Glucosinolate catabolism maintains glucosinolate profiles and transport in sulfur-starved Arabidopsis

Glucosinolates (GSL) are sulfur (S)-rich specialized metabolites produced by plants of the Brassicales order. Our previous study found that in Arabidopsis seedlings, S deficiency (−S) promoted GSL catabolism by activating two ß-glucosidases (BGLU), BGLU28 and BGLU30. The induced GSL catabolism was a survival strategy for seedlings grown under −S, because S released from GSL was reincorporated into primary S metabolites which are essential for plant growth. However, as GSL profile in plants vary among growth stages and organs, we set out to test a potential contribution of BGLU28/30-dependent GSL catabolism at the reproductive growth stage. Thus, in this study, we assessed growth, metabolic, and transcriptional phenotypes of mature bglu28/30 double mutants grown under different S conditions. Our results showed that compared to wild-type plants grown under −S, mature bglu28/30 mutants displayed impaired growth and accumulated increased levels of GSL in their mature seeds, siliques, flowers, and rosette leaves of before bolting plants. In contrast, the levels of primary S-containing metabolites, glutathione and cysteine, were decreased in mature seeds. Furthermore, the transport of GSL from rosette leaves to the reproductive organs was stimulated in the bglu28/30 mutants under −S. Transcriptome analysis revealed that genes related to other biological processes, such as phytohormone signaling and plant response to heat, responded differentially to −S in the bglu28/30 mutants. Altogether, these findings broadened our understanding of the roles of BGLU28/30-dependent GSL catabolism in plant adaptation to nutrient stress. One-sentence summary Disruption of glucosinolate catabolic genes, BGLU28 and BGLU30, in sulfur-starved mature Arabidopsis impaired growth, affected glucosinolate distribution, and altered transcriptional profiles.