Epigenetic regulation of fruit shape determination by JAGGED gene in Capsella rubella

Fruits that protect the seeds and aid their dispersal are a key feature distinguishing angiosperms from other land plants, and fruit shape varies widely between species. However, it remains largely unknown how local growth behaviors are coordinated during development to generate fruits with characteristic sizes and shapes. Members of the Capsella genus in the mustard family produce unique fruits with an evolutionarily derived heart shape, making it an exceptional system suited for addressing this question. In this study, we demonstrate that the Capsella rubella C2H2-zinc finger transcription factor JAGGED (CrJAG) controls fruit shape. Whole-mount live imaging analysis indicates that CrJAG regulates valve development by promoting both cell division and anisotropic growth. Ectopic expansion of the valve epidermal cells in Crjag mutants is accompanied by mis-patterned endoreduplication events. CrJAG physically interacts with the histone chaperones Capsella rubella MULTICOPY SUPPRESSOR OF IRA1 members, increasing the chromatin accessibility and thereby sustaining the expression of genes involved in fruit morphogenesis. The resulting closed chromatin state in Crjag fruits is characterized by a reduction of the active histone marker (H3K18ac) and an increase of the repressive marker (H3K27me3). Expression analyses and pharmacological treatments indicate that the developmental defects in Crjag fruits are largely attributable to down-regulation of the key cell-cycle regulator CrAUR2 . Collectively, our findings suggest that fine-tuning the cell cycle via epigenetic modification represents an additional, essential layer of regulation critical to organ development.