A Pangenome Analysis of the RPD3/HDA1-Type Histone Deacetylase (HDAC) Family in Musaceae Unveils MaHDAC3 as an Epigenetic Repressor of Fruit Ripening.

Histone deacetylases (HDACs) are critical epigenetic modulators of fruit ripening. In plants, the RPD3/HDA1 subfamily is the most evolutionarily dynamic and functionally diverse group within the HDAC superfamily. To decipher how the RPD3/HDA1 subfamily coordinates fruit ripening, we conducted a pangenomic investigation of these members across 18 Musaceae genomes. A total of 199 RPD3/HDA1-type members were identified, with 20 representatives unveiling a distinct subcellular landscape. Evolutionary analyses revealed a dichotomy within the subfamily: Class-I expanded via multiple duplications, while Class-II remained constrained, shaped primarily by dispersed and whole-genome duplications. Transcriptional and functional screening identified MaHDAC3 as a ripening inhibitor, and its silencing triggered premature degreening and accelerated sugar/ROS accumulation. MaHDAC3 deficiency elevated global histone acetylation, derepressing rate-limiting genes and boosting glycolytic flux. Collectively, our study highlights the evolutionary plasticity of Musaceae RPD3/HDA1 HDACs and defines MaHDAC3 as an epigenetic brake on carbon metabolism, offering a promising target for extending fruit shelf life.