Transition from glycogen to starch metabolism in Archaeplastida

•Starch evolved from glycogen in the host cytosol after plastid endosymbiosis.•A chlamydial debranching enzyme was recruited for crystalline polysaccharide synthesis.•A GWD evolved to enable mobilization of amylopectin crystals.•The novel dikinase step built on preexisting glycogen phosphorylation in eukaryotes.•The dikinases coupled starch catabolism to cyanobacterial carbon supply.•Transition from glycogen to starch maximized cytosolic carbon-sink strength.

In this opinion article we propose a scenario detailing how two crucial components have evolved simultaneously to ensure the transition of glycogen to starch in the cytosol of the Archaeplastida last common ancestor: (i) the recruitment of an enzyme from intracellular Chlamydiae pathogens to facilitate crystallization of α-glucan chains; and (ii) the evolution of novel types of polysaccharide (de)phosphorylating enzymes from preexisting glycogen (de)phosphorylation host pathways to allow the turnover of such crystals. We speculate that the transition to starch benefitted Archaeplastida in three ways: more carbon could be packed into osmotically inert material; the host could resume control of carbon assimilation from the chlamydial pathogen that triggered plastid endosymbiosis; and cyanobacterial photosynthate export could be integrated in the emerging Archaeplastida.