A chromosome-level genome assembly of Platycladus orientalis and comparative genomics reveal pivotal roles of transposable elements in gene duplication and pseudogenization across gymnosperm giga-genomes

Gymnosperms, particularly conifers, exhibit a high abundance of transposable elements (TEs) in their giga-scale genomes. TEs interact antagonistically and cooperatively with the host genome, promoting structural and genetic innovations across evolutionary lineages. How TEs are involved in shaping the coding space of gymnosperm genomes is one remaining key question. Herein, we generate the high-quality genome assembly for a keystone conifer, Platycladus orientalis, with a contig N50 of 57.54 Mb (the highest continuity currently available) to investigate the role of TEs. Comparative genomics affirms the absence of recent whole-genome duplication and the presence of genome expansion in gymnosperms, revealing the complex interactions among recurrent TE proliferation, low removal rate, and DNA methylation silencing. Computationally detectable TE-mediated gene duplication and pseudogenization provide the genetic basis for adaptive evolution and functional innovation, significantly shaping gene family dynamics and the emergence of species-specific genes. Additionally, TEs capture and duplicate an average of 400,000 coding gene fragments per gymnosperm genome, facilitating exon shuffling and triggering epigenetic conflicts between source genes and captive exon fragments. Genes from which the fragment has been captured (donor genes) show significantly higher levels of exon methylation compared to genes without the capture by TEs (free genes), while syntenic donor genes exhibit lower levels of silencing response than non-syntenic donor genes. This study provides important genomic resources and offers insights into the evolutionary patterns and principles underlying the giant size and complexity of gymnosperm genomes.