Abstract
Osmotic stress activates the biosynthesis of the phytohormone abscisic acid (ABA) through a pathway that is rate limited by the carotenoid cleavage enzyme 9-cis-epoxycarotenoid dioxygenase (NCED). To understand the signal transduction mechanism underlying the activation of ABA biosynthesis, we performed a forward genetic screen to isolate mutants defective in osmotic stress regulation of the NCED3 gene. Here, we identified the Arabidopsis (Arabidopsis thaliana) Vacuolar Sorting Receptor1 (VSR1) as a unique regulator of ABA biosynthesis. The vsr1 mutant not only shows increased sensitivity to osmotic stress, but also is defective in the feedback regulation of ABA biosynthesis by ABA. Further analysis revealed that vacuolar trafficking mediated by VSR1 is required for osmotic stress-responsive ABA biosynthesis and osmotic stress tolerance. Moreover, under osmotic stress conditions, the membrane potential, calcium flux, and vacuolar pH changes in the vsr1 mutant differ from those in the wild type. Given that manipulation of the intracellular pH is sufficient to modulate the expression of ABA biosynthesis genes, including NCED3, and ABA accumulation, we propose that intracellular pH changes caused by osmotic stress may play a signaling role in regulating ABA biosynthesis and that this regulation is dependent on functional VSR1.
Highlights
Biological and Environmental Sciences and Engineering Division, King Abdullah University of Science and Technology, Thuwal 23955–6900, Saudi Arabia (Z.-Y.W., C.G., L.X.); State Key Laboratory of Grassland Agroecosystem, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, Lanzhou 730000, Gansu Province, China (Z.-Y.W., F.-M.L.); Department of Plant Science and Landscape Architecture, University of Maryland, College Park, Maryland 20742 (J.Z.); Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, Indiana 47907 (J.-K.Z.); and Shanghai Center for Plant Stress Biology, Shanghai Institutes of Biological Sciences, Chinese Academy of Sciences, Shanghai 200032, China (J.-K.Z.)
Given that manipulation of the intracellular pH is sufficient to modulate the expression of abscisic acid (ABA) biosynthesis genes, including NCED3, and ABA accumulation, we propose that intracellular pH changes caused by osmotic stress may play a signaling role in regulating ABA biosynthesis and that this regulation is dependent on functional Vacuolar Sorting Receptor1 (VSR1)
The shoot and root growth was inhibited by osmotic stress treatments in both wild-type and ced2 mutant seedlings, but the inhibition was more pronounced in the ced2 mutant (Supplemental Fig. S1, C and D)
Summary
To understand the signal transduction mechanism underlying the activation of ABA biosynthesis, we performed a forward genetic screen to isolate mutants defective in osmotic stress regulation of the NCED3 gene. In turn, is oxidized by a short-chain alcohol dehydrogenase (ABA2) to abscisic aldehyde, which is converted to ABA by abscisic acid aldehyde oxidase (AAO3) using a molybdenum cofactor activated by the molybdenum cofactor sulfurase (ABA3; Nambara and Marion-Poll, 2005) In this pathway, it is generally thought that the cleavage step catalyzed by NCED is the rate-limiting step (Iuchi et al, 2000, 2001; Qin and Zeevaart, 2002; Xiong and Zhu, 2003). Our study further suggests that intracellular pH changes might act as an early stress response signal triggering osmotic stress-activated ABA biosynthesis
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