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A cooperative regulatory module between TAGL2 and JMJC1 activates specific defense genes against root-knot nematodes in tomato.

Ting Yang·Yile Miao·Jiameng Zhao·Weiduo Jin·Tingting Ran·Tina Kyndt·Jingquan Yu·Jie Zhou
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Abstract

Plant-parasitic nematodes (PPNs) threaten global food security. Although epigenetic modifications are crucial for plant immunity, how histone modifiers contribute to root-knot nematodes (RKNs, Meloidogyne incognita) resistance remains unclear. Here, using genetic, molecular and biochemical approaches, we investigated the epigenetic and transcriptional mechanisms underlying RKN resistance mediated by the histone demethylase (HDM) JMJC1 and the MADS-box transcription factor TAGL2 in tomato (Solanum lycopersicum). We identified JMJC1 as an RKN-induced positive defense regulator targeting H3K9me3 and H3K27me3 histone marks. JMJC1 physically interacts with TAGL2, which also positively regulates RKN resistance. Transcriptomic analysis indicated that TAGL2 regulates multiple layers of the plant defense network, transcriptionally activating representative genes from distinct pathways (including PUB10, bHLH98, CCaMK, and SAUR3), which we validated as positive regulators of RKN resistance via virus-induced gene silencing (VIGS). At the chromatin level, TAGL2 and JMJC1 co-regulate these loci, associating with localized H3K9me3 and H3K27me3 reduction. Furthermore, TAGL2 directly activates JMJC1 transcription, establishing a positive feedback loop that amplifies immune signaling. Our findings reveal a cooperative model wherein a HDM and a transcription factor coordinate at specific loci to fine-tune multiple defense layers at both epigenetic and transcriptional levels, providing insights for breeding durable nematode-resistant plants.

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Solanum lycopersicumAnimalsGene Expression Regulation, PlantPlant ProteinsPlant DiseasesPlant RootsTylenchoideaHistonesGenes, PlantDisease ResistanceProtein BindingTranscription FactorsJMJC1MADS‐box transcription factorTAGL2histone demethylaseroot‐knot nematodetomatoJournal Article

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Ting Yang, Yile Miao, Jiameng Zhao, Weiduo Jin, Tingting Ran, Tina Kyndt, Jingquan Yu, Jie Zhou. 2026-08-09. A cooperative regulatory module between TAGL2 and JMJC1 activates specific defense genes against root-knot nematodes in tomato.. https://doi.org/10.1111/nph.71496

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Journal Article resourceAnimals subjectDisease Resistance subjectJournal Article subjectPlant Diseases subjectPlant Proteins subjectPlant Roots subject

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