Fruit ripening is a complex physiological process involving softening, color change, and aroma synthesis. In tomatoes, this process is closely related to ethylene production and signaling. Previous studies have identified several transcription factors, such as RIN, FUL1, and HY5, as core regulators in fruit ripening. Recently, the importance of DNA methylation as an epigenetic modification in fruit ripening has gained attention, yet its precise role in tomato fruit ripening remains unclear.

A research team led by Professor Zhaobo Lang from the Southern University of Science and Technology (SUSTech) published a study that uncovers the pivotal roles of two key transcription factors, RIN and FUL1, in DNA methylation-mediated regulation of tomato fruit ripening, proposing a novel “epigenetic permission” regulatory model.

Their paper, titled “Two Transcription Factors Play Critical Roles in Mediating Epigenetic Regulation of Fruit Ripening in Tomato”, has been published in the Proceedings of the National Academy of Sciences (PNAS).

The researchers focused on the demethylation enzyme DML2 and elucidated its molecular mechanisms in regulating tomato fruit ripening. The study found that DNA methylation regulates the expression of transcription factors RIN and FUL1, which are critical for tomato fruit ripening. In DML2 mutants, the expressions of both RIN and FUL1 were silenced, leading to similar ripening phenotypes in rin/ful1 double mutants and dml2 mutants. Restoration of RIN expression in dml2 mutants partially rescued the ripening defects and restored ethylene production, highlighting the functional redundancy of RIN and FUL1 downstream of DML2.

Further analyses through ChIP-seq and EMSA experiments revealed that DNA hypermethylation in dml2 mutants indirectly represses RIN binding by altering chromatin structure at a subset of RIN targets. These findings suggest that DML2 not only regulates the expression of ripening factors RIN and FUL1 but also influences RIN’s binding to downstream regulatory sites, affecting fruit ripening.

This research provides new insights into the epigenetic regulation of fruit ripening and offers theoretical evidence for understanding how DNA methylation impacts transcription factor binding in plants.

Professor Qingfeng Niu from Anhui Agricultural University is the first author of the paper. Drs. Yaping Xu and Huan Huang are the co-first authors, with Professors Zhaobo Lang and Jian-Kang Zhu from SUSTech serving as the corresponding authors.

Paper link: https://www.pnas.org/doi/10.1073/pnas.2422798122

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