k-mer cross-species profiling reveals taxon-specific TE expansions accompanied by KZFP co-option and functional impacts in ruminants

Abstract

Transposable elements (TEs), which constitute approximately one-third of ruminant genomes, significantly influence genome evolution. However, the substantial sequence diversity across ruminant species complicates cross-species TE comparison and analysis of their interactions with Krüppel-associated box zinc finger proteins (KZFPs). Through a comprehensive analysis of 32 ruminant genomes, we identify taxon-specific expansions of KZFPs (approximately 271 per genome), which reflect established phylogenies. Among TEs, LINE/RTE-BovB dominates genomic content (55.7%), while LTR/ERVK subfamilies show significant taxon-specific variation. Our k-mer-based clustering approach effectively reconstructs ruminant phylogeny and reveals temporal patterns of TE expansion. Importantly, we uncover robust coevolutionary signatures between 90 KZFPs and specific TE k-mer clusters, notably involving 32 KZFPs that target Bovidae-specific LTR/ERVK clusters. Furthermore, Bovinae-specific TEs impact gene structure by exonizing 14 genes and generating tissue-enriched cis-regulatory elements (CREs), including 1,645 promoter- and enhancer-associated elements. This study establishes a robust computational framework for cross-species TE analysis and provides key insights into the coevolution of KZFPs and TEs, advancing our understanding of TE genomics and function in ruminants.