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Many plants possess two or more ubiquitin-activating enzymes (E1). However, it is unclear whether the E1s of a plant genome play equivalent roles in various pathways. Here we report that tomato and tobacco encode dual ubiquitin-activating systems (DUAS) in which the E1s UBA1 and UBA2 display differential specificities in charging four groups of E2s.The C-terminal ubiquitin-folding domain of the E1s play a major but not sole role in determining the differential specificities of charging the four groups E2s. The dual systems do not play equivalent roles in plant immunity, with silence of UBA2 only compromising host immunity. Among the differentially charged E2s, group IV members UBC32, UBC33 and UBC34 are shown to be essential for ER-associated protein degradation (ERAD) and plant immunity. Like tomato, Arabidopsis UBC32/33/34 E2 triplet are also differentially charged by its E1s and are essential for plant immunity. Loss of function in Arabidopsis UBC32, UBC33 and UBC34 does not affect flg22 and elf18-triggered inhibition of seedling growth but results in alteration of ER stress tolerance, which likely contribute to the diminished plant immunity in the mutants. Our results uncover DUAS in plants and a previously unknown E1‒ERAD-associated E2 triplet module in the regulation of host immunity.