Endoplasmic reticulum (ER)-mediated protein secretion and quality control have been shown to play an important role in immune responses in both animals and plants. In mammals, the ER membrane-located IRE1 kinase/endoribonuclease, a key regulator of unfolded protein response (UPR), is required for plasma cell development to accommodate massive secretion of immunoglobulins. Plant cells can secrete the so-called pathogenesis-related (PR) proteins with antimicrobial activities upon pathogen challenge. However, whether IRE1 plays any role in plant immunity is not known. Arabidopsis thaliana has two copies of IRE1, IRE1a and IRE1b. Here, we show that both IRE1a and IRE1b are transcriptionally induced during chemically-induced ER stress, bacterial pathogen infection and treatment with the immune signal salicylic acid (SA). However, we found that IRE1a plays a predominant role in the secretion of PR proteins upon SA treatment. Consequently, the ire1a mutant plants show enhanced susceptibility to a bacterial pathogen and are deficient in establishing systemic acquired resistance (SAR), whereas ire1b is unaffected in these responses. We further demonstrate that the immune deficiency in ire1a is due to a defect in SA- and pathogen-triggered, IRE1-mediated cytoplasmic splicing of the bZIP60 mRNA, which encodes a transcription factor involved in the expression of UPR-responsive genes. Consistently, IRE1a is preferentially required for bZIP60 splicing upon pathogen infection, while IRE1b plays a major role in bZIP60 processing upon Tunicamycin (Tm)-induced stress. We also show that SA-dependent induction of UPR-responsive genes is altered in the bzip60 mutant resulting in a moderate susceptibility to a bacterial pathogen. These results indicate that the IRE1/bZIP60 branch of UPR is a part of the plant response to pathogens for which the two Arabidopsis IRE1 isoforms play only partially overlapping roles and that IRE1 has both bZIP60-dependent and bZIP60-independent functions in plant immunity.

Rapid and complex immune responses are induced in plants upon pathogen recognition. One form of plant defense response is a programmed burst in transcription and translation of pathogenesis-related proteins, of which many rely on ER processing. Interestingly, several ER stress marker genes are up-regulated during early stages of immune responses, suggesting that enhanced ER capacity is needed for immunity. Eukaryotic cells respond to ER stress through conserved signaling networks initiated by specific ER stress sensors tethered to the ER membrane. Depending on the nature of ER stress the cell prioritizes either survival or initiates programmed cell death (PCD). At present two plant ER stress sensors, bZIP28 and IRE1, have been described. Both sensor proteins are involved in ER stress-induced signaling, but only IRE1 has been additionally linked to immunity. A second branch of immune responses relies on PCD. In mammals, ER stress sensors are involved in activation of PCD, but it is unclear if plant ER stress sensors play a role in PCD. Nevertheless, some ER resident proteins have been linked to pathogen-induced cell death in plants. In this review, we will discuss the current understanding of plant ER stress signaling and its cross-talk with immune signaling.

General Control Non-derepressible 2 (GCN2) is an evolutionarily conserved serine/threonine kinase that modulates amino acid homeostasis in response to nutrient deprivation in yeast, human and other eukaryotes. However, the GCN2 signaling pathway in plants remains largely unknown. Here, we demonstrate that in Arabidopsis, bacterial infection activates AtGCN2-mediated phosphorylation of eIF2α and promotes TBF1 translational derepression. Consequently, TBF1 regulates a subset of abscisic acid signaling components to modulate pre-invasive immunity. We show that GCN2 fine-tunes abscisic acid accumulation and signaling during both pre-invasive and post-invasive stages of an infection event. Finally, we also demonstrate that AtGCN2 participates in signaling triggered by phytotoxin coronatine secreted by P. syringae. During the preinvasive phase, AtGCN2 regulates stomatal immunity by affecting pathogen-triggered stomatal closure and coronatine-mediated stomatal reopening. Our conclusions support a conserved role of GCN2 in various forms of immune responses across kingdoms, highlighting GCN2’s importance in studies on both plant and mammalian immunology.

The plant hormone salicylic acid (SA) plays an essential role in the regulation of diverse biological processes throughout the entire lifespan of the plant. Twenty-five years ago, SA first emerged as an endogenous signal capable of inducing plant defence responses both at the site of infection and in the systemic tissue of the plant. Since then, SA-mediated signalling pathways have been extensively characterized and dissected using genetic and biochemical approaches. Current research is largely focused on the identification of novel SA downstream signalling genes, in order to understand their precise contributions to the phytohormonal cross-talk and signalling network. This will subsequently help us to identify novel targets that are important for plant health, and contribute to advances in modern agriculture. In this chapter we highlight recent advances in the field of SA biosynthesis and the discovery of candidates for systemic mobile signals. We also discuss the molecular mechanisms underlying SA perception. In addition, we review the novel SA signalling components that expand the scope of SA functions beyond plant immunity to include plant growth and development, endoplasmic reticulum (ER) stress, DNA repair and homologous recombination. Finally, we shed light on the roles of SA in epigenetically controlled transgenerational immune memory that has long-term benefits for plants.

The sessile lifestyle of plants requires them to cope with a multitude of stresses in situ. In response to diverse environmental and intracellular cues, plant cells respond by massive reprogramming of transcription and translation of stress response regulators, many of which rely on endoplasmic reticulum (ER) processing. This increased protein synthesis could exceed the capacity of precise protein quality control, leading to the accumulation of unfolded and/or misfolded proteins that triggers the unfolded protein response (UPR). Such cellular stress responses are multilayered and executed in different cellular compartments. Here, we will discuss the three main branches of UPR signaling in diverse eukaryotic systems, and describe various levels of ER stress response regulation that encompass transcriptional gene regulation by master transcription factors, post-transcriptional activities including cytoplasmic splicing, translational control, and multiple post-translational events such as peptide modifications and cleavage. In addition, we will discuss the roles of plant ER stress sensors in abiotic and biotic stress responses and speculate on the future prospects of engineering these signaling events for heightened stress tolerance.