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

Abstract 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.