Rhizosphere Streptomyces confers dual-mode resistance to root-knot nematodes through nematicidal metabolites and JA-mediated immunity in maize

Abstract

Root-knot nematodes (RKNs) are major soil-borne pests that cause substantial agricultural losses globally. Biological control using microbial antagonists has emerged as a promising, environmentally sustainable, and cost-effective stra-tegy for RKN management. However, the diversity and mechanisms of nematode-antagonistic microbes in the rhizosphereremain insufficiently explored. Here, we systematically profiled the maize rhizosphere microbiome across developmental stages under Meloidogyne incognita infestation and identified microbial taxa with potential nematode-suppressive activity. RKN infection significantly reshaped the rhizosphere with the strongest effects observed during the seedling and jointing stages. Among the taxa enriched in RKN-infected rhizospheres, Streptomyces and Bradyrhizobium emerged as core candidates. Functional assays revealed that Streptomyces, but not Bradyrhizobium, exhibited strong nematode-antagonistic activity, reducing RKN gall formation from 75% to 31% compared to the control treatment. In particular, the effective Streptomyces strain suppressed RKN infection through dual mechanisms: the production of nematicidal metabolites and the activation of the maize jasmonic acid signaling pathway. These findings identify Streptomyces as a central component of the maize rhizosphere microbiome with dual modes of action against RKN, offering new opportunities for microbiome-informed nematode biocontrol and soil health management in sustainable agriculture.

Graphical abstract

Keywords

plant-herbivore interactions / root-knot nematode / rhizosphere bacteria / Streptomyces / jasmonic acid / maize

Highlight

	● RKN infection reshapes maize rhizosphere microbiota at early growth stages.
	● Streptomyces and Bradyrhizobium are enriched in RKN-infected rhizospheres.
	● Streptomyces but not Bradyrhizobium shows nematode-antagonistic activity.
	● Streptomyces combats RKN via nematicidal metabolites and JA pathway activation.

References

[1] Alzate Zuluaga, M.Y., Fattorini, R., Cesco, S., Pii, Y., 2024. Plant-microbe interactions in the rhizosphere for smarter and more sustainable crop fertilization: the case of PGPR-based biofertilizers. Frontiers in Microbiology15, 1440978.

[2] Bonkowski, M., Tarkka, M., Razavi, B.S., Schmidt, H., Blagodatskaya, E., Koller, R., Yu, P., Knief, C., Hochholdinger, F., Vetterlein, D., 2021. Spatiotemporal dynamics of maize (Zea Mays L.) root growth and its potential consequences for the assembly of the rhizosphere microbiota. Frontiers in Microbiology12, 619499.

[3] Buchan, D., Moeskops, B., Ameloot, N., De Neve, S., Sleutel, S., 2012. Selective sterilisation of undisturbed soil cores by gamma irradiation: effects on free-living nematodes, microbial community and nitrogen dynamics. Soil Biology and Biochemistry47, 10–13.

[4] Compant, S., Samad, A., Faist, H., Sessitsch, A., 2019. A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. Journal of Advanced Research19, 29–37.

[5] Costa, S.R., Ng, J.L.P., Mathesius, U., 2021. Interaction of symbiotic rhizobia and parasitic root-knot nematodes in legume roots: from molecular regulation to field application. Molecular Plant-Microbe Interactions^®34, 470–490.

[6] Dadi, F.A., Muthusamy, S., Ghosh, S., Muleta, D., Tesfaye, K., Assefa, F., Xu, J., Ghadamgahi, F., Ortiz, R., Vetukuri, R.R., 2025. Plant development influences dynamic shifts in the root compartment microbiomes of wild and domesticated finger millet cultivars. BMC Microbiology25, 259.

[7] Dai, R., Zhang, J.Y., Liu, F., Xu, H.R., Qian, J.M., Cheskis, S., Liu, W.D., Wang, B.L., Zhu, H.H., Pronk, L.J.U., Medema, M.H., de Jonge, R., Pieterse, C.M.J., Levy, A., Schlaeppi, K., Bai, Y., 2025. Crop root bacterial and viral genomes reveal unexplored species and microbiome patterns. Cell188, 2521–2539.e22.

[8] Edgar, R.C., 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics26, 2460–2461.

[9] Farda, B., Djebaili, R., Vaccarelli, I., Del Gallo, M., Pellegrini, M., 2022. Actinomycetes from caves: an overview of their diversity, biotechnological properties, and insights for their use in soil environments. Microorganisms10, 453.

[10] Habteweld, A., Kantor, M., Kantor, C., Handoo, Z., 2024. Understanding the dynamic interactions of root-knot nematodes and their host: role of plant growth promoting bacteria and abiotic factors. Frontiers in Plant Science15, 1377453.

[11] Han, L.L., Wang, Q., Shen, J.P., Di, H.J., Wang, J.T., Wei, W.X., Fang, Y.T., Zhang, L.M., He, J.Z., 2019. Multiple factors drive the abundance and diversity of the diazotrophic community in typical farmland soils of China. FEMS Microbiology Ecology95, fiz113.

[12] He, X.M., Wang, D.N., Jiang, Y., Li, M., Delgado-Baquerizo, M., McLaughlin, C., Marcon, C., Guo, L., Baer, M., Moya, Y.A.T., Von Wirén, N., Deichmann, M., Schaaf, G., Piepho, H.P., Yang, Z.K., Yang, J.L., Yim, B., Smalla, K., Goormachtig, S., De Vries, F.T., Hüging, H., Baer, M., Sawers, R.J.H., Reif, J.C., Hochholdinger, F., Chen, X.P., Yu, P., 2024. Heritable microbiome variation is correlated with source environment in locally adapted maize varieties. Nature Plants10, 598–617.

[13] Hu, L., Mateo, P., Ye, M., Zhang, X., Berset, J.D., Handrick, V., Radisch, D., Grabe, V., Köllner, T.G., Gershenzon, J., Robert, C.A.M., Erb, M., 2018a. Plant iron acquisition strategy exploited by an insect herbivore. Science361, 694–697.

[14] Hu, L.F., Robert, C.A.M., Cadot, S., Zhang, X., Ye, M., Li, B.B., Manzo, D., Chervet, N., Steinger, T., van der Heijden, M.G.A., Schlaeppi, K., Erb, M., 2018b. Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nature Communications9, 2738.

[15] Hu, L.F., Ye, M., Erb, M., 2019. Integration of two herbivore-induced plant volatiles results in synergistic effects on plant defence and resistance. Plant, Cell & Environment42, 959–971.

[16] Hu, L.F., Zhang, K.D., Xu, Y.C., Zheng, X.X., Waterman, J.M., Ouyang, X., Wu, Z.W., Shen, Z.C., He, Y., Ma, B., Robert, C.A.M., Raaijmakers, J.M., Ye, M., Erb, M., Xu, J.M., 2025. Herbivory-induced green leaf volatiles increase plant performance through jasmonate-dependent plant–soil feedbacks. Nature Plants11, 1001–1017.

[17] Kantor, M., Handoo, Z., Kantor, C., Carta, L., 2022. Top ten most important U.S. -regulated and emerging plant-parasitic nematodes. Horticulturae8, 208.

[18] Katoh, K., Misawa, K., Kuma, K.I., Miyata, T., 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research30, 3059–3066.

[19] Khan, S., Srivastava, S., Karnwal, A., Malik, T., 2023. Streptomyces as a promising biological control agents for plant pathogens. Frontiers in Microbiology14, 1285543.

[20] Köhl, J., Kolnaar, R., Ravensberg, W.J., 2019. Mode of action of microbial biological control agents against plant diseases: relevance beyond efficacy. Frontiers in Plant Science10, 845.

[21] Kudjordjie, E.N., Santos, S.S., Topalović, O., Vestergård, M., 2024. Distinct changes in tomato-associated multi-kingdom microbiomes during Meloidogyne incognita parasitism. Environmental Microbiome19, 53.

[22] La, S.K., Li, J.F., Ma, S., Liu, X.Q., Gao, L.H., Tian, Y.Q., 2024. Protective role of native root-associated bacterial consortium against root-knot nematode infection in susceptible plants. Nature Communications15, 6723.

[23] Li, L.L., Sun, Y.F., Chen, F.M., Hao, D.J., Tan, J.J., 2023a. An alkaline protease from Bacillus cereus NJSZ-13 can act as a pathogenicity factor in infection of pinewood nematode. BMC Microbiology23, 10.

[24] Li, T., Zhang, X.P., Liu, Q., Liu, J., Chen, Y.Q., Sui, P., 2022. Yield penalty of maize (Zea mays L. ) under heat stress in different growth stages: a review. Journal of Integrative Agriculture21, 2465–2476.

[25] Li, X., Hu, H.J., Li, J.Y., Wang, C., Chen, S.L., Yan, S.Z., 2019. Effects of the endophytic bacteria Bacillus cereus BCM2 on tomato root exudates and Meloidogyne incognita infection. Plant Disease103, 1551–1558.

[26] Li, Y., Lei, S.N., Cheng, Z.Q., Jin, L.Y., Zhang, T., Liang, L.M., Cheng, L.J., Zhang, Q.Y., Xu, X.H., Lan, C.H., Lu, C.J., Mo, M.H., Zhang, K.Q., Xu, J.P., Tian, B.Y., 2023b. Microbiota and functional analyses of nitrogen-fixing bacteria in root-knot nematode parasitism of plants. Microbiome11, 48.

[27] Lotrario, J.B., Stuart, B.J., Lam, T., Arands, R.R., O’Connor, O.A., Kosson, D.S., 1995. Effects of sterilization methods on the physical characteristics of soil: implications for sorption isotherm analyses. Bulletin of Environmental Contamination and Toxicology54, 668–675.

[28] Ma, W.M., Tang, S.H., Dengzeng, Z., Zhang, D., Zhang, T., Ma, X.L., 2022. Root exudates contribute to belowground ecosystem hotspots: a review. Frontiers in Microbiology13, 937940.

[29] Madigan, M., Cox, S.S., Stegeman, R.A., 1984. Nitrogen fixation and nitrogenase activities in members of the family Rhodospirillaceae. Journal of Bacteriology157, 73–78.

[30] Magoč, T., Salzberg, S.L., 2011. FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics27, 2957–2963.

[31] McNamara, N.P., Black, H.I.J., Beresford, N.A., Parekh, N.R., 2003. Effects of acute gamma irradiation on chemical, physical and biological properties of soils. Applied Soil Ecology24, 117–132.

[32] Mhatre, P.H., Thorat, Y.E., Manimaran, B., Divya, K.L., Bairwa, A., Chavan, S.N., Pokhare, S.S., Dukare, A.S., Karthik, C., 2024. Nematicidal activity of secondary metabolites from soil microbes. In: Chaudhary, K.K., Meghvansi, M.K., Siddiqui, S., eds. Sustainable Management of Nematodes in Agriculture, Vol. 2: Role of Microbes-Assisted Strategies. Cham: Springer, 297–324.

[33] Myo, E.M., Ge, B.B., Ma, J.J., Cui, H.L., Liu, B.H., Shi, L.M., Jiang, M.G., Zhang, K.C., 2019. Indole-3-acetic acid production by Streptomyces fradiae NKZ-259 and its formulation to enhance plant growth. BMC Microbiology19, 155.

[34] Navarro-Noya, Y.E., Chávez-Romero, Y., Hereira-Pacheco, S., de León Lorenzana, A.S., Govaerts, B., Verhulst, N., Dendooven, L., 2022. Bacterial communities in the rhizosphere at different growth stages of maize cultivated in soil under conventional and conservation agricultural practices. Microbiology Spectrum10, e01834–21.

[35] Nguyen, L.T., Schmidt, H.A., von Haeseler, A., Minh, B.Q., 2015. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution32, 268–274.

[36] Nimnoi, P., Ruanpanun, P., 2020. Suppression of root-knot nematode and plant growth promotion of chili (Capsicum flutescens L.) using co-inoculation of Streptomyces spp. Biological Control145, 104244.

[37] Ning, D.L., Deng, Y., Tiedje, J.M., Zhou, J.Z., 2019. A general framework for quantitatively assessing ecological stochasticity. Proceedings of the National Academy of Sciences of the United States of America116, 16892–16898.

[38] Przybylska, A., Kornobis, F., Obrępalska-Stęplowska, A., 2018. Analysis of defense gene expression changes in susceptible and tolerant cultivars of maize (Zea mays) upon Meloidogyne arenaria infection. Physiological and Molecular Plant Pathology103, 78–83.

[39] Przybylska, A., Obrępalska-Stęplowska, A., 2020. Plant defense responses in monocotyledonous and dicotyledonous host plants during root-knot nematode infection. Plant and Soil451, 239–260.

[40] Qu, Q., Zhang, Z.Y., Peijnenburg, W.J.G.M., Liu, W.Y., Lu, T., Hu, B.L., Chen, J.M., Chen, J., Lin, Z.F., Qian, H.F., 2020. Rhizosphere microbiome assembly and its impact on plant growth. Journal of Agricultural and Food Chemistry68, 5024–5038.

[41] Rognes, T., Flouri, T., Nichols, B., Quince, C., Mahé, F., 2016. VSEARCH: a versatile open source tool for metagenomics. PeerJ4, e2584.

[42] Segata, N., Izard, J., Waldron, L., Gevers, D., Miropolsky, L., Garrett, W.S., Huttenhower, C., 2011. Metagenomic biomarker discovery and explanation. Genome Biology12, R60.

[43] Sharma, R., Kapoor, N., Ohri, P., 2025. Ameliorative effect of rhizobacteria Bradyrhizobium japonicum on antioxidant enzymes, cell viability and biochemistry in tomato plant under nematode stress. Scientific Reports15, 8017.

[44] Shi, J.W., Sun, M., 2025. Bacillus thuringiensis: a gift for nematode management. Trends in Parasitology41, 235–246.

[45] Sun, X.W., Zhang, R., Ding, M.J., Liu, Y.X., Li, L., 2021. Biocontrol of the root-knot nematode Meloidogyne incognita by a nematicidal bacterium Pseudomonas simiae MB751 with cyclic dipeptide. Pest Management Science77, 4365–4374.

[46] Topalović, O., Hussain, M., Heuer, H., 2020. Plants and associated soil microbiota cooperatively suppress plant-parasitic nematodes. Frontiers in Microbiology11, 313.

[47] Topalović, O., Vestergård, M., 2021. Can microorganisms assist the survival and parasitism of plant-parasitic nematodes. Trends in Parasitology37, 947–958.

[48] Vasantha-Srinivasan, P., Park, K.B., Kim, K.Y., Jung, W.J., Han, Y.S., 2025. The role of Bacillus species in the management of plant-parasitic nematodes. Frontiers in Microbiology15, 1510036.

[49] Vlot, A.C., Sales, J.H., Lenk, M., Bauer, K., Brambilla, A., Sommer, A., Chen, Y.Y., Wenig, M., Nayem, S., 2021. Systemic propagation of immunity in plants. New Phytologist229, 1234–1250.

[50] Wang, Q., Garrity, G.M., Tiedje, J.M., Cole, J.R., 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology73, 5261–5267.

[51] Wang, R.B., Li, B.J., Cai, S.L., Ding, Y.F., Shi, M.Y., Jin, T., Lin, W., Liu, P.Q., 2024a. Genetic diversity of Ralstonia solanacearum causing tobacco bacterial wilt in Fujian province and identification of biocontrol Streptomyces sp. Plant Disease108, 1946–1958.

[52] Wang, X.M., Wu, M., Wei, Z.J., Hazard, C., Nicol, G.W., Zhao, H.C., Liu, B.B., Zhang, J., Shan, J., Yan, X.Y., 2024b. Investigating drivers of free-living diazotroph activity in paddy soils across China. Soil Biology and Biochemistry199, 109601.

[53] Wilschut, R.A., Geisen, S., 2021. Nematodes as drivers of plant performance in natural systems. Trends in Plant Science26, 237–247.

[54] Xu, X.M., Dinesen, C., Pioppi, A., Kovács, Á.T., Lozano-Andrade, C.N., 2025. Composing a microbial symphony: synthetic communities for promoting plant growth. Trends in Microbiology33, 738–751.

[55] Yang, Z.J., Qiao, Y.J., Konakalla, N.C., Strøbech, E., Harris, P., Peschel, G., Agler-Rosenbaum, M., Weber, T., Andreasson, E., Ding, L., 2023. Streptomyces alleviate abiotic stress in plant by producing pteridic acids. Nature Communications14, 7398.

[56] Ye, M., Liu, M.M., Erb, M., Glauser, G., Zhang, J., Li, X.W., Sun, X.L., 2021. Indole primes defence signalling and increases herbivore resistance in tea plants. Plant, Cell & Environment44, 1165–1177.

[57] Yergaliyev, T.M., Alexander-Shani, R., Dimerets, H., Pivonia, S., Bird, D.M., Rachmilevitch, S., Szitenberg, A., 2020. Bacterial community structure dynamics in Meloidogyne incognita-infected roots and its role in worm-microbiome interactions. mSphere5, e00306–20.

[58] Yu, P., He, X.M., Baer, M., Beirinckx, S., Tian, T., Moya, Y.A.T., Zhang, X.C., Deichmann, M., Frey, F.P., Bresgen, V., Li, C.J., Razavi, B.S., Schaaf, G., von Wirén, N., Su, Z., Bucher, M., Tsuda, K., Goormachtig, S., Chen, X.P., Hochholdinger, F., 2021. Plant flavones enrich rhizosphere Oxalobacteraceae to improve maize performance under nitrogen deprivation. Nature Plants7, 481–499.

[59] Yu, Y.Y., Gui, Y., Li, Z.J., Jiang, C.H., Guo, J.H., Niu, D.D., 2022. Induced systemic resistance for improving plant immunity by beneficial microbes. Plants11, 386.

[60] Zhang, H.L., Guo, D.S., Lei, Y.T., Lozano-Torres, J.L., Deng, Y., Xu, J.M., Hu, L.F., 2025. Cover crop rotation suppresses root-knot nematode infection by shaping soil microbiota. New Phytologist245, 363–377.

[61] Zhang, J.Y., Liu, Y.X., Zhang, N., Hu, B., Jin, T., Xu, H.R., Qin, Y., Yan, P.X., Zhang, X.N., Guo, X.X., Hui, J., Cao, S.Y., Wang, X., Wang, C., Wang, H., Qu, B.Y., Fan, G.Y., Yuan, LX., Garrido-Oter, R., Chu, C.C., Bai, Y., 2019. NRT1.1B is associated with root microbiota composition and nitrogen use in field-grown rice. Nature Biotechnology37, 676–684.

[62] Zhou, D.M., Feng, H., Schuelke, T., De Santiago, A., Zhang, Q.M., Zhang, J.F., Luo, C.P., Wei, L.H., 2019. Rhizosphere microbiomes from root knot nematode non-infested plants suppress nematode infection. Microbial Ecology78, 470–481.

[63] Zhu, L., Huang, J.M., Lu, X.M., Zhou, C., 2022. Development of plant systemic resistance by beneficial rhizobacteria: recognition, initiation, elicitation and regulation. Frontiers in Plant Science13, 952397.

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