INCREASED DNA METHYLATION 3 forms a potential chromatin remodelling complex with HAIRPLUS to regulate DNA methylation and trichome development in tomato

Nyikó, Tünde and Gyula, Péter and Ráth, Szilvia and Sós-Hegedűs, Anita and Csorba, Tibor and Abbas, Syed Hussam and Bóka, Károly and Pettkó-Szandtner, Aladár and Móricz, Ágnes and Molnár, Béla Péter and Erdei, Anna Laura and Szittya, György (2025) INCREASED DNA METHYLATION 3 forms a potential chromatin remodelling complex with HAIRPLUS to regulate DNA methylation and trichome development in tomato. PLANT JOURNAL, 121 (6). No. e70085. ISSN 0960-7412

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Abstract

DNA methylation, a dynamic epigenetic mark influencing gene expression, is regulated by DNA demethylases that remove methylated cytosines at genomic regions marked by the INCREASED DNA METHYLATION (IDM) complex. In Arabidopsis , IDM3, a small α‐crystalline domain‐containing protein, stabilises the IDM complex. To investigate its role in tomato, we generated slidm3 mutants using genome editing. These mutants displayed a ‘hairy’ phenotype with increased glandular trichomes, resembling the hairplus ( hap ) mutant. Affinity purification of SlIDM3‐GFP associated proteins identified several chromatin remodelling factors, including HAP. Genome‐wide DNA methylation analysis revealed sequence context dependent alterations in the slidm3‐1 plants, similar to the hap mutant. CHH methylation was predominantly increased, while CG methylation, particularly in intergenic regions, was decreased in both mutants. This imbalanced methylation suggests the presence of a ‘methylstat’ mechanism attempting to restore methylation levels at abnormally demethylated sites in the mutants. Comparative functional analysis of differentially methylated regions in the slidm3‐1 and hap mutants identified potential methylation‐regulated genes that could be linked to the hairy phenotype. Our findings indicate that SlIDM3 may form a chromatin remodelling complex with HAP, epigenetically regulating trichome development.

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