Easier Lost than Found? What We Know about Plastid Genome Reduction

Plastids are eukaryotic organelles that evolved from a photobiotic symbiont, imparting photosynthetic abilities to heterotrophic hosts. Plastids lose much of their complexity during the endosymbiont-to-organelle transition, reflecting the need of the symbiotic partners to synchronize reproduction and streamline metabolism. This is obvious from genome size reduction, and while the genomes of plastid predecessors, cyanobacteria, typically range 1.6–7.8 Mbp, most plastid genomes range 110–190 kbp. In some lineages, plastid genomes depart from convention, which manifests two-way. Whereas in rhodophytes, chlorophytes, plants, and euglenids this leads to the expansion of noncoding DNA, in dinoflagellates, the plastid genome is fragmented into single-gene minicircles, and in one chlorophyte lineage into linear single-stranded hairpin chromosomes. Yet, plastids may later enter the dark phase of their “life history.” Driven by competition, even established phototrophic organisms sometimes revert to heterotrophy or parasitism, leading to further impairment or complete loss of photosynthesis. Here, we recapitulate the history of plastids from early acquisition to their disappearance in nonphotosynthetic algae and plants. We compare how molecular functions encoded by plastids vary in diverse eukaryotic lineages that acquired them, and how they vary in lineages about to lose them. We highlight how genome reduction accompanies plastid life cycles and how evolutionary history shapes their ultimate future.