Genome-Wide Analysis of Eudicot Species Reveals Lower Duplicability and Higher Network Clustering among Nuclear Encoded Organelle-Related Genes

The mechanisms by which genome evolution drive organisms’ diversification remain elusive. Plant cells provide a particularly interesting model to study such mechanisms due to the coexistence of three genomes as a result of two endosymbiotic events leading to the acquisition of plastids and mitochondria, and the major and diverse roles of gene duplication in plant nuclear genomes. As a result from this genetic partitioning between organelle and nucleus, organelle related functions are encoded by a mosaic of nuclear and organelle genes, a scenario that may pose particular constraints on the evolution of organelle related functions. We examined the modes of evolution of nuclear-encoded plastid and mitochondrial gene families across five plant genomes. Our results reveal the preferential loss of organelle gene copies following duplication. Many nuclear-encoded organelle genes occur in single-gene families that are highly conserved across species, likely reflecting their involvement in essential plant biological processes. Furthermore, biological networks of organelle gene functions show distinctive features in terms of clustering. Our approach unravels the distinctive modes of evolution of nuclear-encoded plastid and mitochondrial genes and supports them as complex biological systems showing specific evolutionary constraints in terms of duplicability and network clustering, possibly due to i) the importance of their encoded functions among plant biological processes, ii) the required dosage balance of nuclear-encoded organelle functions, and iii) the occurrence of dominant-negative phenotypes.