"2023","journal-title":"J. Exp. Bot."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.mimet.2014.08.023","article-title":"Estimation Method for Serial Dilution Experiments","volume":"107","author":"Davidson","year":"2014","journal-title":"J. Microbiol. Methods"},{"key":"ref_43","unstructured":"Narwal, S.S., Sampietro, D.A., Catal\u00e1n, C.A.N., Vattuone, M.A., and Politycka, B. (2009). Plant Bioassays, Studium Press, LLC."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1016\/S0021-9258(18)65959-9","article-title":"A modified colorimetric method for the estimation of N-acetyl-amino sugars","volume":"217","author":"Reissig","year":"1955","journal-title":"J. Biol. Chem."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S0076-6879(57)03350-9","article-title":"Colorimetric analysis of sugars","volume":"3","author":"Ashwell","year":"1957","journal-title":"Methods Enzymol."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/20\/15416\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:09:31Z","timestamp":1760130571000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/20\/15416"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,21]]},"references-count":45,"journal-issue":{"issue":"20","published-online":{"date-parts":[[2023,10]]}},"alternative-id":["ijms242015416"],"URL":"https:\/\/doi.org\/10.3390\/ijms242015416","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,21]]}}}