Genome-wide characterization and comparative transcriptomics unravel CpMADS47 as a positive regulator during fruit ripening and softening in Chinese cherry

Chinese cherry [Cerasus pseudocerasus (Lindl.) G.Don] (syn. Prunus pseudocerasus Lindl.) is an economically important fruit crop native to China. The fruits are prone to softening and rotting after harvest, which significantly limits their marketability and hinders its rapid development throughout China. The MADS-box gene family, particularly the SEP subfamily, plays a crucial role in governing fruit ripening and softening. However, the molecular mechanisms underlying fruit ripening and softening in Chinese cherry remains unclear. Herein, we identified 92 MADS genes from the Chinese cherry genome and analyzed their physicochemical characteristics, chromosomal localization, phylogeny, gene structures, covariance, and cis-acting elements. Many cis-elements in the promoters of CpMADSs are implicated in fruit development, ripening and stress response. Using comparative transcriptomics and RT-qPCR analysis, we identified a key gene, CpMADS47, as a positive regulator of cherry fruit ripening. CpMADS47 is localized in both the nucleus and cell membrane and shows highly expression in flowers and mature fruits. Transient overexpression of CpMADS47 in cherry fruit demonstrated its role in mediating fruit ripening and softening by promoting reduction in fruit firmness, anthocyanin accumulation, depolymerization of cell wall components, enhancement of cell wall degradation enzyme activity, and ABA biosynthesis. Conversely, silencing CpMADS47 generated the opposite effect. Yeast one-hybrid and dual-luciferase assays revealed that the CpMADS47 targets the promoters of cell wall degrading genes (CpPME3 and CpXTH31) and ABA signal transduction genes (CpPP2C12), thereby activating their transcription and promoting cherry fruit ripening. In summary, this study enriches our understanding of the transcriptional regulation of fruit ripening and softening in Chinese cherry.