An evolutionary model for protein body formation in the endoplasmic reticulum of cereal endosperm cells

The seed storage proteins present in all plants accumulate in storage vacuoles. Prolamins, which are the major seed storage proteins in cereals and are present only in these plants, instead accumulate within the endoplasmic reticulum (ER) lumen as very large insoluble polymers held by disulfide bonds, termed protein bodies. The model prolamin gamma-zein of maize contains seven cysteine residues involved in interchain bonds. We show that progressive substitution of these amino acids with serine residues leads to similarly progressive increase in solubility and availability to traffic from the ER along the secretory pathway. Total substitution results in very efficient secretion, whereas the presence of a single cysteine is sufficient to promote partial sorting to the vacuole via a pathway that is sensitive to brefeldin A and wortmannin, similarly to the normal traffic pathway of vacuolar storage proteins. We propose that the mechanism leading to accumulation of prolamins in the ER is a further evolutionary step of the one responsible for accumulation in storage vacuoles. Supported by the FILAGRO Project of CNR-Regione Lombardia