Massive intracellular gene transfer during plastid genome reduction in nongreen Orobanchaceae

Summary Plastid genomes (plastomes) of nonphotosynthetic plants experience extensive gene losses and an acceleration of molecular evolutionary rates. Here, we inferred the mechanisms and timing of reductive genome evolution under relaxed selection in the broomrape family (Orobanchaceae). We analyzed the plastomes of several parasites with a major focus on the genus Orobanche using genome-descriptive and Bayesian phylogenetic-comparative methods. Besides this, we scanned the parasites’ other cellular genomes to trace the fate of all genes that were purged from their plastomes. Our analyses indicate that the first functional gene losses occurred within 10 Myr of the transition to obligate parasitism in Orobanchaceae, and that the physical plastome reduction proceeds by small deletions that accumulate over time. Evolutionary rate shifts coincide with the genomic reduction process in broomrapes, suggesting that the shift of selectional constraints away from photosynthesis to other molecular processes alters the plastid rate equilibrium. Most of the photosynthesis-related genes or fragments of genes lost from the plastomes of broomrapes have survived in their nuclear or mitochondrial genomes as the results of multiple intracellular transfers and subsequent fragmentation. Our findings indicate that nonessential DNA is eliminated much faster in the plastomes of nonphotosynthetic parasites than in their other cellular genomes.