Episodic and Ongoing Mechanisms Drive Plastid-Derived Nuclear DNA Evolution in Angiosperms

NUPTs are DNA sequences of plastid origin that are present in plant nuclear genomes in varying, though typically low, amounts. It is assumed that they are continuously formed and, due to their potentially mutagenic effect, they are removed at a constant turnover rate, which should result in an exponential decay of their age distributions and a negative correlation between age and size. However, these assumptions are based on analyses from a limited number of species and have never been explicitly tested. To gain insight into the mechanisms driving the origin and evolution of NUPTs, here we surveyed the plastid and nuclear genomes of 30 species representing the main angiosperm (flowering plants) lineages. By modeling the distribution of ages and sizes, examining their linear arrangement across the plastid genome, and statistically assessing spatial biases with respect to other genomic features, we showed that NUPTs are: (i) formed by both continuous and episodic mechanisms; (ii) unevenly represented across the plastid genome; (iii) consistently associated with certain classes of RNA genes, in particular rRNA, tRNA, and regulatory RNA genes; (iv) differentially contributing to structural genes; and (v) closer than expected to different superfamilies of transposons in a species-specific manner. Our results reveal the unexpected complexity in the mechanisms driving the origin of NUPTs, which not only involve their continuous formation but also episodic events, highlight their role as a major source of noncoding RNA genes and other genomic features, and provide a more complete picture of the different drivers of evolutionary change at the genome level.