Two transcription factors play critical roles in mediating epigenetic regulation of fruit ripening in tomato

Qingfeng Niu, Yaping Xu, Huan Huang, Linzhu Li, Dengguo Tang, Siqun Wu, Ping Liu, Ruie Liu, Yu Ma, Bo Zhang, Jian-Kang Zhu, Zhaobo Lang

Proc Natl Acad Sci U S A; 2025 Apr 15; 122(15):e2422798122. doi:10.1073/pnas.2422798122.

Abstract

DNA methylation regulates fruit ripening in tomato, and disruption of the DNA demethylase DEMETER-LIKE 2 (DML2) results in genome-wide DNA hypermethylation and impaired ripening. We report here that the transcription factors Ripening Inhibitor (RIN) and FRUITFULL 1 (FUL1) play critical roles in mediating the effect of DNA methylation on tomato fruit ripening. RIN and FUL1 are silenced in dml2 mutant plants, and the defective ripening phenotype of dml2 is mimicked by the rin/ful1 double mutant. Restoration of RIN expression in dml2 partially rescues its ripening defects. DNA methylation controls ripening not only by regulating the expression of RIN and FUL1 but also by interfering with the genomic binding of RIN. In dml2 mutant plants, RIN cannot bind to some of its targets in vivo even though DNA methylation does not interfere with RIN binding in vitro; this inhibited binding in vivo is correlated with increased DNA methylation and histone H3 enrichment within 100 bp of the binding site. Our work uncovers the molecular mechanisms underlying DNA methylation control of fruit ripening in tomato.

See https://pubmed.ncbi.nlm.nih.gov/40203043/

Figure 1:

RIN and FUL1 function redundantly downstream of DML2 in the control of tomato fruit ripening. (A) Phenotypes of tomato fruits of AC (the WT), and of rin, ful1, rin/ful1, nor, and dml2 mutants at 17, 25, 34, 38, 45, and 52 dpa. (Scale bar: 2 cm.) (B) Heatmap showing transcript profiles of RIN and FUL1 in AC and dml2-3 fruits. Transcriptome data of AC and dml2-3 fruits at 25 dpa and 34 dpa were used. (C) RT-qPCR analysis of RIN and FUL1 transcript levels in AC and dml2-3 fruits at 25 dpa and 34 dpa. Values are means ± SD. One-tailed Student’s t test was used to determine significance, ***P < 0.001. (D) Methylation levels of promoters of RIN and FUL1 in AC and dml2-3 fruits at 25 dpa and 34 dpa. Bisulfite sequencing data (Bs-seq) were displayed using Integrative Genome Browser software (IGB), where each vertical bar represents an mC, and the height of the bar indicates the methylation level.