Programmed cortical ER collapse drives selective ER degradation and inheritance in yeast meiosis.

George Maxwell Otto,Tia Cheunkarndee,Gloria Ann Brar,Jessica Mae Leslie

doi:10.1083/jcb.202108105

George Maxwell Otto, Tia Cheunkarndee + Show 2 more

Open Access

https://doi.org/10.1083/jcb.202108105

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Abstract

The endoplasmic reticulum (ER) carries out essential and conserved cellular functions, which depend on the maintenance of its structure and subcellular distribution. Here, we report developmentally regulated changes in ER morphology and composition during budding yeast meiosis, a conserved differentiation program that gives rise to gametes. A subset of the cortical ER collapses away from the plasma membrane at anaphase II, thus separating into a spatially distinct compartment. This programmed collapse depends on the transcription factor Ndt80, conserved ER membrane structuring proteins Lnp1 and reticulons, and the actin cytoskeleton. A subset of ER is retained at the mother cell plasma membrane and excluded from gamete cells via the action of ER-plasma membrane tethering proteins. ER remodeling is coupled to ER degradation by selective autophagy, which relies on ER collapse and is regulated by timed expression of the autophagy receptor Atg40. Thus, developmentally programmed changes in ER morphology determine the selective degradation or inheritance of ER subdomains by gametes.

Highlights

The expressing GFP-HDEL (ER) is a membrane-bound organelle that carries out a range of essential and conserved cellular functions, including protein synthesis and trafficking, lipid metabolism, and interorganelle communication
Premeiotic cells displayed ER morphology that is characteristic of mitotic cells, with ER distributed around the cell periphery and the nucleus
This remodeling occurs in a stepwise manner, beginning early in meiosis with cortical ER cabling and ER-plasma membrane (PM) tether clustering

Summary

Introduction

The ER is a membrane-bound organelle that carries out a range of essential and conserved cellular functions, including protein synthesis and trafficking, lipid metabolism, and interorganelle communication. These functions rely on the maintenance of ER structure and subcellular distribution, which are achieved through membrane-shaping proteins, fusion and fission of ER tubules, and tethering between the ER and other cellular structures, including organelles and the plasma membrane (PM; reviewed in Westrate et al, 2015; Schwarz and Blower 2016). Cells lacking these tethers have dramatically reduced cortical ER, disrupted lipid homeostasis, and acute sensitivity to ER stress, underscoring the importance of membrane tethering in maintaining ER structure and function. While factors that define ER structure are conserved across eukaryotes, we are only beginning to understand the diverse ways in which ER morphology and dynamics promote ER function

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