The monoplastidic bottleneck in algae and plant evolution

Abstract

Plant and algae plastids evolved from the endosymbiotic integration of a cyanobacterium by a heterotrophic eukaryote. A consequence of their ancestry is that new plastids can only emerge through fission and vital to organelle and host co-evolution was the early synchronization of bacterial division with the hosts eukaryotic cell cycle. Most of the sampled algae, including multicellular macroalgae, house a single plastid per cell -- or nucleus in case of coenocytic cells -- and basal branching relatives of polyplastidic lineages are all monoplastidic. The latter is also true regarding embryophytes, as some non-vascular plants are monoplastidic at least at some stage of their life cycle. Here we synthesize recent advances regarding plastid division and associated proteins, including those of the peptidoglycan wall biosynthesis, across the diversity of phototrophic eukaryotes. Through the comparison of the phenotype of 131 species harbouring plastids of primary or secondary origin, we uncover that one prerequisite for an algae or plant to house multiple plastids per nucleus appears the loss of the genes MinD and MinE from the plastid genome. Housing a single plastid whose division is coupled to host cytokinesis appears a prerequisite of plastid emergence; escaping that monoplastidic bottleneck succeeded rarely and appears tied to evolving a complex morphology. Considering how little we know about the mechanisms that guarantee proper organelle (and genome) inheritance raises the peculiar possibility that a quality control checkpoint of plastid transmission remains to be explored and which is tied to understanding the monoplastidic bottleneck.