MADS-box genes play important roles in plant development, especially flowering and fruiting. In this study, we identified 54 type I and 69 type II MADS-box genes from the apple reference genome 'GDDH13'. The type II MADS-box genes were further divided into 12 closely related subgroups, each exhibiting similar gene structures and conserved domains. Among these, two genes, MADS35 and MADS5, belonging to APETALA1 (AP1) subfamily, were found to be predominantly expressed in apple fruit. To explore their functions, transgenic apple plants with altered expression of these genes were produced. Overexpression of MADS35 induced early flowering, while overexpression of MADS5 induced both early flowering and parthenocarpy. Transcriptome analysis suggested that the parthenocarpy observed in the transgenic apple plants might be associated with changes of gene expression within the auxin, GA, ABA, and ethylene signaling pathways. MADS5 and MADS35, although paralogs, differ by one amino acid in the MADS-domain and six amino acids in the K-domain, which could account for their function diversity in regulating apple fruiting. In summary, the present study provides a comprehensive analysis of MADS-box genes in apple and lays the foundation for future efforts to shorten the juvenile stage and enhance parthenocarpy-related traits in apple plants.
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