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Sulphur limitation 1 (SLIM1), a member of ethylene‐insensitive3‐like (EIN3/EIL) protein family, is recognised as the pivotal transcription factor regulating sulphur assimilation, essential for maintaining sulphur homoeostasis in Arabidopsis. However, the function of its monocot homologues is largely unknown. In this study, we identified PvEIL3a, a homologous gene of AtSLIM1, from switchgrass (Panicum virgatum L.), a significant perennial bioenergy crop. Our results demonstrated that introducing PvEIL3a into Arabidopsis slim1 mutants significantly increased the expression of genes responsive to sulphur deficiency, and transgenic plants exhibited shortened root length and delayed development. Moreover, PvEIL3a activated the expression of AtAPR1, AtSULTR1;1 and AtBGLU30, which plays an important role in sulphur assimilation and glucosinolate metabolism. Results of transcriptome and metabonomic analysis further indicated a perturbation in the metabolic pathways of tryptophan‐dependent indole glucosinolates (IGs), camalexin and auxin. In addition, PvEIL3a conservatively regulated sulphur assimilation and the biosynthesis of tryptophan pathway‐derived secondary metabolites, which reduced the biosynthesis of indole‐3‐acetic acid (IAA) and inhibited the root elongation of transgenic Arabidopsis. In conclusion, this study highlights the functional difference of the ethylene‐insensitive 3‐like (EIL) family gene in monocot and dicot plants, thereby deepening the understanding of the specific biological roles of EIL3 in monocot plant species. Summary statement: The heterologous expression of PvEIL3a in Arabidopsis slim1 mutant altered sulphur assimilation and glucosinolate metabolism significantly.Glucosinolates and their derivatives increased in pAtSLIM1:PvEIL3a/slim1‐1 transgenic Arabidopsis plants inhibited the root elongation. [ABSTRACT FROM AUTHOR]