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

Elevated carbon dioxide (CO 2) in leaves closes stomatal apertures. Research has shown key functions of the β-carbonic anhydrases (βCA1 and βCA4) in rapid CO 2-induced stomatal movements by catalytic transmission of the CO 2 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 CO 2-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 CO 2 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 CO 2 regulation of stomatal conductance. Mathematical modeling of cellular CO 2 catalysis suggests that the dynamics of the intracellular HCO 3 - concentration change in guard cells can be driven by plasma membrane and cytoplasmic localizations of CAs but not as clearly by chloroplast targeting. Therefore,more » modeling supports the notion that the intracellular HCO 3 - concentration dynamics in guard cells are a key mechanism in mediating CO 2 -regulated stomatal movements but that an additional chloroplast role of CAs exists that has yet to be identified.« less
Authors:
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
Publication Date:
Grant/Contract Number:
FG02-03ER15449; MCB1414339; GM060396
Type:
Accepted Manuscript
Journal Name:
Plant Physiology (Bethesda)
Additional Journal Information:
Journal Name: Plant Physiology (Bethesda); Journal Volume: 169; Journal Issue: 2; Journal ID: ISSN 0032-0889
Publisher:
American Society of Plant Biologists
Research Org:
Univ. of California, San Diego, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF); National Institutes of Health (NIH)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES
OSTI Identifier:
1411720