Indole glucosinolate over-accumulation affects plant fitness and tolerance to biotic stress in oilseed Brassica juncea

The Brassicales-specific glucosinolates (GSLs) exhibit a wide range of chemical diversity that is crucial for plant survival in complex environments. Our initial metabolite analysis suggested, that the cultivated Brassica crops had a lower accumulation of indole GLSs (iGSLs), that were otherwise inducible upon pest and pathogen challenges. However, the ecological significance behind the accumulation of class-specific GSLs and their metabolic shifts in Brassica crops has not been traced to date. Herein, we observed that the polyploid Brassica juncea possesses an expanded repertoire of candidate MYBs regulating iGSLs, however with a reduced transcript abundance than the corresponding aliphatic GSL (aGSL) MYB counterparts. To selectively manipulate a durable resistance in B. juncea, iGSLs were constitutively overexpressed using Arabidopsis MYB regulator genes (AtMYB34, AtMYB51, AtMYB122) independently, which significantly enhanced the iGSL accumulation and distribution across different tissue types. However, the iGSL overaccumulation in B. juncea was accompanied by a reduction in the aGSL pool and altered expression of its pathway genes. The performance of B. juncea lines with altered iGSL and aGSL pools was evaluated against two generalist pests and a necrotrophic pathogen. Our data suggest that iGSL over-accumulation does not confer any fitness advantage against biotic stress. Moreover, iGSL enhancement over the wild-type levels significantly declined the growth and yield-related parameters along with the alteration of the growth phytohormones, auxin and cytokinin. Overall, the current study highlights that iGSLs although being inducible upon biotic stimulus, their over-accumulation in crops may impose physiological costs that outweigh their otherwise potential benefits in plants.