植物寄生線蟲是威脅多數作物的主要威脅之一，據統計光是根瘤線蟲就能夠導致番茄產量損失高達40 %。而目前已知攜帶 Mi-1 基因座的野生番茄品系具有對根瘤線蟲的天然抗性，能夠顯著減少根瘤和卵塊形成。為培育抗線蟲的栽培種品系，育種者通常將 Mi-1 基因座引入商業番茄品種。為更加了解Mi-1基因座所提供的線蟲抗性，本研究中，我們透過基因分型標記篩選出 Mi/Mi（抗線蟲）與 mi/mi（易感線蟲）純系品系，並確認 Mi/Mi 相較 mi/mi 具有顯著抗 Meloidogyne incognita 的能力，且能抑制線蟲發育。進一步，我們針對感染前後的 Mi/Mi 與 mi/mi 品系進行定量蛋白體與代謝體分析，系統性的探索與 Mi-1 抗性相關的分子路徑。我們的研究結果表明，Mi-1介導的抗性涉及免疫途徑、壓力反應和代謝調控的協同變化。本研究闡明了抗線蟲和易感線蟲番茄基因型在根瘤線蟲感染過程中的多層次分子變化，揭示了基因型和感染階段對植物生理和代謝狀態的深遠影響，並為深入理解抗線蟲番茄與線蟲相互作用的關係提供整合性資料基礎。

Plant-parasitic nematodes pose a major threat to most crops. Statistics show that root-knot nematodes (RKNs) alone can cause up to a 40% yield loss in tomato production. Wild tomato varieties carrying the Mi-1 locus are known to possess natural resistance to RKNs, significantly reducing gall and egg mass formation. To develop resistant commercial cultivars, breeders typically introgressed the Mi-1 locus into cultivated tomato lines. To investigate the nematode resistance conferred by the Mi-1 locus, we screened and selected Mi/Mi (resistant) and mi/mi (susceptible) homozygous tomato lines by using a specific genotyping marker. Phenotypic resistance assays confirmed that Mi/Mi lines exhibited significantly stronger resistance to Meloidogyne incognita compared to mi/mi lines, including suppression of nematode development. Furthermore, we conducted quantitative proteomic and metabolomic analyses on both genotypes before and after nematode infection to identify molecular pathways associated with Mi-1-mediated resistance. Our results reveal that Mi-1-mediated resistance involves coordinated changes in immune pathways, stress responses, and metabolic regulation. This study elucidates the multilayered molecular changes in resistant and susceptible tomato genotypes during root-knot nematode infection, revealing the profound impact of genotype and infection stage on the plant's physiological and metabolic status. It provides an integrative data framework for advancing our understanding of resistant tomato and nematode interactions.

Abad P, Favery B, Rosso MN, Castagnone-Sereno P. Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Molecular Plant Pathology. 2003;4:217-24.
Abad P, Williamson VM. Plant Nematode Interaction: A Sophisticated Dialogue. Advances in Botanical Research, Vol 53. 2010;53:147-92.
Abdul-Baki AA, Haroon SA, Chitwood DJJH. Temperature effects on resistance to Meloidogyne spp. in excised tomato roots. HORTSCIENCE. 1996;31:147-9.
Adriana Murillo-Williams AC, Paul D. Esker. Plant Parasitic Nematodes Explained. Penn State Extension. 2023.
Aioub AA, Elesawy AE, Ammar EEJJoPD, Protection. Plant growth promoting rhizobacteria (PGPR) and their role in plant-parasitic nematodes control: a fresh look at an old issue. Journal of Plant Diseases and Protection. 2022;129:1305-21.
Ammati M, Thomason I, Mckinney HJJoN. Retention of resistance to Meloidogyne incognita in Lycopersicon genotypes at high soil temperature. Journal of Nematology. 1986;18:491.
Azlay L, El Boukhari MEM, Mayad EH, Barakate MJOA. Biological management of root-knot nematodes (Meloidogyne spp.): a review. Agricultural Sciences. 2023;13:99-117.
Bano S, Iqbal EY, Lubna, Zik-ur-Rehman S, Fayyaz S, Faizi S. Nematicidal activity of flavonoids with structure activity relationship (SAR) studies against root knot nematode Meloidogyne incognita. European Journal of Plant Pathology. 2020;157:299-309.
Banora MY. Impacting of Root-Knot Nematodes on Tomato: Current Status and Potential Horizons for Its Managing. IntechOpen. 2024.
Banora MY, Almaghrabi OAAJJoPPR. Differential response of some nematode-resistant and susceptible tomato genotypes to Meloidogyne javanica infection. Journal of Plant Protection Research. 2019;59.
Batistic O, Waadt R, Steinhorst L, Held K, Kudla J. CBL-mediated targeting of CIPKs facilitates the decoding of calcium signals emanating from distinct cellular stores. The Plant Journal. 2010;61:211-22.
Bellafiore S, Shen Z, Rosso MN, Abad P, Shih P, Briggs SP. Direct identification of the Meloidogyne incognita secretome reveals proteins with host cell reprogramming potential. PLoS Pathogens. 2008;4:e1000192.
Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I. The MI-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiology. 2007;144:312-23.
Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T, Navarre DA, et al. Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Molecular Plant-Microbe Interactions. 2008;21:1205-14.
Bigeard J, Colcombet J, Hirt H. Signaling mechanisms in pattern-triggered immunity (PTI). Molecular Plant. 2015;8:521-39.
Branch C, Hwang CF, Navarre DA, Williamson VM. Salicylic acid is part of the --mediated defense response to root-knot nematode in tomato. Molecular Plant-Microbe Interactions. 2004;17:351-6.
Branon TC, Bosch JA, Sanchez AD, Udeshi ND, Svinkina T, Carr SA, et al. Efficient proximity labeling in living cells and organisms with TurboID. Nature Biotechnology. 2018;36:880-7.
Chand RC, Subhash, Vimal S, Gautam S, Singh D, Pratap D. Impact assessment of neem products in the control of root-knot nematode, Meloidogyne incognita on Brinjal. Scientist. 2022;3:3496-501.
Chen YL, Fan KT, Hung SC, Chen YR. The role of peptides cleaved from protein precursors in eliciting plant stress reactions. New Phytologist. 2020;225:2267-82.
Chowanski S, Adamski Z, Marciniak P, Rosinski G, Büyükgüzel E, Büyükgüzel K, et al. A Review of Bioinsecticidal Activity of Alkaloids. Toxins. 2016;8.
Cooper WR, Jia L, Goggin L. Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars. Journal of Chemical Ecology. 2005;31:1953-67.
Cui J, Jiang N, Meng J, Yang G, Liu W, Zhou X, et al. LncRNA33732-respiratory burst oxidase module associated with WRKY1 in tomato- Phytophthora infestans interactions. The Plant Journal. 2019;97:933-46.
de Ilarduya OM, Nombela G, Hwang CF, Williamson VM, Muñiz M, Kaloshian I. is necessary for -mediated resistance and acts early in the resistance pathway. Molecular Plant-Microbe Interactions. 2004;17:55-61.
De Waele D, Elsen A. Challenges in tropical plant nematology. Annual Review of Phytopathology. 2007;45:457-85.
Devran Z, Özalp T, Studholme DJ, Tör M. Mapping of the gene in tomato conferring resistance to root-knot nematodes at high soil temperature. Frontiers in Plant Science. 2023;14.
Dropkin V. The necrotic reaction of tomatoes and other hosts resistant to Meloidogyne. reversal by temperature. Phytopathology. 1969a;59:1632-1637.
Dropkin VH. Cellular responses of plants to nematode infections. Annual Review of Phytopathology. 1969b;7.
El-Sappah AH, M MI, H HE-A, Yan S, Qi S, Liu J, et al. Tomato Natural Resistance Genes in Controlling the Root-Knot Nematode. Genes (Basel). 2019;10.
Forghani F, Hajihassani AJFips. Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Frontiers in Plant Science. 2020;11:1125.
Fujimoto T, Tomitaka Y, Abe H, Tsuda S, Futai K, Mizukubo T. Expression profile of jasmonic acid-induced genes and the induced resistance against the root-knot nematode (Meloidogyne incognita) in tomato plants (Solanum lycopersicum) after foliar treatment with methyl jasmonate. Journal of Plant Physiology. 2011;168:1084-97.
Garcia BE, Mejía L, Salus MS, Martin CT, Seah S, Williamson VM, et al. A co-dominant SCAR marker , Mi 23 , for detection of the Mi-1 . 2 gene for resistance to root-knot nematode in tomato germplasm. Tomato Genetics Cooperative Report. 2007.
Haeger W, Henning J, Heckel DG, Pauchet Y, Kirsch R. Direct evidence for a new mode of plant defense against insects via a novel polygalacturonase-inhibiting protein expression strategy. Journal of Biological Chemistry. 2020;295:11833-44.
Herlihy JH, Long TA, McDowell JM. Iron homeostasis and plant immune responses: Recent insights and translational implications. The Journal of Biological Chemistry. 2020;295:13444-57.
Ho JY, Weide R, Ma HM, van Wordragen MF, Lambert KN, Koornneef M, et al. The root-knot nematode resistance gene (Mi) in tomato: construction of a molecular linkage map and identification of dominant cDNA markers in resistant genotypes. The Plant Jornal. 1992;2:971-82.
Hunt DJ, Handoo ZA. Taxonomy, Identification and Principal Species. Root-Knot Nematodes. 2010:55-97.
Huot B, Yao J, Montgomery BL, He SY. Growth-defense tradeoffs in plants: a balancing act to optimize fitness. Molecular Plant. 2014;7:1267-87.
Hwang CF, Williamson VM. Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. The Plant Jornal. 2003;34:585-93.
Hwang IS, Hwang BK. The pepper mannose-binding lectin gene CaMBL1 is required to regulate cell death and defense responses to microbial pathogens. Plant Physiology. 2011;155:447-63.
Ioannou N. Soil solarization as a substitute for methyl bromide fumigation in greenhouse tomato production in Cyprus. Phytoparasitica. 2000;28:248-56.
Jagodzik P, Tajdel-Zielinska M, Ciesla A, Marczak M, Ludwikow A. Mitogen-Activated Protein Kinase Cascades in Plant Hormone Signaling. Frontiers in Plant Science. 2018;9:1387.
Jaouannet M, Magliano M, Arguel MJ, Gourgues M, Evangelisti E, Abad P, et al. The Root-Knot Nematode Calreticulin Mi-CRT Is a Key Effector in Plant Defense Suppression. Molecular Plant-Microbe Interactions. 2013;26:97-105.
Kammerhofer N, Radakovic Z, Regis JM, Dobrev P, Vankova R, Grundler FM, et al. Role of stress-related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytologist. 2015;207:778-89.
Lee J-M, Kubota C, Tsao SJ, Bie Z, Echevarria PH, Morra L, et al. Current status of vegetable grafting: Diffusion, grafting techniques, automation. Scientia Horticulturae. 2010;127:93-105.
Letia S, Bhattacharyya S, Mendy B, Vothknecht UC, von Reuss SH, Inada M, et al. Ascaroside#18 Promotes Plant Defence by Repressing Auxin Signalling. Physiologia Plantarum. 2025;177:e70386.
Ma M, Taylor PWJ, Chen D, Vaghefi N, He JZ. Major Soilborne Pathogens of Field Processing Tomatoes and Management Strategies. Microorganisms. 2023;11.
Manohar M, Tenjo-Castano F, Chen S, Zhang YK, Kumari A, Williamson VM, et al. Plant metabolism of nematode pheromones mediates plant-nematode interactions. Nature Communications. 2020;11:208.
Manosalva P, Manohar M, von Reuss SH, Chen S, Koch A, Kaplan F, et al. Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nature Communications. 2015;6:7795.
Mantelin S, Bhattarai KK, Jhaveri TZ, Kaloshian I. Mi-1-mediated resistance to Meloidogyne incognita in tomato may not rely on ethylene but hormone perception through ETR3 participates in limiting nematode infection in a susceptible host. PLoS One. 2013;8:e63281.
Marques de Carvalho L, Benda ND, Vaughan MM, Cabrera AR, Hung K, Cox T, et al. Mi-1-Mediated Nematode Resistance in Tomatoes is Broken by Short-Term Heat Stress but Recovers Over Time. Journal of Nematology. 2015;47:133-40.
Martínez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CMJ, Van Wees SCM. Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by protects tomato against the root knot nematode. New Phytologist. 2017;213:1363-77.
Mejias J, Truong NM, Abad P, Favery B, Quentin M. Plant Proteins and Processes Targeted by Parasitic Nematode Effectors. Frontiers in Plant Science. 2019;10:970.
Melech-Bonfil S, Sessa G. Tomato MAPKKKε is a positive regulator of cell-death signaling networks associated with plant immunity. The Plant Joural. 2010;64:379-91.
Meng X, Zhang S. MAPK cascades in plant disease resistance signaling. Annual Review of Phytopathology. 2013;51:245-66.
Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM. The Root Knot Nematode Resistance Gene Mi from Tomato Is a Member of the Leucine Zipper, Nucleotide Binding, Leucine-Rich Repeat Family of Plant Genes. The Plant Cell. 1998;10:1307-19.
Molinari S, Fanelli E, Leonetti P. Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in mediated and SA-induced resistance to root-knot nematodes. Molecular Plant Pathology. 2014;15:255-64.
Monson RK, Trowbridge AM, Lindroth RL, Lerdau MT. Coordinated resource allocation to plant growth-defense tradeoffs. New Phytologist. 2022;233:1051-66.
Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C. The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiology. 2006;140:249-62.
Nelson SD, Locascio SJ, Allen LH, Dickson DW, Mitchell DJ. Soil flooding and fumigant alternatives to methyl bromide in tomato and eggplant production. Hortscience. 2002;37:1057-60.
Nguyen CN, Perfus-Barbeoch L, Quentin M, Zhao J, Magliano M, Marteu N, et al. A root-knot nematode small glycine and cysteine-rich secreted effector, MiSGCR1, is involved in plant parasitism. New Phytologist. 2018;217:687-99.
Nguyen TLA, Bhattacharya D. Antimicrobial Activity of Quercetin: An Approach to Its Mechanistic Principle. Molecules. 2022;27.
Nikoo FS, Sahebani N, Aminian H, Mokhtarnejad L, Ghaderi R. Induction of systemic resistance and defense-related enzymes in tomato plants using Pseudomonas fluorescens CHAO and salicylic acid against root-knot nematode Meloidogyne javanica. Journal of Plant Protection Research. 2014;54:383-9.
Niu JH, Liu P, Liu Q, Chen CL, Guo QX, JunmeiYin, et al. Msp40 effector of root-knot nematode manipulates plant immunity to facilitate parasitism. Scientific Reports. 2016;6.
Özalp T, Devran Z. Response of tomato plants carrying gene to (Kofoid & White, 1919) Chitwood, 1949 under high soil temperatures. Turkiye Entomoloji Dergisi-Turkish Journal of Entomology. 2018;42:313-22.
Palomares-Rius JE, Escobar C, Cabrera J, Vovlas A, Castillo P. Anatomical Alterations in Plant Tissues Induced by Plant-Parasitic Nematodes. Frontiers in Plant Science. 2017;8.
Perpétuo LS, Cunha M, Batista MT, Conceição IL. Evaluation of Solanum linnaeanum and S. sisymbriifolium extracts for the management of Meloidogynechitwoodi. Heliyon. 2023;9:e16298.
Perry RN, Moens M, Starr JL. Root-knot nematodes. Cambridge, MA: CABI North American Office; 2009.
Prautsch J, Erickson JL, Özyürek S, Gormanns R, Franke L, Lu Y, et al. Effector XopQ-induced stromule formation in Nicotiana benthamiana depends on ETI signaling components ADR1 and NRG1. Plant Physiology. 2023;191:161-76.
Regmi H, Desaeger J. Integrated management of root-knot nematode (Meloidogyne spp.) in Florida tomatoes combining host resistance and nematicides. Crop Protection. 2020;134.
Ren C, Zhu X, Zhang P, Gong Q. Arabidopsis COP1-interacting protein 1 is a positive regulator of ABA response. Biochemical and Biophysical Research Communications. 2016;477:847-53.
Rodiuc N, Vieira P, Banora MY, de Almeida Engler J. On the track of transfer cell formation by specialized plant-parasitic nematodes. Frontiers in Plant Science. 2014;5:160.
Satyandra Singh BS, A.P. Singh,. Nematodes: A Threat to Sustainability of Agriculture. Procedia Environmental Sciences. 2015;29:215-6.
Schouteden N, De Waele D, Panis B, Vos CMJFim. Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Frontiers in Microbiology. 2015;6:1280.
Shi Y, Zhang Z, Yan Z, Chu H, Luo C. Tomato mitogen-activated protein kinase: mechanisms of adaptation in response to biotic and abiotic stresses. Frontiers in Plant Science. 2025;16:1533248.
Shinde BA, Dholakia BB, Hussain K, Aharoni A, Giri AP, Kamble AC. WRKY1 acts as a key component improving resistance against Alternaria solani in wild tomato, Solanum arcanum Peralta. Plant Biotechnology Journal. 2018;16:1502-13.
Smith PG. Embryo culture of a tomato species hybrid. Proceedings of the American Society for Horticultural Science. 1944;44:413–416.
Solo N, Kud J, Dandurand LM, Caplan A, Kuhl JC, Xiao F. Characterization of Superoxide Dismutase from the Potato Cyst Nematode, Globodera pallida. Phytopathology. 2021;111:2110-7.
Stuart Seah VMW, Brenda E. Garcia, L. Mejía, Melinda S. Salus, Christopher T. Martin, and Douglas P. Maxwell. Evaluation of a co-dominant SCAR marker for detection of the Mi-1 locus for resistance to root-knot nematode in tomato germplasm. Tomato Genetic Cooperative Report. 2007;57:37–40.
Talavera M, Verdejo-Lucas S, Ornat C, Torres J, Vela MD, Macias FJ, et al. Crop rotations with gene resistant and susceptible tomato cultivars for management of root-knot nematodes in plastic houses. Crop Protection. 2009;28:662-7.
Tang RJ, Wang C, Li K, Luan S. The CBL-CIPK Calcium Signaling Network: Unified Paradigm from 20 Years of Discoveries. Trends in Plant Science. 2020;25:604-17.
Thomas T, Sakure AA, Kumar S, Mishra A, Ahmad S, Rojasara YM, et al. The Mi- 1 gene is a key regulator of defence mechanisms and cellular gene dynamics in response to root-knot nematodes. Plant Cell Reports. 2025;44.
ul Hassan MN, Zainal Z, Ismail I. Plant kelch containing F-box proteins: structure, evolution and functions. Rsc Advances. 2015;5:42808-14.
Vanlay M, Samnang S, Jung HJ, Choe P, Kang KK, Nou IS. Interspecific and Intraspecific Hybrid Rootstocks to Improve Horticultural Traits and Soil-Borne Disease Resistance in Tomato. Genes (Basel). 2022;13.
Verbon EH, Trapet PL, Stringlis IA, Kruijs S, Bakker P, Pieterse CMJ. Iron and Immunity. Annual Review of Phytopathology. 2017;55:355-75.
Verdejo-Lucas S, Blanco M, Cortada L, Sorribas FJJCP. Resistance of tomato rootstocks to Meloidogyne arenaria and Meloidogyne javanica under intermittent elevated soil temperatures above 28°C. Crop Protection. 2013;46:57-62.
Wang X, Xue B, Dai J, Qin X, Liu L, Chi Y, et al. A novel chorismate mutase effector suppresses plant immunity by manipulating the salicylic acid pathway and functions mainly during the early stages of nematode parasitism. Plant Pathology. 2018;67:1436-48.
Wang Y, Bao Z, Zhu Y, Hua JJMp-mi. Analysis of temperature modulation of plant defense against biotrophic microbes. Molecular Plant-Microbe Interactions. 2009;22:498-506.
Weinl S, Kudla J. The CBL-CIPK Ca(2+)-decoding signaling network: function and perspectives. New Phytologist. 2009;184:517-28.
Williamson VM, Hussey RS. Nematode pathogenesis and resistance in plants. Plant Cell. 1996;8:1735-45.
Williamson VMJARoP. Root-knot nematode resistance genes in tomato and their potential for future use. Annual Review of Phytopathology. 1998;36:277-93.
Wondafrash M, Van Dam NM, Tytgat TO. Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects. Frontiers in Plant Science. 2013;4:87.
Xie M, Yu B. siRNA-directed DNA Methylation in Plants. Current Genomics. 2015;16:23-31.
Yadav H, Roberts PA, Lopez-Arredondo D. Combating Root-Knot Nematodes (Meloidogyne spp.): From Molecular Mechanisms to Resistant Crops. Plants (Basel). 2025;14.
Yadav M, Pandey J, Chakraborty A, Hassan MI, Kundu JK, Roy A, et al. A Comprehensive Analysis of Calmodulin-Like Proteins of Indicates Their Role in Calcium Signaling and Plant Defense Against Insect Attack. Frontiers in Plant Science. 2022;13.
Ye W, Robbins RT, Kirkpatrick T. Molecular characterization of root-knot nematodes (Meloidogyne spp.) from Arkansas, USA. Scientific Reports. 2019;9:15680.
Yu XQ, Niu HQ, Liu C, Wang HL, Yin W, Xia X. PTI-ETI synergistic signal mechanisms in plant immunity. Plant Biotechnology Journal. 2024;22:2113-28.
Yue SY, Xu P, Cao ZH, Zhuang M. PUP-IT2 as an alternative strategy for PUP-IT proximity labeling. Frontiers in Molecular Biosciences. 2022;9.
Zhao G, Guo D, Wang L, Li H, Wang C, Guo X. Functions of RPM1-interacting protein 4 in plant immunity. Planta. 2021;253:11.
Zhou J, Xu X-C, Cao J-J, Yin L-L, Xia X-J, Shi K, et al. Heat shock factor HsfA1a is essential for R gene-mediated nematode resistance and triggers H2O2 production. Plant Physiology. 2018;176:2456-71.
蔡佳芳, 蔡東纂, 陳珮臻. 土壤溫度對三種根瘤線蟲Meloidogyne incognita, M. javanica及M. hapla侵入與發育之影響. 植物病理學會刊. 2010;19:235-42.