What is endoplasmic reticulum do

It was hypothesized that the mitochondrial stress somehow activates yet unknown proteases that proteolytically activate the two ER-anchored ANAC proteins that can subsequently translocate into the nucleus Wang et al.

It is also interesting to note that the two ANACs were recently implicated in coordinating mitochondrial and chloroplast functions via their physical interactions with a nuclear protein Radical-induced Cell Death1 RCD1 that was known to be regulated by ROS Shapiguzov et al.

The plasma membrane PM , a lipid bilayer embedded with proteins, is an essential cellular component for the plant stress tolerance. It not only serves as a physical barrier to shield cellular contents from the extracellular environment and controls the flux of solutes and macromolecules but also contains a wide range of sensors and receptors that perceive and transmit all kinds of environmental signals. The composition of EPCSs and their molecular functions have been well established in the yeast and mammalian cells in the last decade Stefan, SYT1 has been previously described as an essential component for maintaining the PM integrity, especially under conditions of high risks of membrane disruption such as osmotic shock, freezing, and salt stresses Schapire et al.

EPCSs are now widely accepted as important sites for the non-vesicular lipid transport, which appears to be the major transport route of certain lipid species Lev, Plants exposed to abiotic stresses have to adapt their membrane lipid composition and fluidity to changing environmental conditions by adjusting the relative amounts of various lipids, such as phospholipids and galactolipids Hou et al.

It is well known that lipids synthesized in the ER need to be delivered to other membranes for assembly of biological membranes or for lipid-mediated signaling cascades.

It is proposed that the lipid transfer proteins LTPs are localized at the EPCSs and function as dynamic tethers between the two membranes with their lipid transfer module regulating lipid exchange Dickson et al. Mammalian VAPs are known to interact with proteins involved in lipid transfer Gatta et al. It is likely that the plant EPCSs are also involved in the ER-PM lipid transfer and thus play important role in plant stress tolerance by modulating the composition and fluidity of the PM.

The space between the PD-PM and the desmotubule constitutes the actual channel the cytoplasmic sleeve that transports a wide range of molecular cargos across cell walls of neighboring cells Tilsner et al. Given the key role of PD in generating cytosolic and membrane continuity that are essential for growth and development, stress tolerance, and plant defense, the permeability of PD also known as size exclusion limit , governed by the size of the cytoplasmic sleeve and distribution of spokes that creates nanochannels, is constantly regulated by various of developmental and environmental signals Sun et al.

Chloroplasts conduct photosynthesis and produce energy for plant growth, development, and defense. In addition, chloroplasts are essential for synthesizing certain amino acids, lipids, and fatty acids. Like mitochondrion, chloroplast is also a semiautonomous organelle with its own genome and a majority of chloroplast proteins are encoded by the nuclear genome and imported from the cytosol.

Accordingly, the plant cells execute anterograde and retrograde communications between the chloroplast and the nucleus to respond to changing environment Watson et al. Under stress conditions, ROS such as singlet oxygen and superoxide were generated from electron transport chain in the chloroplasts, which cause oxidative damage to the photosynthetic organelle. The chloroplast-nucleus signaling might also involve chloroplast-nucleus contact sites consisting of stromules, the stroma-filled tubular protrusions from the chloroplast outer membrane Figure 1 ; Kohler and Hanson, ; Hanson and Hines, , which facilitate translocations of chloroplast-sequestered transcription factors into the nucleus in response to various stresses Caplan et al.

The ER and chloroplasts are the two major sites of lipid biosynthesis van Meer et al. The ER-chloroplast-mediated lipid biosynthesis involving de novo synthesis of fatty acids FAs in chloroplasts, the chloroplast-ER transport of FAs, the ER-catalyzed assembly and modification of glycerolipids that move back to chloroplasts for producing galactolipids Benning and Ohta, , the major chloroplast lipids Dormann and Benning, Studies in recent years strongly suggest that the chloroplast-ER physical contact sites, better known as plastid-associated membranes [PLAMs, Andersson et al.

At least two groups of proteins were detected at the ER-chloroplast membrane contact sites Tan et al. The first group includes several members of the trigalactosyldiacylglycerol TGD protein family, which form a bacterial-type ABC transporter for transporting lipids from the ER to the thylakoid membrane Xu et al.

Various abiotic stresses, such as high light exposure and wounding, can lead to accumulation of MEcPP in chloroplasts, which serves as a retrograde signaling metabolite that relays the chloroplast stress signal into the nucleus to alter gene expression Xiao et al.

In addition, a loss-of-function mutation in an Arabidopsis gene encoding the chloroplast stearoyl-acyl carrier protein desaturase, which introduces double bonds into FAs, constitutively activates the expression of a known ER-UPR marker gene BIP3 Iwata et al.

Together, these findings provide additional support for the involvement of the photosynthetic organelle in regulating the ER homeostasis. In plants, peroxisomes also perform other important functions such as the glycolate cycle and photorespiration, secondary metabolism, hormone auxin and jasmonic acid biosynthesis, metabolism of ROS and reactive nitrogen species RNS Nyathi and Baker, ; Hu et al.

Notably, peroxisomes are highly dynamic organelles that alter their morphology, proliferation, and metabolic activities in response to environmental signals Honsho et al.

The membrane extensions of peroxisomes, termed as peroxules Figure 1 , are often observed when plants are exposed to exogenous H 2 O 2 or high-intensity light Sinclair et al. Salt stress, heavy metals, and herbicide application were known to increase the metabolic activity and proliferation rate of peroxisomes Palma et al. It has been well known that peroxisome dynamics such as elongation, fission, and degradation as well as metabolic changes require their constant collaborations and communications with other intracellular organelles Hu et al.

Although there is no clear evidence to support the ER budding model for the plant peroxisomes Mullen and Trelease, ; Trelease and Lingard, , the ER is at least involved in the plant peroxisome biogenesis by providing membranes, lipids, and certain peroxisome membrane proteins PMPs to preexisting or fission-created nascent peroxisomes Hu et al.

The plant peroxisomes were shown to be closely associated with the ER by early microscopic observation Huang et al. However, it remains unknown whether the observed ER-peroxisome contiguity in Arabidopsis is mediated by the peroxisome-ER physical tether that was first described in yeast.

The yeast peroxisome-ER tethering complex consists of a peroxisome biogenic protein, peroxin 3 PEX3 , localized on the ER and peroxisome, and the peroxisome inheritance factor Inp1 that serves as a bridge to link the ER and peroxisome-localized PEX3 Knoblach and Rachubinski, The PEX3-Inp1-PEX3 trimeric complex plays a key role in partitioning peroxisomes in dividing yeast cells and controlling the peroxisome population Knoblach et al.

Despite microscopic observations of the ER-peroxule association Sinclair et al. The chloroplast works together with mitochondria and peroxisomes in photorespiration involving inter-organellar metabolite exchanges while the chloroplast tubular extensions, stromules, are thought to interact with the ER, mitochondria, and peroxisomes Mathur et al.

Vacuoles are single-membrane-bound organelles that are filled with a wide range of inorganic ions and organic molecules Figure 1. In plants, at least two types of vacuoles have been identified, including protein storage vacuoles PSVs and lytic vacuoles LVs Paris et al. PSVs usually serve as a warehouse for seed storage proteins that are synthesized in the ER during seed maturation, while LVs occur in the vegetative tissues and contain acidic contents and degradative enzymes with lysosome-like properties Shimada et al.

It has been shown that the vacuoles play crucial roles in storage of nutrients and metabolites, detoxification, pH homeostasis, and stress tolerance Muntz, ; Viotti, Maintaining proper turgor pressure in vacuoles is required for morphological alterations of cells during plant development, and the rapid vacuolar uptake or unloading of various ions and metabolites allows plants to efficiently cope with environmental stresses.

It is well known that stomatal opening or closure is associated with vacuole morphology changes in guard cells, highlighting the important roles of vacuole in plant response to abiotic stresses, such as high temperature and drought Gao et al. Many vacuolar proteins and metabolites are synthesized and processed in the ER and transported to the vacuoles.

Recent studies indicated the presence of a direct Golgi-independent ER-vacuole trafficking route involving the machinery of autophagy Viotti et al. Under the ER stress, ER components bud from the ER and form autophagosome with the aid of appropriate cargo receptors, and the autophagosome subsequently fuses with the lytic vacuole to release the ER cargos for degradation via the classical macroautophagy pathway Liu et al.

A special process of autophagy, ER-phagy Schuck et al. Given the presence of a direct ER-vacuole trafficking route for transporting metabolites, proteins, and membranes in plant cells, it is quite possible that plant cells have multiple ER-vacuole contact sites that serve important cellular functions, especially when responding to environmental stresses.

The yeast NVJ is established by interaction between one of the two ER membrane proteins, Nvj1 and Ltc1 lipid transfer at contact site1 , and an armadillo repeat protein Vac8 that requires palmitoylation for its localization to the vacuolar membrane Pan et al.

Despite essential roles of the vacuoles in plant growth, stress tolerance, and plant defense Shimada et al. Given the widespread occurrence of SMP-containing proteins at multiple MCSs in yeast and mammalian cells Toulmay and Prinz, , identification of a plant ER-vacuole tethering complex might be facilitated by confocal microscopic examination of fluorescently tagged AtSYT1—5 followed by biochemical studies of an AtSYT localized at the ER-vacuole contact sites.

Accumulating evidence supports important roles of the ER-organelle interactions in plant stress tolerance, which involves exchanges of metabolites and signaling molecules at specialized MCSs with unique tethering complexes. Further studies that combine live cell imaging, proteomics, and plant genetics are needed to fully understand the composition and dynamic regulation of these MCSs in response to environmental changes and their additional physiological functions.

The open access publication fee is provided by a startup fund from South China Agricultural University. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

We would like to thank Fen Su for her help in generating the figure and the handling editor and two reviewers for their constructive criticisms and helpful suggestions. We apologize to those colleagues whose works were not fully cited in this article. Andersson, M. Optical manipulation reveals strong attracting forces at membrane contact sites between endoplasmic reticulum and chloroplasts. Anelli, T. Redox Signal.

Angelos, E. Plant J. Maintaining the factory: the roles of the unfolded protein response in cellular homeostasis in plants. Apse, M. Science , — Arimura, S. Fission and fusion of plant mitochondria, and genome maintenance. Plant Physiol. Bak, G. Rapid structural changes and acidification of guard cell vacuoles during stomatal closure require phosphatidylinositol 3,5-bisphosphate.

Plant Cell 25, — Bao, Y. Autophagy 14, — Barton, K. Simultaneous live-imaging of peroxisomes and the ER in plant cells suggests contiguity but no luminal continuity between the two organelles.

Benn, G. USA , — Benning, C. Three enzyme systems for galactoglycerolipid biosynthesis are coordinately regulated in plants. Bhandary, B. An involvement of oxidative stress in endoplasmic reticulum stress and its associated diseases. Birk, J. Endoplasmic reticulum: reduced and oxidized glutathione revisited. Cell Sci. Block, M. Lipid trafficking at endoplasmic reticulum-chloroplast membrane contact sites. Cell Biol. Brandizzi, F. Organization of the ER-Golgi interface for membrane traffic control.

Brillada, C. Vacuolar trafficking and biogenesis: a maturation in the field. Plant Biol. Caplan, J. Chloroplastic protein NRIP1 mediates innate immune receptor recognition of a viral effector.

Cell , — Carraretto, L. Calcium flux across plant mitochondrial membranes: possible molecular players. Plant Sci. Cecchini, N. Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Chan, K. Sensing and signaling of oxidative stress in chloroplasts by inactivation of the SAL1 phosphoadenosine phosphatase. USA , E—E Chung, W. Cell Calcium 63, 29— Costello, J. Cell Cycle 16, — Craxton, M. Synaptotagmin gene content of the sequenced genomes.

BMC Genomics Das, K. Dasilva, L. Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells.

Plant Cell 16, — Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature , — De Clercq, I. Del Rio, L. ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol. Deng, Y. Detmer, S. Functions and dysfunctions of mitochondrial dynamics. Dickson, E. Dynamic formation of ER-PM junctions presents a lipid phosphatase to regulate phosphoinositides. Ding, B. Substructure of freeze-substituted plasmodesmata.

Protoplasma , 28— Dojcinovic, D. Identification of a region of the Arabidopsis AtAOX1a promoter necessary for mitochondrial retrograde regulation of expression.

Plant Mol. Dormann, P. Galactolipids rule in seed plants. Trends Plant Sci. Duncan, O. Unique components of the plant mitochondrial protein import apparatus. Acta , — Dupree, P. The plant Golgi apparatus. Fahy, D. Impact of salt stress, cell death, and autophagy on peroxisomes: quantitative and morphological analyses using small fluorescent probe N-BODIPY. Fan, J. Plant Cell 27, — Foyer, C. Fujita, M. Gao, H. A membrane-tethered transcription factor defines a branch of the heat stress response in Arabidopsis thaliana.

Gao, X. The dynamic changes of tonoplasts in guard cells are important for stomatal movement in Vicia faba. Gatta, A. Giordano, F. Grison, M. Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Hanson, M. Stromules: probing formation and function. Hariri, H. Lipid droplet biogenesis is spatially coordinated at ER-vacuole contacts under nutritional stress.

EMBO Rep. Hawes, C. The plant ER-Golgi interface. Traffic 9, — Heilmann, I. Towards understanding the function of stress-inducible PtdIns 4,5 P 2 in plants. Hetz, C. Notably, processing of secreted proteins can considerably elevate under stress conditions and exceed ER folding capacities. The resulting accumulation of unfolded proteins is defined as ER stress.

The efficiency of cells to re-establish proper ER function is crucial for stress adaptation. Besides delivering proteins directly antagonizing and resolving stress conditions, the ER monitors synthesis of immune receptors.

This indicates the significance of the ER for the establishment and function of the plant immune system. Recent studies point out the fragility of the entire system and highlight the ER as initiator of programed cell death PCD in plants as was reported for vertebrates.

Understanding the integration of stress signals by the ER bears a considerable potential to optimize development and to enhance stress resistance of plants. The endoplasmic reticulum ER is an organelle with important functions in eukaryotic cells.

It connects to other cellular compartments [e. It is further involved in lipid and hormone biosynthesis Staehelin, ; Sparkes et al.

ER integrity is central to proper function of cells and whole organisms. Especially under stress conditions, any impairment of ER function can result in disturbed plant development and plant immunity Wang et al.

Protein folding demand and capacities in the ER are usually in equilibrium. However, responses to environmental stresses create an increased requirement for secreted proteins.

Prolonged ER stress impairs ER function and thus threatens cellular integrity. Under non-stressed conditions, luminal parts of these ER stress sensors bind to luminal binding proteins BiPs , which keeps the sensors in an inactive state. If unfolded proteins accumulate, BiPs disconnect from ER stress sensors to mediate processing of unfolded proteins.

Once liberated, ER stress sensors initiate different adaptive signaling cascades defined as unfolded protein response UPR to re-establish proper ER function. Upon BiP release, IRE1 oligomerizes and activates its endoribonuclease domain, leading to the unconventional splicing of a 26 nucleotide intron out of XBP1 or its yeast counterpart HAC1 , which allows the resulting proteins to enter the nucleus Mori, ; Walter and Ron, ; Hetz, Models indicate overlaps and differences in ER stress signaling.

Further, transcripts of genes encoding proteins of the ER-QC machinery [e. Putative plant ER stress sensors and signaling components have been identified Figure 1B , however, except for IRE, respective plant proteins do not show sequence but structural or functional homology Koizumi et al.

Arabidopsis possesses at least two IRE1-like proteins, while only one homolog is present in rice Oryza sativa. Atbzip mutants do not display morphological or developmental differences under non-stress conditions, but are more sensitive to salt stress Atbzip17 , Liu et al.

The expression of salt stress responsive genes is impaired in Atbzip17 mutants Liu et al. This leads to a frame shift that removes the transmembrane domain of the new proteins and allows nuclear entrance Deng et al. The UPR is supposed to ensure cell survival. CHOP down-regulates anti-apoptotic proteins e. BH3-only proteins promote the cell death activation-related oligomerization and translocation of BAX and BAK to the mitochondrial membrane, followed by cytochrome c release and caspase activation for execution of apoptosis.

Dynamic differential interactions with pro- and anti-apoptotic proteins modulated by the intensity and duration of ER stress signals might regulate separate functions of IRE1, and timely coordinated on- and offset of ATF6, PERK, and IRE1 signaling may play a decisive role in determining cell fate.

Autophagy is further suggested to abolish ER stress in yeast and mammals as it might support the removal of unfolded proteins Bernales et al. However, regulators of this cell death pathway and its link to ER stress are currently unknown Verfaillie et al. New insights into the role of vacuolar processing enzymes with caspase1-like activities in the execution of ER-PCD come from Qiang et al. These studies demonstrate the dependence of the mutualistic fungus Piriformospora indica on ER-PCD for successful Arabidopsis root colonization.

Consequently, the P. Plants ward off pathogens by a multi-layered immune system. PM localized pattern recognition receptors PRRs detect conserved molecules, so-called microbe-associated molecular patterns MAMPs , of invading microbes. Successful pathogens have evolved effector molecules to suppress MTI.

The ER participates in plant innate immunity in several ways. Firstly, immunity depends on the secretory apparatus for the production of immune proteins Wang et al. Secondly, synthesis and proper function of PRRs e. Meanwhile, a number of membrane-localized immune receptors have been identified, whose functions depend on ER-QC, among them the rice PRR XA21 involved in resistance to Xanthomonas oryzae pv.

Similarly, proper execution of defense responses may rely on the induction of UPR genes. Consistent with this, many viruses employ host UPR by targeting ER stress sensors to enhance folding of viral proteins or to modulate immune responses in mammals Ke and Chen, ; Qian et al.

In tobacco, infection with Potato virus X or overexpression of a viral movement protein induces bZIP60 and UPR genes possibly to suppress host cell death responses Ye et al.

In addition, Yamamoto et al. This supports infection as it leads to the accumulation of unfolded proteins eventually promoting host cell death Bernal-Bayard et al.

Several bacterial toxins, e. As production site of antimicrobial proteins and of immune signaling components, the ER functions as central regulator in the execution of immune responses in plants and animals. Therefore, the disturbance of ER integrity is certainly of primary relevance for pathogens to achieve host cell infection. Plants further rely on proper ER function and likely ER membrane localized stress sensors for adaptation to abiotic stress such as salt or heat stress Liu et al.

Taken together, the improvement of plant UPR in order to maintain ER homeostasis under unfavorable conditions may increase plant adaptability to biotic and abiotic stress, which bears a potential to enhance crop yield and yield stability. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Aronson, L. DangER: protein ovERload — targeting protein degradation to treat myeloma. Haematologica 97, — Bailly-Maitre, B. Bernal-Bayard, J. Bernales, S. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response.

PLoS Biol. Boller, T. A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Plant Biol. Caplan, J. Induced ER chaperones regulate a receptor-like kinase to mediate antiviral innate immune response in plants. Cell Host Microbe 6, — Chakrabarti, A.

A review of the mammalian unfolded protein response. Che, P. Signaling from the endoplasmic reticulum activates brassinosteroid signaling and promotes acclimation to stress in Arabidopsis.

Chen, L. Cell Host Microbe 7, — Chen, Y. Plant J. Chisholm, S. Host-microbe interactions: shaping the evolution of the plant immune response.

Cell , — The rough endoplasmic reticulum has on it ribosomes, which are small, round organelles whose function it is to make those proteins. Sometimes, when those proteins are made improperly, the proteins stay within the endoplasmic reticulum.

They're retained and the endoplasmic reticulum becomes engorged because it seems to be constipated, in a way, and the proteins don't get out where they're suppose to go. Then there's the smooth endoplasmic reticulum, which doesn't have those ribosomes on it.

And that smooth endoplasmic reticulum produces other substances needed by the cell.