A Functional Unfolded Protein Response Is Required for Normal Vegetative Development

Bao, Yan; Bassham, Diane C.; Howell, Stephen H.

doi:10.1104/pp.18.01261

Cited by 36 publications

(49 citation statements)

References 38 publications

(51 reference statements)

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“…Upon TM treatment, the atire1a atire1b double mutant showed over‐sensitivity phenotype compared with atire1a or atire1b single mutants and WT (Deng et al ), showing that the AtIre1 pathway is essential for UPR in Arabidopsis under extreme conditions. In addition, Yan et al (2019) reported that knockout of bZip17 has profound effects on vegetative development in the atire1a atire1b atbzip17 triple mutant background under normal condition (Bao et al ), revealing the UPR not only participates in development of Arabidopsis at a low active level under normal condition but is also highly regulated upon ER stress. Thus, UPR pathways are essential for plant reproductive and vegetative growth.…”

Section: Discussionmentioning

confidence: 99%

AtSec62 is critical for plant development and is involved in ER‐phagy in Arabidopsis thaliana

Hao

Cui

et al. 2019

JIPB

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The endoplasmic reticulum (ER) is the major site for protein folding in eukaryotic cells. ER homeostasis is essential for the development of an organism, whereby the unfolded protein response (UPR) within the ER is precisely regulated. ER‐phagy is a newly identified selective autophagic pathway for removal of misfolded or unfolded proteins within the ER in mammalian cells. Sec62, a component of the translocon complex, was recently characterized as an ER‐phagy receptor during the ER stress recovery phase in mammals. In this study, we demonstrated that the Arabidopsis Sec62 (AtSec62) is required for plant development and might function as an ER‐phagy receptor in plants. We showed that AtSec62 is an ER‐localized membrane protein with three transmembrane domains (TMDs) with its C‐terminus facing to the ER lumen. AtSec62 is required for plant development because atsec62 mutants display impaired vegetative growth, abnormal pollen and decreased fertility. atsec62 mutants are sensitive towards tunicamycin (TM)‐induced ER stress, whereas overexpression of AtSec62 subsequently enhances stress tolerance during the ER stress recovery phase. Moreover, YFP‐AtSec62 colocalizes with the autophagosome marker mCh‐Atg8e in ring‐like structures upon ER stress induction. Taken together, these data provide evidence for the pivotal roles of AtSec62 in plant development and ER‐phagy.

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Section: Discussionmentioning

confidence: 99%

AtSec62 is critical for plant development and is involved in ER‐phagy in Arabidopsis thaliana

Hao

Cui

et al. 2019

JIPB

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“…Studies in animals and plants have shown that IRE1 executes essential functions in physiological growth (Bao, Bassham, & Howell, ; Chen & Brandizzi, ; Coelho & Domingos, ; Deng et al, ). The knockout alleles of the mammalian Ire1α , the Arabidopsis IRE1B, and the rice OsIRE1 are lethal in standard conditions of growth.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, we found that the ire1b mutant has root elongation defects in recovery from temporary ER stress, suggesting that IRE1B is prominent in root growth in conditions of temporary ER stress recovery. Studies in animals and plants have shown that IRE1 executes essential functions in physiological growth (Bao, Bassham, & Howell, 2019;Chen & Brandizzi, 2013;Coelho & Domingos, 2014;Deng et al, 2016). The knockout alleles of the mammalian Ire1α, the Arabidopsis IRE1B, and the rice OsIRE1 are lethal in standard conditions of growth.…”

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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“…It is interesting to note that TabZIP74 knockdown seedlings developed fewer lateral roots, while other studies have found that IRE1a and IRE1b support root growth in ways other than the splicing of bZIP60 mRNA (Deng et al, 2016). The growth of single or double bZIP60 mutants in combination with either bZIP17 or bZIP28 appear to be normal in unstressed conditions (Kim et al, 2018;Bao et al, 2019). Biotic stress, ER stress-inducing agent, ABA treatment, and drought could induce TabZIP74 mRNA splicing.…”

Section: Tabzip74 Involved In Wheat Drought Tolerance and Developmentmentioning

confidence: 92%

“…The ER stress triggers cytoprotective signaling pathways, titled the unfold protein response (UPR), this signaling pathway restores and maintains ER homeostasis. There is growing recognition that ER stress responses are involved in normal plant development (Deng et al, 2016;Kim et al, 2018;Bao et al, 2019); for example, ER stress is involved in the cells synthesizing and secreting materials comprising the pollen coat (Deng et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

TabZIP74 Acts as a Positive Regulator in Wheat Stripe Rust Resistance and Involves Root Development by mRNA Splicing

FengTao

Lin

et al. 2019

Front. Plant Sci.

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Basic leucine zipper (bZIP) membrane-bound transcription factors (MTFs) play important roles in regulating plant growth and development, abiotic stress responses, and disease resistance. Most bZIP MTFs are key components of signaling pathways in endoplasmic reticulum (ER) stress responses. In this study, a full-length cDNA sequence encoding bZIP MTF, designated TabZIP74, was isolated from a cDNA library of wheat near-isogenic lines of Taichung29*6/Yr10 inoculated with an incompatible race CYR32 of Puccinia striiformis f. sp. tritici (Pst). Phylogenic analysis showed that TabZIP74 is highly homologous to ZmbZIP60 in maize and OsbZIP74 in rice. The mRNA of TabZIP74 was predicted to form a secondary structure with two kissing hairpin loops that could be spliced, causing an open reading frame shift immediately before the hydrophobic region to produce a new TabZIP74 protein without the transmembrane domain. Pst infection and the abiotic polyethylene glycol (PEG) and abscisic acid (ABA) treatments lead to TabZIP74 mRNA splicing in wheat seedling leaves, while both spliced and unspliced forms in roots were detected. In the confocal microscopic examination, TabZIP74 is mobilized in the nucleus from the membrane of tobacco epidermal cells in response to wounding. Knocking down TabZIP74 with barley stripe mosaic virus-induced gene silencing (BSMV-VIGS) enhanced wheat seedling susceptibility to stripe rust and decreased drought tolerance and lateral roots of silenced plants. These findings demonstrate that TabZIP74 mRNA is induced to splice when stressed by biotic and abiotic factors, acts as a critically positive regulator for wheat stripe rust resistance and drought tolerance, and is necessary for lateral root development.

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A Functional Unfolded Protein Response Is Required for Normal Vegetative Development

Cited by 36 publications

References 38 publications

AtSec62 is critical for plant development and is involved in ER‐phagy in Arabidopsis thaliana

AtSec62 is critical for plant development and is involved in ER‐phagy in Arabidopsis thaliana

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

TabZIP74 Acts as a Positive Regulator in Wheat Stripe Rust Resistance and Involves Root Development by mRNA Splicing

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