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Title: Distinct Cellular Locations of Carbonic Anhydrases Mediate Carbon Dioxide Control of Stomatal Movements

Journal Article · · Plant Physiology (Bethesda)
DOI:https://doi.org/10.1104/pp.15.00646· OSTI ID:1411720
ORCiD logo [1];  [2];  [3];  [4]; ORCiD logo [4];  [5];  [5];  [4];  [6];  [4]
  1. Huazhong Agricultural Univ., Wuhan (China). College of Life Science and Technology; Univ. of California, San Diego, CA (United States). Division of Biological Sciences Cell and Developmental Biology Section
  2. Univ. of California, San Diego, CA (United States). Physics Dept.
  3. Case Western Reserve Univ., Cleveland, OH (United States). Dept. of Physiology and Biophysics
  4. Univ. of California, San Diego, CA (United States). Division of Biological Sciences Cell and Developmental Biology Section
  5. Huazhong Agricultural Univ., Wuhan (China). College of Life Science and Technology
  6. Case Western Reserve Univ., Cleveland, OH (United States). Dept. of Physiology and Biophysics, Dept. of Medicine
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Elevated carbon dioxide (CO2) in leaves closes stomatal apertures. Research has shown key functions of the β-carbonic anhydrases (βCA1 and βCA4) in rapid CO2-induced stomatal movements by catalytic transmission of the CO2 signal in guard cells. But, the underlying mechanisms remain unclear, because initial studies indicate that these Arabidopsis (Arabidopsis thaliana) βCAs are targeted to distinct intracellular compartments upon expression in tobacco (Nicotiana benthamiana) cells. Which cellular location of these enzymes plays a key role in native guard cells in CO2-regulated stomatal movements remains unknown. We express fluorescently tagged CAs in guard cells of ca1ca4 double-mutant plants and show that the specific locations of βCA4 at the plasma membrane and βCA1 in native guard cell chloroplasts each can mediate rapid CO2 control of stomatal movements. Localization and complementation analyses using a mammalian αCAII-yellow fluorescent protein in guard cells further show that cytoplasmic localization is also sufficient to restore CO2 regulation of stomatal conductance. Mathematical modeling of cellular CO2 catalysis suggests that the dynamics of the intracellular HCO3- concentration change in guard cells can be driven by plasma membrane and cytoplasmic localizations of CAs but not as clearly by chloroplast targeting. Therefore, modeling supports the notion that the intracellular HCO3- concentration dynamics in guard cells are a key mechanism in mediating CO2 -regulated stomatal movements but that an additional chloroplast role of CAs exists that has yet to be identified.

Research Organization:
Univ. of California, San Diego, CA (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF); National Institutes of Health (NIH)
Grant/Contract Number:
FG02-03ER15449; MCB1414339; GM060396
OSTI ID:
1411720
Journal Information:
Plant Physiology (Bethesda), Vol. 169, Issue 2; ISSN 0032-0889
Publisher:
American Society of Plant BiologistsCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 61 works
Citation information provided by
Web of Science

References (1)

Distinct Cellular Locations of Carbonic Anhydrases Mediate Carbon Dioxide Control of Stomatal Movements journal August 2015

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Function and Compensatory Mechanisms Among the Components of the Chloroplastic Redox Network text January 2018
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OsWRKY53, a versatile switch in regulating herbivore-induced defense responses in rice journal March 2016
Metabolomic Responses of Guard Cells and Mesophyll Cells to Bicarbonate journal December 2015
Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae journal April 2020

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