Unfolded protein-independent IRE1 activation contributes to multifaceted developmental processes in Arabidopsis

Mishiba, Kei‐ichiro; Iwata, Yuji; Mochizuki, Tomofumi; Matsumura, Atsushi; Nishioka, Nanami; Hirata, Rikako; Koizumi, Nozomu

doi:10.26508/lsa.201900459

Cited by 31 publications

(34 citation statements)

References 69 publications

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“…A. thaliana has three IRE1 genes, two full length genes, AtIRE1a and -b, discovered by Koizumi et al (2001), and a shorter version called AtIRE1c (Figure 4). Arabidopsis lyrata has four IRE1 genes, AlIRE1a, -b, -c and c-like (Mishiba et al, 2019). Surprisingly, there are three ZmIRE1 genes in maize (Zea mays B73)two full-length genes, which cannot be classified as either IRE1a or -b-like and a shorter one, which by virtue of its size suggests that it is IRE1c-like.…”

Section: Are Two Ire1s Better Than One?mentioning

confidence: 99%

“…IRE1c is largely limited to the Brassicas, is a smaller form that lacks the N-terminal lumenal or sensory domain and is expressed primarily in flowers (Winter et al, 2007;Figure 4). Reporter constructs involving the IRE1c promoter demonstrated that the gene is expressed in the anther and embryo (Mishiba et al, 2019) Moreno et al (2012) [Colour figure can be viewed at wileyonlinelibrary.com] for a long time, because single knockout mutations in IRE1c had no demonstrable phenotype. However, a role of IRE1c came to light when two groups created a triple ire1a/b/c mutant and reported that it was lethal, and when a heterozygous IRE1c mutation was created in conjunction with ire1a/ire1b (ire1a/ire1b/ire1c/+) it was found to be defective in male gametogenesis (Mishiba et al, 2019;Pu et al, 2019).…”

Section: The Weirdness Of Ire1cmentioning

confidence: 99%

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Evolution of the unfolded protein response in plants

Howell

2021

Plant Cell & Environment

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The unfolded protein response (UPR) in plants is elicited by endoplasmic reticulum stress, which can be brought about by adverse environmental conditions. The response is mediated by a conserved signalling network composed of two branchesone branch involving inositol requiring enzyme1-basic leucine zipper60 (IRE1-bZIP60) signalling pathway and another branch involving the membrane transcription factors, bZIP17 and À28. The UPR has been reported in Chlamydomonas reinhardtii, a unicellular green alga, which lacks some canonical UPR signalling components found in vascular plants, raising the question whether C. reinhardtii uses other means such as oxidative signalling or Regulated IRE1-Dependent Decay to activate the UPR. In vascular plants, IRE1 splices bZIP60 mRNA in response to endoplasmic reticulum stress by cutting at a site in the RNA that is highly conserved in structure and sequence. Monocots have a single IRE1 gene required for viability in rice, while dicots have two IRE1 genes, IRE1a and -b. Brassicas have a third IRE1 gene, IRE1c, which lacks a lumenal domain, but is required in combination with IRE1b for gametogenesis. Vascular and non-vascular plants upregulate a similar set of genes in response to endoplasmic reticulum stress despite differences in the complexity of their UPR signalling networks.

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Section: Are Two Ire1s Better Than One?mentioning

confidence: 99%

Section: The Weirdness Of Ire1cmentioning

confidence: 99%

Evolution of the unfolded protein response in plants

Howell

2021

Plant Cell & Environment

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“…While this manuscript was under revision, complementary work on the characterization of IRE1C was published (Mishiba et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis

Ruberti

Angelos

et al. 2019

Plant Direct

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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.

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“…Secondly, an EMS-based genetic screen identified a plastidial stearoyl-acyl carrier protein desaturase, responsible for the conversion of stearic acid (18:0) into oleic acid (18:1), as an upstream regulator of UPR [ 246 ]. Thirdly, glycerol application to seedlings, that was shown to augment steady-state levels of saturated lipids, was able to induce RIDD, but bZIP60 splicing, in ire1 double mutant background engineered for expressing a luminal domain-deleted IRE1B protein [ 247 ]. Therefore, it is likely that lipo-toxic ER stress could actuate a protective RIDD response in Arabidopsis.…”

Section: Autophagy Rewires Cellular Activities To Mediate Plant Adaptation To Stress: the Complex Relationship Between Autophagy And Lipimentioning

confidence: 99%

How Lipids Contribute to Autophagosome Biogenesis, a Critical Process in Plant Responses to Stresses

Gomez

Lupette

Chambaud

et al. 2021

Cells

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Throughout their life cycle, plants face a tremendous number of environmental and developmental stresses. To respond to these different constraints, they have developed a set of refined intracellular systems including autophagy. This pathway, highly conserved among eukaryotes, is induced by a wide range of biotic and abiotic stresses upon which it mediates the degradation and recycling of cytoplasmic material. Central to autophagy is the formation of highly specialized double membrane vesicles called autophagosomes which select, engulf, and traffic cargo to the lytic vacuole for degradation. The biogenesis of these structures requires a series of membrane remodeling events during which both the quantity and quality of lipids are critical to sustain autophagy activity. This review highlights our knowledge, and raises current questions, regarding the mechanism of autophagy, and its induction and regulation upon environmental stresses with a particular focus on the fundamental contribution of lipids. How autophagy regulates metabolism and the recycling of resources, including lipids, to promote plant acclimation and resistance to stresses is further discussed.

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Unfolded protein-independent IRE1 activation contributes to multifaceted developmental processes in Arabidopsis

Abstract: The Arabidopsis unfolded protein response transducer IRE1 contributes to male gametophyte development using an alternative activation mechanism bypassing the unfolded protein-sensing domain.

Cited by 31 publications

References 69 publications

Evolution of the unfolded protein response in plants

Evolution of the unfolded protein response in plants

AtIRE1C, an unconventional isoform of the UPR master regulator AtIRE1, is functionally associated with AtIRE1B in Arabidopsis gametogenesis

How Lipids Contribute to Autophagosome Biogenesis, a Critical Process in Plant Responses to Stresses

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