Responses of Endoplasmic Reticulum to Plant Stress

Abstract

Global climate change has resulted in alterations in the biotic and abiotic conditions of the planet. This has led to changes in the agricultural system resulting from reduced water availability, increased temperature increase in the population and occurrences of pests and diseases. Plants are adversely affected when they experience any stress retarding their growth, development and productivity. Endoplasmic Reticulum (ER) is an organelle that shows a tremendous response when subjected to stress conditions. Therefore, to explore and comprehend plants’ multidimensional interactions when subjected to stress conditions, an insight into the molecular stress signalling in the ER in response to the stress situation is discussed in this chapter.

1. Introduction

The endoplasmic reticulum (ER) is a versatile, dynamic and largely pleiotropic subcellular organelle forming an essential part of eukaryotes. It is one of the largest in size, complex in functionality and variable in architecture [1]. It plays a significant role in maintaining the spatial organisation of endomembrane organelles by acting as an architectural framework. It also synthesises essential cellular building blocks like lipids and proteins. ER lies at the core of the endomembrane system, which comprises unified endocytic and biosynthetic cellular processes and is composed of two different structural subdomains. One is the nuclear envelope enclosing the nucleus, and the other is the peripheral ER comprising the interconnected network of flattened sacs and tubules [2, 3]. At a submicron level, the ER network is organised in morphologically distinct domains that assume specific functions [4]. The ER represents the organelle with the largest membrane surface area owing to its network of interconnected tubules and flattened cisternae. Several genetic studies aided with live-cell imaging have illustrated the underlying drivers and the implausible dynamism of ER. The ER exemplifies a secretory pathway gatekeeper that controls protein quality control, its folding, signalling, and degradation across multiple checkpoints and impacts the general plant growth cellular homeostasis.

The ER is responsible for synthesising an array of proteins such as enzymes, ion channels, receptors and cargo molecules that modulate several essential physiological processes, which are ultimately either retained in or distributed from the ER [5, 6, 7]. Besides syntheses, ER also serves as a storehouse for carbohydrates and calcium [8, 9] and plays an essential role in abiotic and biotic stress resistance through the control of protein folding and signalling [10]. These characteristics of ER make it a functionally and structurally non-uniform yet morphologically continuous cellular compartment.

2. ER in plants: structure and function

In plant cells, the ER plays a critical role in the organism and bears a strong connection with other plant organelles like the vacuole, Golgi apparatus [7, 11, 12] and chloroplast [13, 14] forming the shape of a spider-webbed membrane network and any defect in its functionality can give rise to several developmental defects [15, 16, 17, 18]. Based on electron microscopy studies, the ER can be differentiated into smooth ER-bearing subdomains with associated ribosomes, rough ER with subdomains of ribosomes-free regions, and nuclear envelope regions which are enwrapped by the ER forming a double membrane demarcating the nucleus [4, 19, 20]. The ER forms connections with the neighbouring cells through channels called plasmodesmata that protrude into the cell wall and interconnect with the cytoplasm of the neighbouring cells [21, 22], forming a unique organelle that cannot be delimited by a cell boundary. Electron microscopy-aided studies have also reported that the plant ER form connections with other membranes, including vacuoles, plastids, mitochondria and Golgi apparatus. In addition to the ER- plasma membrane contact sites (EPCSs) and plasmodesmata [4, 23]. The optical trapping and tweezer system has established physical contact of the chloroplast and Golgi apparatus with the ER [24, 25].

It has been thought that the movement of the ER influences the movement of other organelles, which is possible by the several network connections from the ER to the other cell organelles. While the ER enlarges, contracts or reorganises its morphology, its integrity is maintained by unfolded protein response (UPR) [26] signalling demonstrating the relationship between the ER morphology and its functional integrity [27, 28, 29]. Therefore, the connection of ER with other cellular organelles and compartments is crucial for the exchange of constituents as well as for their function and spatial distribution [29, 30].

The most fascinating feature of the ER in the plant cell is its extraordinary dynamicity which can be easily observed through microscopic analysis resulting in the overall evolving architecture of the tubules and cisternae of the ER that are in a state of continuous movement and rearrangement [27, 29, 31]. This morphological reorganisation of the ER has been reported previously where in the initial phases of cell growth, the ER was observed as a compact entanglement of membranes which undergo reorganisation into an open network as the cell growth advances [27, 32]. The ER organisations become even more complicated in root cells where the ER assumes a condensed form, primarily where the root hairs originate [27, 33]. Evidence of a link between ER shape and ER function can be demonstrated when mutations in Root Hair Defective3 (RHD3) ER-shaping protein compromise the functional organisation of the ER by elongation of the cells and transitioning to a reticulate pattern from a more sheet-like form [29, 30].

3. Response of plant ER to stress

The changing climate poses a significant risk to the plants owing to the transitions in its natural environment from typical to very harsh conditions. When plants are exposed to adversities like low water availability, high or chilling temperature, salt concentrations in the soil or pest and disease infestations, they usually respond by changing their response in a dynamic way. Although several studies have aimed to investigate the response of plants to individual environmental stress, in the field, the scenario is such that the plants may be exposed to multiple stresses, and their response may be quite different from that in the laboratory [34]. These dynamic responses in plants include changing the proteome by changing the gene expression patterns [35]. In plants, the ER is the prime organelle that regulates the stress responses [36, 37], as any stress which affects protein folding leads to a cellular homeostatic response mediated by the UPR in response to ER stress [36, 38]. ER is the point of synthesis of the majority of plant cell proteins and also the point of folding of unfolded or misfolded proteins, which are aided by chaperons and co-chaperons [39, 40]. The ER quality control (ERQC) and ER-associated degradations (ERAD) are two mechanisms that maintain the folding of proteins and degrade the misfolded proteins, respectively [39]. Nevertheless, sometimes, these mechanisms are surpassed by the UPR when there is an accumulation and persistence of misfolded and/or unfolded proteins leading to a state where the organelles trigger specific signalling pathways to restore the ER mechanism and recover from the stress [41].

4. ER stress signalling in response to heat stress

Heat stress often poses a serious threat to plants, as it negatively affects photosynthesis and fertility and can at times result in death. At the cellular level, symptoms of heat stress include the accumulation of misfolded or denatured proteins, production of ROS, microtubule disorganisation, and membrane instability. As the endoplasmic reticulum (ER) is the site of production for many proteins and lipids, this organelle is tightly linked with the heat stress response. While heat stress response mechanisms include the accumulation of osmolytes and antioxidants, perhaps the most canonical response is the production of Heat Shock Proteins (HSPs): molecular chaperones which facilitate proper protein folding and/or disaggregation of misfolded proteins [42].

Two critical components of the ER’s Unfolded Protein Response (UPR) are also the major regulators of the heat stress response: the transcription factor bZIP28 and cytosolic RNA-splicing enzyme IRE1. bZIP28 was first determined to be involved in the heat stress response in Arabidopsis through a combination of co-expression analysis, cellular localisation studies, and reverse genetics [43]. Further studies have elucidated the mechanism of action of bZIP28 in the heat stress response [44, 45]. Briefly, in unstressed cells, bZIP28 is tethered to the ER membrane by an HSP (Binding Immunoglobulin Protein, or BiP), but when misfolded or denatured proteins accumulate in the ER, BIP is competed away from bZIP28, thereby releasing it to act as a transcription factor and upregulate the expression of other HSPs. Arabidopsis IRE1 was found to upregulate bZIP60 – another transcription factor upregulating stress-responsive genes – through cytosolic mRNA splicing [46]. These proteins are at once essential for the UPR stress response in general and the heat stress response, specifically as HSPs are among their direct or indirect targets and their loss of function results in decreased survival under heat stress [47]. These initial studies uncovered the ER’s direct role in mediating heat stress.

More recent studies have discovered roles for the ER in the metabolism under heat stress, specifically in the starch and lipid biosynthesis pathways. Although the role of the ER in starch metabolism is less clear than its role in lipid metabolism, several studies have implicated its involvement. In rice, heat stress during grain set can result in a “chalky” grain appearance and decreased starch content. Several studies have found altered expression of starch biosynthetic genes in mutants of the UPR, particularly in seeds [48, 49]. Other studies have found that the application of heat stress during the pre-cellularisation stage of grain set results in increased chalkiness and decreased starch levels [50]. A final study found that components of the UPR regulate starch content and chalkiness in rice seeds under heat stress [51]. When considered together, these results implicate that the ER/UPR regulates starch metabolism under heat stress. While the exact mechanisms underpinning this regulation are unclear, it has been known for some time that the ER is a site of lipid biosynthesis in plants. Tight control of lipid metabolism under heat stress is required as plants alter the lipid composition of membranes in order to combat heat-induced membrane instability.

In many plants, including Arabidopsis [52], tomato [53], wheat [54], and turfgrasses [55], an increase in the amounts of ER-produced lipid classes occurs under heat. Forward genetic studies have further demonstrated that ER stress, as well as heat stress, can alter lipid metabolism. For example, Arabidopsis mutants with inactive Fatty Acid Desaturase 2 (fad2 mutants) show either aberrant phenotypes or increased symptoms under heat [56] or ER stress (imposed by tunicamycin) [57], respectively, compared to WT. In soybean, isoforms of FAD2 were found to be unstable in high temperatures [58], and FAD2 transcripts were found to be downregulated under heat stress in Arabidopsis [59]. These results suggest that lipid metabolism, and to some degree starch metabolism, is dependent upon favourable conditions in the ER and is altered under heat stress.

One of the open questions in ER stress regulation is how the stress is perceived by the ER and what molecules or phenomena serve as the stress signal(s). Extracellular Ca²⁺ was one of the first candidates hypothesised to be the cellular signal for heat stress [60]. Seminal studies hypothesised the following signalling response: the influx of extracellular Ca²⁺ via Cyclic Nucleotide Gated Channels activates Calmodulin, which activates kinases, which finally activates Heat Shock Transcription Factors [61]. Other early putative signals included a nuclear-localised histone sensor and two ER-localised unfolded protein sensors [61]. More recent studies have implicated other molecules to act as a signal for heat stress, specifically Jasmonic Acid (JA) and phytochromes. In a recent study in rice grains, JA biosynthesis and signalling activity was enriched among genes upregulated one hour after heat shock, and JA accumulated three hours after heat. Furthermore, treatment with Methyl JA (MeJA) increased the abundance of IRE1-spliced OsBZIP50(s), an ER-stress response biomarker [50]. In another study conducted in Arabidopsis seeds, HY5, a component of light signalling that is downstream of phytochromes, was found to negatively regulate the UPR [62]. Taken concurrently with evidence that phytochromes have thermo-sensing capabilities and that null phytochrome mutants exhibit a constitutive heat stress phenotype [63], the above study provides evidence that phytochromes may sense and transmit the heat stress signal to the ER. Further research is needed to determine the conditions under which these signals are active and if they act in conjunction with each other.

Heat stress can be particularly damaging to anthers and to the developing pollen. Recent evidence points to the UPR being constitutively active in male reproductive tissues [64], and therefore it is critical to understand how the UPR is affected by heat stress in these tissues. In a recent study, several ER-stress genes, including BiP, other chaperones/HSPs, and genes involved in the ER protein cleaning system, were all upregulated under heat stress in pollen germinating in vitro [65]. Furthermore, through forward-genetic studies, it was recently discovered that ER-localised chaperones are critical for proper pollen development and seed set under heat stress. Arabidopsis mutants of the Thermosensitive Male Sterile 1 (TMS1) gene, encoding an HSP40, showed reduced fertility and pollen coat abnormalities when grown under 29°C [66]. Similarly, Arabidopsis mutants lacking IRE1 were male sterile at 29°C yet had viable pollen when grown at room temperature [64]. As proper protein production and secretion are critical for pollen tube growth, any disruption to this process – such as that caused by heat stress – is hypothesised to be detrimental to pollen growth and viability and, therefore, negatively affect fertility.

5. ER stress signalling in response to drought stress

Drought stress is a major driver of yield losses – with a tremendous potential to limit plant growth than any other abiotic stress [67]. An important drought response mechanism is the closure of stomata. This at once conserves water by decreasing evapotranspiration and lowers photosynthesis rates, leading to decreased growth rates. If a period of drought occurs during the reproductive or grain filling stage, yield losses can occur due to pollen sterility or embryo abortion. Plant responses and adaptions to drought stress include the aforementioned stomatal closure, deeper root growth, reduced leaf size and altered leaf orientation. At the cellular level, these drought responses result in loss of turgor, which stimulates the production of the hormone Abscisic acid (ABA). ABA is a canonical “stress response” hormone [68], bringing about morphological changes through the following signal transduction cascade: ABA molecules bind to their receptors, which causes inhibition of PP2C phosphatases, leading to the autophosphorylation and activation of SUCROSE NONFERMENTING1-RELATED SUBFAMILY 2 (SnRK2) kinases, which phosphorylate ABA-responsive transcription factors (AREBs), ultimately leading to the expression of stress-responsive genes.

Some abiotic stresses, notably salt and heat stress, stimulate ER stress by markedly increasing the numbers of misfolded proteins in a cell. However, the mechanism by which drought stress is related to ER stress has yet to be determined. Toward this end, several studies have found multiple components of the ER protein folding machinery to be essential for proper drought response, including several E3 ubiquitin ligases, the transcription factor bZIP60, and Binding Protein (BiP). BiP is a molecular chaperone that contributes to proper protein folding, especially under ER stress. Overexpression of BiP has been found to confer drought tolerance - specifically less stomatal closure, less wilting, and maintenance of turgor - in Nicotiana tabacum (tobacco) and Glycine max (soybean) [69, 70]. Interestingly, the drought tolerance was concurrent with a decrease in the levels of typical drought stress response mechanisms, including the osmolytes proline/sucrose/glucose, root biomass, and drought stress response genes NAC2, glutathione-S-transferase, and antiquitin [69]. Similar to BiP, E3 ligases play essential roles in ER protein folding. The putative E3 ubiquitin ligase SUPPRESSOR OF DRY2 DEFECTS1 (SUD1) is homologous to the mammalian TEB4, a component of the ER-associated degradation pathway (ERAD) that marks non-functional proteins for destruction [71]. Both TEB4 and Arabidopsis SUD1 are implicated in the regulation of sterol biosynthesis [71, 72] – an interesting link between the ER and cellular stress response as sterols are components of lipid membranes that can change membrane fluidity as the temperature fluctuates. Notably, mutations in SUD1 were found to restore drought hypersensitive2 (dry2) [72] – which show increased sensitivity to drought stress due to abnormal sterol composition in roots and aberrant ROS signalling [73] – to WT phenotypes, revealing a link between the ERAD and drought responses. Two additional E3 ubiquitin ligases, Rma1H1 (from Capsicum annum) and Rma1 (from Arabidopsis), confer drought tolerance when overexpressed, putatively through suppressing the trafficking of the aquaporin channel PIP2;1 [74]. The transcription factor bZIP60 – the target of the mRNA splicing enzyme IRE1 – is a third component of the ER stress response that confers drought tolerance when overexpressed. bZIP60 from Boea hygrometrica (the extremely drought-tolerant “resurrection plant”) conferred drought tolerance to Arabidopsis when overexpressed through the up-regulation of several ER quality control genes [75]. These results, when considered together, suggest that increased activity of the ERAD provides enhanced drought tolerance and therefore that ER functions are essential for survival under drought stress, though further research is needed to pinpoint the specific functions of the ER components under drought stress.

Several studies have uncovered an interesting link between ER stress and ABA signalling under drought stress – suggesting that ER functions are mechanistically related to drought stress through ABA. One study mentioned above transformed bZIP60 from B. hygrometrica (BhbZIP60) into Arabidopsis, overexpressed it, and found enhanced drought tolerance and increased expression of both ER components and ABA-responsive genes [75]. Interestingly, the authors found that BhbZIP60 was able to bind to the ERSE cis-regulatory elements present in ER stress-responsive genes but unable to bind to ABA-responsive cis-regulatory elements. Further, BhbZIP60 (in its native host B. hygrometrica), was found to be highly upregulated under drought but not so under heat or salt – which highly upregulates bZIP60 expression in Arabidopsis [46]. Another study found that inactivating the ERSE in Zea mays PP2C-A gene – which encodes a phosphatase with important roles in ABA signal transduction – confers drought stress tolerance [76]. While the WT (ERSE inactive) promotor was responsive to only ABA, the mutant promotor (with a full, active ERSE) was responsive to ABA and ER stress signalling. From these results, the authors proposed the following mechanism for interrelating ER stress with drought stress. When drought stress occurs, it activates ABA signalling, which includes a feedback mechanism for tightly regulating levels of PP2C-A and thereby confers drought tolerance. However, drought stress also activates ER stress signalling, and when PP2C-A is also upregulated by ER stress, the feedback loop is broken, causing hypersensitivity to drought. Further research is needed to see if this is indeed the mechanism by which ER components are interrelated to drought stress, though multiple lines of evidence have implicated ABA signalling in this mechanism.

6. ER stress signalling in response to salt stress

In addition to serving as a site for protein synthesis and transport, ER also plays a crucial role in protein homeostasis under environmental stresses [77]. Stress-induced cellular disruptions such as improper protein folding, excessive protein degradation, accumulation of unfolded protein or overexpression of a protein or increase in the signalling molecules induce ER stress [47].

Three interactive mechanisms, namely, ER quality control (ERQC), ER-associated degradation (ERAD) and the unfolded protein response (UPR) or ER-nucleus signalling pathway, have been described in relation to ER proteostasis function. Salt stress results in the accumulation of misfolded proteins leading to increased transcription of ER-localised proteins, including chaperons such as binding protein (BiP) [78] and Calreticulin (CRT) which aid in restoring proteostasis [79]. On accumulation of misfolded proteins, BiP physically binds to the misfolded proteins, prevents their aggregation and activates UPR signalling [80]. Overexpression of BiP has been reported to enhance salt stress tolerance. Wang et al. [78] identified BiP in Capsicum annuum L. and observed increased salt tolerance on overexpression of CaBiP1 in Arabidopsis. Herath et al. [81] identified three BiP in Solanum tuberosum and observed that one of the identified candidates, StBiP3, is induced by salt stress. CRT is a Ca²⁺ binding protein having molecular chaperon activity. Salt stress induces the transcript levels of CRT protein. Overexpression of CRT isoforms has been reported to increase stress tolerance in wheat [79] and tobacco [82].

ER stress signalling is also known to induce transcription of salt-responsive genes. Under salt stress, ABA levels increases which initiate proteolytic cleavage of an ER membrane-associated transcription factor bZIP17 by Golgi apparatus-resident site-1 protease (SIP). Processed bZIP17 is translocated to the nucleus to activate salt-responsive genes [83]. Liu et al. [44] showed that mutants of bZIP17 have increased sensitivity to salt stress. Ramakrishna et al. [84] reported increased salt tolerance in tobacco plant overexpressing bZIP17 from finger millet. Similarly, overexpression of ER-small heat shock protein (ER-sHSP), another ER-localised chaperon, has been reported to enhance salt tolerance in tomato (Fu et al., 2016). Guan et al. [85] characterised an ER-localised chaperon, namely Sensitive to Salt1 (SES1), which is induced by salt stress and activated by ER stress sensor bZIP17 by direct binding on the promoter region. These studies highlight the role of ER chaperones in stress signalling and acting as an important positive regulator of salt tolerance in plants.

In addition to chaperons, some enzymes involved in protein modifications also play an essential role in ERQC under salt stress. Blanco-Herrera et al. [86] observed that the mutants of UDP-glucose: glycoprotein Glucosyltransferase (UGGT), an enzyme involved in N-glycan protein modification of the misfolded proteins, are more sensitive to salt stress and negatively impacts plant growth.

Various ERAD components have been reported to act as both positive and negative regulators of salt tolerance in plants. In Arabidopsis, a mutant of ERAD components SEL1L/HRD3A and OS9 showed increased sensitivity to salt stress [87, 88], whereas Cui et al. [89] described a mutant for another ERAD component, ubiquitin-conjugating enzyme 32 (UBC32) to have enhanced salt tolerance in Arabidopsis.

Upregulation of UPR pathway genes has been associated with stress tolerance. Babitha et al. [90] reported that overexpression of a stress-responsive finger millet bZIP60 in tobacco leads to upregulation of UPR pathway genes such as BiP1, CRT1 and PDIL. The study proposed that the improved tolerance, in this case, could be through the UPR pathway.

As part of the salt stress signalling cascade, the components associated with the ERQC, ERAD and UPR mechanisms may work independently or may have regulatory connections with each other [45, 91, 92, 93, 94]. Although many studies have reported the role of ER stress signalling in salt stress response, the underlying molecular mechanism and client proteins for the ER-associated regulatory mechanisms are still unknown. Zhang et al. [95] performed the first ER proteome analysis of wheat seedlings to understand the role of ER proteostasis pathways in salt-induced growth reduction. They proposed a putative mechanism whereby salt stress generates ROS, which triggers Redox reactions in the cell leading to the accumulation of misfolded proteins. This increase in misfolded proteins in the ER lumen then triggers ER stress which further activates UPR to relieve ER stress and maintain proteostasis.

7. ER stress signalling in response to cold stress

Early perception of temperature fluctuation and remodelling of the cell membrane (or lipid bilayer) is the key to acclimation to sub-optimal growth conditions. Because ER is the site of fatty acid synthesis, changes in phospholipid composition in response to cold stress are expected to be determined in the ER. In this context, Tasseva et al. [96] investigated the ability of ER membranes to alter lipid composition in Brassica napus and reported desaturases involved in changing membrane fluidity. Cold stress leads to unstable membrane curvatures resulting from the accumulation of diacylglycerols (DAGs) [97]. Rupiz-Lopez et al. [98] revealed that two ER-localised synaptotagmin proteins, SYT1 and SYT3, remove DAGs to prevent PM damage caused by cold stress. Additionally, ER also hosts membrane proteins that act as a sensor of cold and help elicit a stress response. In this context, Ma et al. [99] identified CHILLING TOLERANCE DIVERGENCE 1 (COLD1), a plasma membrane (PM) and ER-localised protein in rice which triggers Ca²⁺ signalling in response to cold stress. Orthologs of COLD1 have also been identified in wheat [100] and Maize [101]. Overexpression of calcium-dependent protein kinases and calreticulin, also hosted by ER, has been reported to increase cold tolerance in rice [102]. William et al. [103] characterised a member of the Bcl-2-associated athanogene (BAG) family, AtBAG7 affecting cold tolerance in Arabidopsis is localised to the ER. Recently, Hu et al. [104] identified an ER-localised Sugars Will Eventually be Exported Transporters (SWEETs) which confers cold tolerance by regulating sugar metabolism and compartmentalisation under cold stress in Arabidopsis. Although many transporters situated in ER are involved in cold tolerance, our understanding of the underlying molecular mechanism is still limited.

8. ER stress signalling in response to biotic factors

Interactions of plants with various organisms play an essential role in its adaptability to the changing environment, not just in protecting it against various pathogens but also in enhancing its defence mechanisms [105, 106, 107]. When plants are subjected to microbial attack, pathogenesis-related (PR) proteins are synthesised as a response to it. A form of the immune response, Systemic Acquired Resistance (SAR), is established as a result of the NONEXPRESSOR OF PR GENE1 (NPR1)-regulated expression of PR genes in Arabidopsis [108]. Thus, it is conceivable that part of the plant immune response, including SAR, requires the synthesis and subsequent secretion of some PR proteins toward microbial pathogens. Consistent with this notion, the expression of several genes involved in protein secretion is induced in SAR of Arabidopsis in an NPR1- dependent manner, implying increased capability for SAR via transcriptional regulation that requires NPR1 function [109]. It was also reported in tobacco (N. tabacum) plants that induction of the lumenal binding protein, an ER-resident chaperone, occurs rapidly during pathogen attack and precedes the expression of PR genes [110].

Several studies have demonstrated the involvement of ER bodies in plant defence mechanisms. Even if there is an artificial induction of a wound on a plant using the wound hormone jasmonic acid, which mimics the pest chewing damage, ER bodies are stimulated [111, 112]. In a study involving Brassicaceae plants, which are resistant to arbuscular mycorrhizal fungi (AMF) symbiosis, the plants were found to be susceptible to non-AMF groups (Piriformospora indica in particular), which in turn enhanced the growth of the plant [113] and showed that ER bodies act in the defence mechanism [114]. Arabidopsis mutants were impaired in the expression of PYK10, a target gene of P. indica in the roots of Arabidopsis [115]. PYK10 is a gene for an abundant myrosinase located in the ER [116, 117] which has spindle-shaped structures and is named ER bodies [27, 118, 119]. ER bodies can also be induced in rosette leaves by JA [120], and the jasmonate-insensitive coronatine insensitive1 [121] mutant does not form ER bodies [111].

9. Conclusions

Plants experience several stresses during their lifetime and in order to survive them, they should have a fast and dynamic response mechanism. Since nearly one third of the plant cell proteins responsible for being affected by stress are located in the ER, it has been studied that ER expresses differential responses in the plant in response to the situation. These dynamic responses in plants include changing the proteome by changing the gene expression patterns. It is the prime organelle that regulates the stress responses as any stress which affects protein folding leads to a cellular homeostatic response mediated by the UPR in response to ER stress. Figure 1 highlights critical ER responses against perceived biotic/abiotic stress conditions.

Figure 1.

Summary of ER responses to biotic/abiotic stress conditions. Under biotic/abiotic stress conditions in plants such as virus infection, stress-related hormones and heat and osmotic stress, several factors including BiP, IRE1, bZIP60, bZIP17/28, genes involved in NPR1-depenedent pathways. Uncharacterized molecular pathways are indicated in dashed arrows. (adapted from [47]).

Acknowledgments

V.J.B. and B.S. thankfully acknowledge the Department of Biotechnology, Govt. of India for providing research grant to Assam Agricultural University and Dibrugarh University [Grant No. BT/PR25099/NER/95/1014/2017, dated 29 May 2018 and Grant no. BT/PR36255/NNT/28/1728/2020, dated 01/12/2021]. V.J.B. also acknowledge the support rendered by DBT e-Library Consortium (DeLCON) to Centre for Biotechnology and Bioinformatics at Dibrugarh University.

Conflict of interest

The authors declare no conflict of interest.