{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T06:55:53Z","timestamp":1790664953144,"version":"4.1.0"},"reference-count":54,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T00:00:00Z","timestamp":1790553600000},"content-version":"vor","delay-in-days":27,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"},{"start":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T00:00:00Z","timestamp":1788220800000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100007129","name":"Natural Science Foundation of Shandong Province","doi-asserted-by":"publisher","award":["ZR2025QC149"],"award-info":[{"award-number":["ZR2025QC149"]}],"id":[{"id":"10.13039\/501100007129","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007129","name":"Natural Science Foundation of Shandong Province","doi-asserted-by":"publisher","award":["ZR2024MC177"],"award-info":[{"award-number":["ZR2024MC177"]}],"id":[{"id":"10.13039\/501100007129","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Physiologia Plantarum"],"published-print":{"date-parts":[[2026,9]]},"abstract":"ABSTRACT<\/jats:title>\n \n Root\u2010knot nematode causes severe yield losses in cucumber and other cucurbits. The wild relative\n \n Cucumis metuliferus<\/jats:italic>\n <\/jats:styled-content>\n exhibits strong resistance, but the metabolic basis of this resistance and the potential of resistance\u2010associated metabolites to protect susceptible crops remains poorly understood. Here, we compared host status, phenolic content, and untargeted metabolomes of roots and rhizosphere soils of\n \n C. metuliferus<\/jats:italic>\n <\/jats:styled-content>\n and\n \n C. sativus<\/jats:italic>\n <\/jats:styled-content>\n upon\n Meloidogyne incognita<\/jats:italic>\n infection.\n \n C. metuliferus<\/jats:italic>\n <\/jats:styled-content>\n showed delayed nematode development, fewer galls, and a lower reproduction factor compared with\n \n C. sativus<\/jats:italic>\n <\/jats:styled-content>\n , accompanied by higher constitutive phenolic levels in mock\u2010inoculated plants and phenolic levels at 7, 14, 21, and 28\u2009days after inoculation. Untargeted metabolomics revealed that\n \n C. metuliferus<\/jats:italic>\n <\/jats:styled-content>\n underwent more extensive metabolic reprogramming than\n \n C. sativus<\/jats:italic>\n <\/jats:styled-content>\n , with 72 root\u2010specific and 45 rhizosphere\u2010specific differential metabolites enriched mainly in linolenic acid metabolism and dominated by lipids and organic acids. Six\n \n C. metuliferus<\/jats:italic>\n <\/jats:styled-content>\n \u2010specific up\u2010regulated metabolites (arginine, phenylacetic acid, proline, hydroxyproline, malic acid, maleic acid) were selected for functional validation. When exogenously applied to\n \n C. sativus<\/jats:italic>\n <\/jats:styled-content>\n seedlings under nematode stress, these metabolites were associated with enhanced shoot growth and biomass accumulation. Among them, arginine, hydroxyproline, and maleic acid were consistently associated with reduced root gall formation. Our findings demonstrate that\n \n C. metuliferus<\/jats:italic>\n <\/jats:styled-content>\n mounts a resistance phenotype through extensive root and rhizosphere metabolic reprogramming, and that specific up\u2010regulated metabolites from this resistant species can both promote cucumber growth and reduce\n \n M. incognita<\/jats:italic>\n <\/jats:styled-content>\n infection. These metabolites represent promising candidates but require further field validation and formulation studies before being developed into sustainable nematode management strategies.\n <\/jats:p>","DOI":"10.1111\/ppl.71135","type":"journal-article","created":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T06:00:25Z","timestamp":1790661625000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Metabolic Reprogramming in\n Cucumis metuliferus<\/i>\n Roots and Rhizosphere Identifies Candidate Metabolites That Reduce\n Meloidogyne incognita<\/i>\n Infection"],"prefix":"10.1111","volume":"178","author":[{"given":"Xin","family":"Guo","sequence":"first","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuai","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jisong","family":"Qu","sequence":"additional","affiliation":[{"name":"Ningxia Academy of Agriculture and Forestry Science Yinchuan China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hao","family":"Chen","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zongqing","family":"Li","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinzhe","family":"Li","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shunyi","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuhong","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiqun","family":"Chen","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guifang","family":"Feng","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5143-9812","authenticated-orcid":false,"given":"Jingjing","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4040-2461","authenticated-orcid":false,"given":"Xu","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Life Science, Linyi University Linyi China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,9,28]]},"reference":[{"issue":"3","key":"e_1_2_12_2_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.heliyon.2024.e25325","article-title":"Revolutionizing Nematode Management to Achieve Global Food Security Goals\u2010An Overview","volume":"10","author":"Afzal A.","year":"2024","journal-title":"Heliyon"},{"key":"e_1_2_12_3_1","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1038\/nprot.2007.102","article-title":"Estimation of Total Phenolic Content and Other Oxidation Substrates in Plant Tissues Using Folin\u2010Ciocalteu Reagent","volume":"2","author":"Ainsworth E. 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P.","year":"2006","journal-title":"Annual Review of Plant Biology"},{"key":"e_1_2_12_7_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2013.00082","article-title":"Metabolomics of Cereals Under Biotic Stress: Current Knowledge and Techniques","volume":"4","author":"Balmer D.","year":"2013","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_12_8_1","doi-asserted-by":"crossref","first-page":"1789","DOI":"10.1093\/jxb\/ert415","article-title":"Vascularization and Nutrient Delivery at Root\u2010Knot Nematode Feeding Sites in Host Roots","volume":"65","author":"Bartlem D. G.","year":"2014","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_12_9_1","first-page":"142","article-title":"An Improved Technique for Clearing and Staining Plant Tissues for Detection of Nematodes","volume":"15","author":"Bybd D.","year":"1983","journal-title":"Journal of Nematology"},{"key":"e_1_2_12_10_1","doi-asserted-by":"crossref","DOI":"10.3390\/horticulturae11080892","article-title":"Meloidogyne incognita Significantly Alters the Cucumber Root Metabolome and Enriches Differential Accumulated Metabolites Regulating Nematode Chemotaxis and Infection","volume":"11","author":"Chen N.","year":"2025","journal-title":"Horticulturae"},{"key":"e_1_2_12_11_1","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1146\/annurev.phyto.40.032602.130045","article-title":"Phytochemical Based Strategies for Nematode Control","volume":"40","author":"Chitwood D. 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R. R.","year":"2010","journal-title":"Applied Soil Ecology"},{"key":"e_1_2_12_21_1","first-page":"1025","article-title":"A Comparison of Methods of Collecting Inocula of Meloidogyne spp., Including a New Technique","volume":"57","author":"Hussey R. S.","year":"1973","journal-title":"Plant Disease Reporter"},{"key":"e_1_2_12_22_1","doi-asserted-by":"crossref","first-page":"946","DOI":"10.1111\/mpp.12057","article-title":"Top 10 Plant\u2010Parasitic Nematodes in Molecular Plant Pathology","volume":"14","author":"Jones J. T.","year":"2013","journal-title":"Molecular Plant Pathology"},{"key":"e_1_2_12_23_1","doi-asserted-by":"crossref","first-page":"303","DOI":"10.21307\/jofnem-2018-030","article-title":"NMR Analysis Reveals a Wealth of Metabolites in Root\u2010Knot Nematode Resistant Roots of Citrullus amarus Watermelon Plants","volume":"50","author":"Kantor M.","year":"2018","journal-title":"Journal of Nematology"},{"issue":"22","key":"e_1_2_12_24_1","doi-asserted-by":"crossref","first-page":"6658","DOI":"10.1021\/acs.jafc.2c01748","article-title":"Chemo\u2010Ecological Insights Into the Use of the Non\u2010Host Plant Vegetable Black\u2010Jack to Protect Two Susceptible Solanaceous Crops From Root\u2010Knot Nematode Parasitism","volume":"70","author":"Kihika\u2010Opanda R.","year":"2022","journal-title":"Journal of Agricultural and Food Chemistry"},{"key":"e_1_2_12_25_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2021.675429","article-title":"Transcriptomic and Histological Analysis of the Response of Susceptible and Resistant Cucumber to Meloidogyne incognita Infection Revealing Complex Resistance via Multiple Signaling Pathways","volume":"12","author":"Li X.","year":"2021","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_12_26_1","doi-asserted-by":"crossref","DOI":"10.3390\/antiox14060679","article-title":"Elongated HYPOCOTYL5 Regulates Resistance to Root\u2010Knot Nematode by Modulating Antioxidant System and Jasmonic Acid in \n Cucumis sativus","volume":"14","author":"Ma F.","year":"2025","journal-title":"Antioxidants"},{"key":"e_1_2_12_27_1","doi-asserted-by":"crossref","first-page":"788","DOI":"10.1111\/tpj.13543","article-title":"Small Molecules Below\u2010Ground: The Role of Specialized Metabolites in the Rhizosphere","volume":"90","author":"Massalha H.","year":"2017","journal-title":"Plant Journal"},{"issue":"3","key":"e_1_2_12_28_1","doi-asserted-by":"crossref","first-page":"589","DOI":"10.33804\/pp.010.03.5426","article-title":"Therapeutic Potential of Neem (\n Azadirachta indica\n ) and Hemp (\n Cannabis sativa\n ) Soil Amendments for the Sustainable Management of Root\u2010Knot Nematodes (Meloidogyne incognita) in Tomato","volume":"10","author":"Matee\u2010Ur\u2010Rehman H.","year":"2026","journal-title":"Plant Protection"},{"issue":"3","key":"e_1_2_12_29_1","doi-asserted-by":"crossref","first-page":"666","DOI":"10.1105\/tpc.19.00157","article-title":"Metabolite Regulatory Interactions Control Plant Respiratory Metabolism via Target of Rapamycin (TOR) Kinase Activation","volume":"32","author":"O'Leary B. M.","year":"2020","journal-title":"Plant Cell"},{"issue":"360","key":"e_1_2_12_30_1","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1093\/jexbot\/52.360.1383","article-title":"Sink Regulation of Photosynthesis","volume":"52","author":"Paul M. J.","year":"2001","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_12_31_1","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1111\/tpj.13639","article-title":"Metabolite Profiling of Non\u2010Sterile Rhizosphere Soil","volume":"92","author":"P\u00e9triacq P.","year":"2017","journal-title":"Plant Journal"},{"key":"e_1_2_12_32_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.jplph.2024.154186","article-title":"TOR in Plants: Multidimensional Regulators of Plant Growth and Signaling Pathways","volume":"294","author":"Rabeh K.","year":"2024","journal-title":"Journal of Plant Physiology"},{"key":"e_1_2_12_33_1","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1146\/annurev-phyto-021621-120943","article-title":"Rooting Out the Mechanisms of Root\u2010Knot Nematode\u2013Plant Interactions","volume":"60","author":"Rutter W. B.","year":"2022","journal-title":"Annual Review of Phytopathology"},{"key":"e_1_2_12_34_1","first-page":"89","article-title":"Reactions of Citrullus amarus and \n C. metuliferus\n to Meloidogyne chitwoodi, Meloidogyne enterolobii and Meloidogyne luci","volume":"168","author":"Santos D.","year":"2024","journal-title":"European Journal of Plant Pathology"},{"key":"e_1_2_12_35_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2019.01165","article-title":"Plant immune responses to parasitic nematodes","volume":"10","author":"Sato K.","year":"2019","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_12_36_1","doi-asserted-by":"crossref","DOI":"10.1134\/S1021443725604379","article-title":"Foliar Application of Arginine, Proline, Dopamine, and Melatonin Enhances Growth, Yield and Fruit Biochemical Traits of Greenhouse Cucumber (\n Cucumis sativus\n L.) Under Sub\u2010Optimal Temperature Conditions","volume":"72","author":"Sayadi R.","year":"2025","journal-title":"Russian Journal of Plant Physiology"},{"key":"e_1_2_12_37_1","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1186\/s12870-021-02998-4","article-title":"Combining Targeted Metabolite Analyses and Transcriptomics to Reveal the Specific Chemical Composition and Associated Genes in the Incompatible Soybean Variety PI437654 Infected With Soybean Cyst Nematode HG1.2.3.5.7","volume":"21","author":"Shi X.","year":"2021","journal-title":"BMC Plant Biology"},{"key":"e_1_2_12_38_1","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1146\/annurev-phyto-020620-102355","article-title":"Recognition and Response in Plant\u2013Nematode Interactions","volume":"60","author":"Siddique S.","year":"2022","journal-title":"Annual Review of Phytopathology"},{"key":"e_1_2_12_39_1","doi-asserted-by":"crossref","DOI":"10.3389\/fpls.2019.01792","article-title":"Impacts of Root Metabolites on Soil Nematodes","volume":"10","author":"Sikder M. M.","year":"2020","journal-title":"Frontiers in Plant Science"},{"key":"e_1_2_12_40_1","article-title":"Unraveling the Enigma of Root\u2010Knot Nematodes: From Origins to Advanced Management Strategies in Agriculture","volume":"260","author":"Singh R.","year":"2024","journal-title":"Planta"},{"issue":"370","key":"e_1_2_12_41_1","doi-asserted-by":"crossref","first-page":"959","DOI":"10.1093\/jexbot\/53.370.959","article-title":"Steps Towards an Integrated View of Nitrogen Metabolism","volume":"53","author":"Stitt M.","year":"2002","journal-title":"Journal of Experimental Botany"},{"key":"e_1_2_12_42_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.pmpp.2024.102354","article-title":"Molecular Mechanisms and Phytomolecules as Source of Resistance for Sustainable Management of Root Knot Nematode Infestations in Horticultural Crops: A Review","volume":"133","author":"Swaruparani N.","year":"2024","journal-title":"Physiological and Molecular Plant Pathology"},{"key":"e_1_2_12_43_1","doi-asserted-by":"crossref","DOI":"10.1007\/s00425-024-04464-5","article-title":"Unraveling the Enigma of Root\u2010Knot Nematodes: From Origins to Advanced Management Strategies in Agriculture","volume":"260","author":"Vashisth S.","year":"2024","journal-title":"Planta"},{"key":"e_1_2_12_44_1","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.cbpa.2017.01.001","article-title":"How Close Are We to Complete Annotation of Metabolomes?","volume":"36","author":"Viant M. R.","year":"2017","journal-title":"Current Opinion in Chemical Biology"},{"key":"e_1_2_12_45_1","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/s00299-019-02447-5","article-title":"Root Exudates: From Plant to Rhizosphere and Beyond","volume":"39","author":"Vives\u2010Peris V.","year":"2020","journal-title":"Plant Cell Reports"},{"key":"e_1_2_12_46_1","doi-asserted-by":"crossref","DOI":"10.1186\/s12870-026-08301-7","article-title":"Integrated Omics Reveal Phenylpropanoid Biosynthesis as a Key Defense Pathway Against Meloidogyne incognita in \n Cucumis metuliferus","volume":"26","author":"Wang Y.","year":"2026","journal-title":"BMC Plant Biology"},{"key":"e_1_2_12_47_1","doi-asserted-by":"crossref","DOI":"10.1093\/hr\/uhac051","article-title":"Negative Regulation of Root\u2010Knot Nematode Parasitic Behavior by Root\u2010Derived Volatiles of Wild Relatives of \n Cucumis metuliferus\n CM3","volume":"9","author":"Xie X.","year":"2022","journal-title":"Horticulture Research"},{"key":"e_1_2_12_48_1","article-title":"Defense Responses in Prickly Pear (\n C. metuliferus\n ) to Meloidogyne incognita: Insights From Transcriptomics and Metabolomics Analysis","volume":"23","author":"Xie X.","year":"2022","journal-title":"International Journal of Molecular Sciences"},{"key":"e_1_2_12_49_1","doi-asserted-by":"crossref","DOI":"10.1007\/s00425-025-04649-6","article-title":"Comparative Transcriptomics of Susceptible and Resistant \n Cucumis metuliferus\n Upon Meloidogyne incognita Infection","volume":"261","author":"Xie X.","year":"2025","journal-title":"Planta"},{"issue":"4","key":"e_1_2_12_50_1","first-page":"5927","article-title":"Integrated Management of Meloidogyne spp. in Cucumber Using Plant Extracts","volume":"10","author":"Yao A. S.","year":"2026","journal-title":"Plant Protection"},{"key":"e_1_2_12_51_1","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.jplph.2017.02.002","article-title":"Histopathology Combined With Transcriptome Analyses Reveals the Mechanism of Resistance to Meloidogyne Incognita in \n Cucumis metuliferus","volume":"212","author":"Ye D. Y.","year":"2017","journal-title":"Journal of Plant Physiology"},{"key":"e_1_2_12_52_1","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1146\/annurev-phyto-073009-114425","article-title":"Managing Nematodes Without Methyl Bromide","volume":"48","author":"Zasada I. A.","year":"2010","journal-title":"Annual Review of Phytopathology"},{"key":"e_1_2_12_53_1","doi-asserted-by":"crossref","DOI":"10.1111\/mpp.13396","article-title":"Metabolic Variations in Root Tissues and Rhizosphere Soils of Weak Host Plants Potently Lead to Distinct Host Status and Chemotaxis Regulation of Meloidogyne incognita in Intercropping","volume":"25","author":"Zhang X.","year":"2024","journal-title":"Molecular Plant Pathology"},{"key":"e_1_2_12_54_1","doi-asserted-by":"crossref","first-page":"1651","DOI":"10.1111\/nph.18837","article-title":"Tomato Defence Against Meloidogyne incognita by Jasmonic Acid\u2010Mediated Fine\u2010Tuning of Kaempferol Homeostasis","volume":"238","author":"Zhao W.","year":"2023","journal-title":"New Phytologist"},{"key":"e_1_2_12_55_1","first-page":"1023","article-title":"Plant Metabolic Reprogramming in Response to Root\u2010Knot Nematode Infection: A Comprehensive Review","volume":"76","author":"Zhou Q.","year":"2025","journal-title":"Journal of Experimental Botany"}],"container-title":["Physiologia Plantarum"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/ppl.71135","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/ppl.71135","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/ppl.71135","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T06:00:34Z","timestamp":1790661634000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/ppl.71135"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9]]},"references-count":54,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2026,9]]}},"alternative-id":["10.1111\/ppl.71135"],"URL":"https:\/\/doi.org\/10.1111\/ppl.71135","archive":["Portico"],"relation":{},"ISSN":["0031-9317","1399-3054"],"issn-type":[{"value":"0031-9317","type":"print"},{"value":"1399-3054","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9]]},"assertion":[{"value":"2026-04-19","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-15","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-28","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e71135"}}