Coordination of the endoplasmic reticulum stress response and lipid metabolism in plants

Abstract

The endoplasmic reticulum (ER) stress response is an important signal transduction pathway that senses ER stress caused by misfolded proteins or increased secretory protein traffic and induces molecular chaperone expression to counter such stress. The response has been well characterized in yeast and mammals where it has been associated with a variety of metabolic pathways, such as phospholipid biosynthesis, translational inhibition, and ER associated degradation. In plants, however, the connections of the ER stress response with metabolic pathways other than those involved in chaperone biosynthesis have not been characterized. This study defines a connection between phospholipid synthesis and the ER stress response in plants. Two model systems were used to characterize this association, the maize mutant floury-2 (fl2), which displays a unique endosperm specific ER stress response mediated by a mutant seed storage protein, and soybean cell cultures treated with the pharmacological agents tunicamycin (Tm) or azetidine-2-carboxylic acid (AZC). These chemicals interfere with normal protein synthesis and processing events, and are well characterized inducers of ER stress responses in animals, plants, and yeast. Investigation of both of these systems revealed a common theme; induction of the ER stress response in plants leads to increased activity and/or expression of various phospholipid biosynthetic enzymes. These increases were correlated with previously described amplifications in expression of the molecular chaperones binding protein (BiP), protein disulfide isomerase (PDI) and calreticulin. Certain aspects of the ER stress response may be unique to plants. A seed-specific result of the ER stress response was the accumulation of triacylglycerols (TG), which specifically increased in the endosperm of the fl2 mutant to more than 3-fold higher than normal endosperm levels by 36 days after pollination (DAP). The maize and soybean systems used in this study provide a starting point for the investigation of other details of the ER stress response in plants and represent important tools for future efforts to define the components of the signaling pathway.