Post‐transfer adaptation of HGT‐acquired genes and contribution to guanine metabolic diversification in land plants

Summary Horizontal gene transfer (HGT) is a major driving force in the evolution of prokaryotic and eukaryotic genomes. Despite recent advances in distribution and ecological importance, the extensive pattern, especially in seed plants, and post‐transfer adaptation of HGT‐acquired genes in land plants remain elusive. We systematically identified 1150 foreign genes in 522 land plant genomes that were likely acquired via at least 322 distinct transfers from nonplant donors and confirmed that recent HGT events were unevenly distributed between seedless and seed plants. HGT‐acquired genes evolved to be more similar to native genes in terms of average intron length due to intron gains, and HGT‐acquired genes containing introns exhibited higher expression levels than those lacking introns, suggesting that intron gains may be involved in the post‐transfer adaptation of HGT in land plants. Functional validation of bacteria‐derived gene GuaD in mosses and gymnosperms revealed that the invasion of foreign genes introduced a novel bypass of guanine degradation and resulted in the loss of native pathway genes in some gymnosperms, eventually shaping three major types of guanine metabolism in land plants. We conclude that HGT has played a critical role in land plant evolution.