Transposable element dynamics and regulatory role in sika deer (Cervus nippon) antler development.

Abstract

Background: Deer antlers represent one of the few mammalian organs capable of complete regeneration, yet the underlying genomic regulatory mechanisms remain incompletely understood. Transposable elements (TEs), as key drivers of genome evolution and gene regulation, may play pivotal roles in the evolution of complex traits. This study aimed to systematically investigate the evolutionary dynamics of TEs in sika deer genome and to elucidate their potential regulatory functions in the development of antler by integrating comparative and functional genomics approaches.

Results: Comparative genomics revealed a lineage-specific massive expansion of LINE retrotransposons (dominated by RTE-BovB and L1 subfamilies) in cervid genomes, particularly in sika deer and red deer, where they constitute over 29% of the genomic sequence. The peak of this expansion (~ 7.5 million years ago) coincides with the major cladogenesis events within Cervus. Expression analysis showed that approximately 8.88% of annotated TEs are transcriptionally active in antler mesenchyme, with LINE and LTR elements being predominant among the 1,191 TEs consistently highly expressed across all stages. We identified numerous stage-specifically expressed TEs (SETEs) and found positive correlations between SETEs and key antler development genes, such as the osteogenic master regulator RUNX2, the extracellular matrix remodeling gene ANPEP, and the collagen synthesis gene P4HA3. Enrichment analysis demonstrated that genes adjacent to these TEs are significantly involved in pathways crucial for regeneration and rapid growth, including Wnt signaling, Hippo signaling, regulation of the actin cytoskeleton, and protein digestion and absorption.

Conclusions: Our findings point to a potential role for cervid TEs expansion in driving genomic evolution and the acquisition of cervid-specific phenotypes, particularly antler growth and development. Through profiling TE expression in antler mesenchymal tissue across key development stages, the results suggest that dynamic TEs expression may be involved in the regulation of antler development, implicating a potential regulatory role for TEs in this rapid growth process. This study provides new insights into the molecular mechanisms underlying the rapid growth of antlers.