Abstract
The unfolded protein response (UPR), a highly conserved set of eukaryotic intracellular signaling cascades, controls the homeostasis of the endoplasmic reticulum (ER) in normal physiological growth and situations causing accumulation of potentially toxic levels of misfolded proteins in the ER, a condition known as ER stress. During evolution, eukaryotic lineages have acquired multiple UPR effectors, which have increased the pliability of cytoprotective responses to physiological and environmental stresses. The ER‐associated protein kinase and ribonuclease IRE1 is a UPR effector that is conserved from yeast to metazoans and plants. IRE1 assumes dispensable roles in growth in yeast but it is essential in mammals and plants. The Arabidopsis genome encodes two isoforms of IRE1, IRE1A and IRE1B, whose protein functional domains are conserved across eukaryotes. Here, we describe the identification of a third Arabidopsis IRE1 isoform, IRE1C. This protein lacks the ER lumenal domain that has been implicated in sensing ER stress in the IRE1 isoforms known to date. Through functional analyses, we demonstrate that IRE1C is not essential in growth and stress responses when deleted from the genome singularly or in combination with an IRE1A knockout allele. However, we found that IRE1C exerts an essential role in gametogenesis when IRE1B is also depleted. Our results identify a novel, plant‐specific IRE1 isoform and highlight that at least the control of gametogenesis in Arabidopsis requires an unexpected functional coordination of IRE1C and IRE1B. More broadly, our findings support the existence of a functional form of IRE1 that is required for development despite the remarkable absence of a protein domain that is critical for the function of other known IRE1 isoforms.
Highlights
Environmental and physiological situations that increase the cell's secretory activity alter the homeostasis of protein synthesis in the endoplasmic reticulum (ER) and ignite a potentially lethal condition, known as ER stress
Inositol requiring enzyme-1 assumes roles that are independent from the gene-regulatory functions of the target unfolded protein response (UPR) basic leucine zipper (bZIP)-transcription factor (TF), as supported by the evidence that inositol requiring enzyme-1 (IRE1)-ribonuclease activity controls the selective degradation of cytosolic mRNA transcripts, via a process known as Regulated IRE1-Dependent Decay (RIDD) in yeast, metazoans, and plants (Hollien et al, 2009; Kimmig et al, 2012; Mishiba et al, 2013), possibly to reduce the secretory protein load in conditions of ER stress
Error bars refer to standard error values
Summary
Environmental and physiological situations that increase the cell's secretory activity alter the homeostasis of protein synthesis in the endoplasmic reticulum (ER) and ignite a potentially lethal condition, known as ER stress. Inositol requiring enzyme-1 assumes roles that are independent from the gene-regulatory functions of the target UPR bZIP-TF, as supported by the evidence that IRE1-ribonuclease activity controls the selective degradation of cytosolic mRNA transcripts, via a process known as Regulated IRE1-Dependent Decay (RIDD) in yeast, metazoans, and plants (Hollien et al, 2009; Kimmig et al, 2012; Mishiba et al, 2013), possibly to reduce the secretory protein load in conditions of ER stress. IRE1 is dispensable in Caenorhabditis elegans (Shen et al, 2001) but essential in Drosophila meloganaster (Plongthongkum, Kullawong, Panyim, & Tirasophon, 2007), similar to mammals and plants, supporting the hypothesis that while the enzymatic activity of the IRE1 isoforms is conserved across eukaryotes, the degree of relevance of the IRE1 signaling in growth varies greatly Such degree of functional relevance has possibly evolved to suit taxa-specific features during organismal development. Our results report on a unique IRE1 isoform in eukaryotes that contributes to the UPR and highlight a plant-specific innovation of UPR management in growth
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