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<p>Reduction of DNA methylation has traditionally been associated with gene activation. Here, we show that DNA hypomethylation permits the binding of a transcriptional repressor, leading to gene silencing. In tomato, the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE TF SlSPL-CNR exhibits methylation-sensitive DNA binding and preferentially occupies unmethylated GTACGG motifs. During fruit ripening, DEMETER-LIKE 2 (SlDML2)-mediated DNA demethylation at the <i>alcohol acyltransferase 1</i> (<i>SlAAT1</i>) promoter allows SlSPL-CNR binding, which in turn represses <i>SlAAT1</i> expression and thereby modulates the biosynthesis of ester metabolites—key components of fruit flavor. Structural analysis reveals that cytosine methylation introduces a steric clash with Gln94 in the SBP domain of SlSPL-CNR, explaining its methylation sensitivity. CRISPR knockout of <i>SlSPL-CNR</i> de-represses <i>SlAAT1</i> and increases ester accumulation, confirming its inhibitory role. Importantly, this methylation-sensitive binding is conserved across SBP domain proteins from rice, maize, and tomato. Our findings reveal a mechanism in which DNA hypomethylation facilitates repressor recruitment, establishing a regulatory logic linking epigenetic dynamics to metabolic control in plants.</p>

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DNA hypomethylation enables the transcriptional repressor SlSPL-CNR to control fruit flavor ester biosynthesis

  • 期刊论文

  • 出版模式：

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  • 发表日期：

    2026年7月1日

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  • Zhifeng Zeng,
  • Yu Ma,
  • Hang He,
  • Linzhu Li,
  • Yuan Peng,
  • Yawen Hou,
  • Songge Chai,
  • Pengcheng Wang,
  • Cheng-Guo Duan,
  • Jian-Kang Zhu,
  • Jiamu Du,
  • Zhaobo Lang

摘要

Reduction of DNA methylation has traditionally been associated with gene activation. Here, we show that DNA hypomethylation permits the binding of a transcriptional repressor, leading to gene silencing. In tomato, the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE TF SlSPL-CNR exhibits methylation-sensitive DNA binding and preferentially occupies unmethylated GTACGG motifs. During fruit ripening, DEMETER-LIKE 2 (SlDML2)-mediated DNA demethylation at the alcohol acyltransferase 1 (SlAAT1) promoter allows SlSPL-CNR binding, which in turn represses SlAAT1 expression and thereby modulates the biosynthesis of ester metabolites—key components of fruit flavor. Structural analysis reveals that cytosine methylation introduces a steric clash with Gln94 in the SBP domain of SlSPL-CNR, explaining its methylation sensitivity. CRISPR knockout of SlSPL-CNR de-represses SlAAT1 and increases ester accumulation, confirming its inhibitory role. Importantly, this methylation-sensitive binding is conserved across SBP domain proteins from rice, maize, and tomato. Our findings reveal a mechanism in which DNA hypomethylation facilitates repressor recruitment, establishing a regulatory logic linking epigenetic dynamics to metabolic control in plants.