Solving the Insoluble: Regulation of α-Polyglucan Solubility and Functionality in Nature

Carbohydrate storage in the form of α-polyglucans plays essential roles in fitness and survival of organisms from all kingdoms of life. Optimal biological functionality of carbohydrate storage reserves in different cellular environments requires strict control of specific physicochemical and biochemical parameters, such as water solubility and susceptibility to hydrolytic and phosphorolytic digestion. This review focuses on the major storage α-polyglucans found in nature: glycogen, plant and floridean starches, and semi-amylopectin, and how each are modified in different cells to maximize efficient storage and access carbon reserves. We highlight the important role of branching to induce and maintain water solubility or insolubility. The tendency of proximal long linear α-1,4-linked chains to interact and form water-insoluble starch granules in plants and green algae (Archaeplastida) is through controlled formation and removal of specific α-1,6-branch linkages. Conversely, the stability of water-soluble glycogen particles is compromised when there is an imbalance between α-glucan elongation and branching activities, leading to excess long chains prone to insolubility. In Archaeplastida starches, α-glucan phosphate esters are thought to disrupt neighboring chains to prime granules for amylolytic degradation, whereas their role in glycogen metabolism remains an open question. We discuss current knowledge of the functional significance of these modifications to α-polyglucan architecture.