Subcellular Enrichment Patterns of New Genes in <i>Drosophila</i> Evolution

The evolutionary patterns of proteins within subcellular compartments underlie the innovation and diversification foundation of the living eukaryotic organism. The location of proteins in subcellular compartments promotes the formation of network interaction modules, which in turn reshape the architecture of higher-level protein-protein interaction networks. Here, we conducted the most up-to-date gene age dating of Drosophila melanogaster by employing recently available long-read sequencing genomes as references. We found that an elevated gene fixation in the most recent common ancestor of Drosophila genus predated the divergence between two Drosophila subgenera, and a significant tendency of these genes in D. melanogaster encode proteins that localize to the extracellular matrix, accompanying the adaptive radiation of Drosophila species. Proteins encoded by genes located in the extracellular space exhibit higher sequence divergence, suggesting a rapid evolutionary process. We also observed that proteins encoded by genes originating from the same evolutionary branches tend to co-localize in the same subcellular compartments, and proteins in the same subcellular compartment tend to interact with each other. The proteins encoded by genes that have persisted through deeper branches exhibit broader localization across multiple subcellular compartments, enhancing the likelihood of their integration into various protein or gene regulatory networks, thereby increasing functional diversity. These evolutionary patterns not only contribute to understanding the evolution of subcellular localization in proteins encoded by genes originating from different branches, but also provide insights into the evolution of protein-protein networks driven by the emergence of new genes.