Ire1 supports normal ER differentiation in developing Drosophila photoreceptors

Abstract

The endoplasmic reticulum (ER) serves virtually all aspects of cell physiology and, by pathways incompletely understood, is dynamically remodeled to meet changing cell needs. Inositol-requiring enzyme 1 (Ire1), a conserved core of the Unfolded Protein Response (UPR), participates in ER remodeling and is particularly required during the differentiation of cells devoted to intense secretory activity, “professional” secretory cells. Here, we characterize Ire1's role in ER differentiation in developing Drosophila compound eye photoreceptors (R cells). As part of normal development, R cells take a turn as professional secretory cells with a massive secretory effort that builds the photosensitive membrane organelle, the rhabdomere. We find rough ER sheets proliferate as rhabdomere biogenesis culminates and Ire1 is required for normal ER differentiation. Ire1 is active early in R cell development and is required in anticipation of peak biosynthesis. Without Ire1, rough ER sheets are strongly reduced and the extensive cortical ER network at the rhabdomere base, the subrhabdomere cisterna (SRC), fails. Instead, ER proliferates in persistent, ribosome-poor tubular tangles. A phase of Ire1 activity early in R cell development thus shapes dynamic ER.