Dynamics of the leaf endoplasmic reticulum modulate β-glucosidase-mediated stress-activated ABA production from its glucosyl ester

The phytohormone abscisic acid (ABA) is produced via a multistep de novo biosynthesis pathway or via single-step hydrolysis of inactive ABA-glucose ester (ABA-GE). The hydrolysis reaction is catalyzed by beta-glucosidase (BG, or BGLU) isoforms localized to various organelles, where they become activated upon stress, but the mechanisms underlying this organelle-specific activation remain unclear. We investigated the relationship between the subcellular distribution and stress-induced activation of BGLU18 (BG1), an endoplasmic reticulum enzyme critical for abiotic stress responses, in Arabidopsis thaliana leaves. High BGLU18 levels were present in leaf petioles, primarily in endoplasmic reticulum bodies. These Brassicaceae-specific endoplasmic reticulum-derived organelles responded dynamically to abiotic stress, particularly drought-induced dehydration, by changing in number and size. Under stress, BGLU18 distribution shifted toward microsomes, which was accompanied by increasing BGLU18-mediated ABA-GE hydrolytic activity and ABA levels in leaf petioles. Under non-stress conditions, impaired endoplasmic reticulum body formation caused a microsomal shift of BGLU18 and increased its enzyme activity; however, ABA levels increased only under stress, probably because ABA-GE is supplied to the endoplasmic reticulum only under these conditions. Loss of BGLU18 delayed dehydration-induced ABA accumulation, suggesting that ABA-GE hydrolysis precedes the biosynthesis. We propose that dynamics of the endoplasmic reticulum modulate ABA homeostasis and abiotic stress responses by activating BGLU18-mediated ABA-GE hydrolysis.