The transglutaminase (TGMs) family plays a crucial role in regulating mammalian reproduction, yet its impact on poultry reproductive traits has not been extensively studied. In this study, we identified eight members of the TGMs family in chickens and examined the contributions of genetic variations of coagulation factor XIII A chain (F13A1), transglutaminase 4 (TGM4), and LOC101749664 to selective breeding in commercial layers through genetic variation response pattern analysis. Transcriptome data from various tissues of high- and low-egg-yielding Gushi chickens revealed significant positive correlations between the mRNA expression levels of TGM4 and F13A1 genes and egg production (P < 0.05). Genotype-phenotype correlation analysis showed that 26 single nucleotide polymorphisms (SNPs) within genomic sequences of TGM4 and F13A1 genes exhibited significant associations with egg production traits across different laying periods. Additionally, spatiotemporal expression patterns of TGM4 in ovarian follicles between high- and low-laying chicken breeds determined by RT-qPCR highlighted the pivotal role of TGM4 in follicle development. Functionally, the gain-of-function assay demonstrated that TGM4 promoted granulosa cell proliferation, inhibited apoptosis, and enhanced progesterone synthesis. In conclusion, this is the first study to elucidate the role of the TGMs gene family in regulating egg production in chickens, offering new insights for the selective breeding of layers with improved egg-laying traits.
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