Guard cell starch degradation yields glucose for rapid stomatal opening in Arabidopsis

Flütsch, S., Wang, Y., Takemiya, A., Vialet-Chabrand, S. R., Klejchova, M., Nigro, A., Hills, A., Lawson, T., Blatt, M. R. and Santelia, D. (2020) Guard cell starch degradation yields glucose for rapid stomatal opening in Arabidopsis. Plant Cell, 32(7), pp. 2325-2344. (doi: 10.1105/tpc.18.00802) (PMID:32354788)

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Abstract

Starch in Arabidopsis guard cells is rapidly degraded at the start of the day by the glucan hydrolases a-amylase3 (AMY3) and b-amylase1 (BAM1) to promote stomatal opening. This process is activated via phototropin-mediated blue light signaling downstream of the plasma membrane H+-ATPase. It remains unknown how guard cell starch degradation integrates with light-regulated membrane transport processes in the fine control of stomatal opening kinetics. We report that H+, K+ and Cl- transport across the guard cell plasma membrane is unaltered in the amy3bam1 mutant, suggesting that starch degradation products do not directly affect the capacitiy to transport ions. Enzymatic quantification revealed that after 30 min of blue light illumination, amy3bam1 guard cells had similar malate levels as the wild type, but had dramatically altered sugar homeostasis, with almost undetectable amounts of glucose. Thus, glucose, not malate, is the major starch-derived metabolite in Arabidopsis guard cells. We further show that impaired starch degradation in the amy3bam1 mutant resulted in an increase in the time constant for opening of 40 min. We conclude that rapid starch degradation at dawn is required to maintain the cytoplasmic sugar pool, clearly needed for fast stomatal opening. The conversion and exchange of metabolites between subcellular compartments therefore coordinates the energetic and metabolic status of the cell with membrane ion transport.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Blatt, Professor Michael and Wang, Dr Yizhou
Authors: Flütsch, S., Wang, Y., Takemiya, A., Vialet-Chabrand, S. R., Klejchova, M., Nigro, A., Hills, A., Lawson, T., Blatt, M. R., and Santelia, D.
College/School:College of Medical Veterinary and Life Sciences > Institute of Molecular Cell and Systems Biology
Journal Name:Plant Cell
Publisher:American Society of Plant Biologists
ISSN:1040-4651
ISSN (Online):1532-298X
Published Online:30 April 2020
Copyright Holders:Copyright © 2020 The Authors
First Published:First published in Plant Cell 32(7):2325-2344
Publisher Policy:Reproduced under a Creative Commons licence

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
190663Stomatal-based systems analysis of water use efficiencyMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/L001276/1MCSB - Plant Sciences
170599Analysing GORK clustering for enhanced stomatal controlMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/M001601/1MCSB - Plant Sciences
172302Dissecting a new and vital checkpoint in SNARE recycling and plant growthMichael BlattBiotechnology and Biological Sciences Research Council (BBSRC)BB/N006909/1MCSB - Plant Sciences