In eukaryotic cells, the accumulation of unfolded or misfolded proteins in the endoplasmic reticulum (ER) results in ER stress that induces a cascade of reactions called the unfolded protein response (UPR). In Arabidopsis, the most conserved UPR sensor, Inositol-requiring enzyme 1 (IRE1), responds to both abiotic- and biotic-induced ER stress. Guanine nucleotide-binding proteins (G proteins) constitute another universal and conserved family of signal transducers that have been extensively investigated due to their ubiquitous presence and diverse nature of action. Arabidopsis GTP-binding protein β1 (AGB1) is the only G-protein β-subunit encoded by the Arabidopsis genome that is involved in numerous signaling pathways. Mounting evidence suggests the existence of a crosstalk between IRE1 and G protein signaling during ER stress. AGB1 has previously been shown to control a distinct UPR pathway independently of IRE1 when treated with an ER stress inducer tunicamycin. Our results obtained with combinatorial knockout mutants support the hypothesis that both IRE1 and AGB1 synergistically contribute to ER stress responses chemically induced by dithiothreitol (DTT) as well as to the immune responses against a phytopathogenic bacterium Pseudomonas syringae pv. tomato strain DC3000. Our study highlights the crosstalk between the plant UPR transducers under abiotic and biotic stress.