Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO 2 signal transduction in guard cell

Handle URI:
http://hdl.handle.net/10754/597745
Title:
Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO 2 signal transduction in guard cell
Authors:
Xue, Shaowu; Hu, Honghong; Ries, Amber; Merilo, Ebe; Kollist, Hannes; Schroeder, Julian I
Abstract:
Plants respond to elevated CO(2) via carbonic anhydrases that mediate stomatal closing, but little is known about the early signalling mechanisms following the initial CO(2) response. It remains unclear whether CO(2), HCO(3)(-) or a combination activates downstream signalling. Here, we demonstrate that bicarbonate functions as a small-molecule activator of SLAC1 anion channels in guard cells. Elevated intracellular [HCO(3)(-)](i) with low [CO(2)] and [H(+)] activated S-type anion currents, whereas low [HCO(3)(-)](i) at high [CO(2)] and [H(+)] did not. Bicarbonate enhanced the intracellular Ca(2+) sensitivity of S-type anion channel activation in wild-type and ht1-2 kinase mutant guard cells. ht1-2 mutant guard cells exhibited enhanced bicarbonate sensitivity of S-type anion channel activation. The OST1 protein kinase has been reported not to affect CO(2) signalling. Unexpectedly, OST1 loss-of-function alleles showed strongly impaired CO(2)-induced stomatal closing and HCO(3)(-) activation of anion channels. Moreover, PYR/RCAR abscisic acid (ABA) receptor mutants slowed but did not abolish CO(2)/HCO(3)(-) signalling, redefining the convergence point of CO(2) and ABA signalling. A new working model of the sequence of CO(2) signalling events in gas exchange regulation is presented.
Citation:
Xue S, Hu H, Ries A, Merilo E, Kollist H, et al. (2011) Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO 2 signal transduction in guard cell . The EMBO Journal 30: 1645–1658. Available: http://dx.doi.org/10.1038/emboj.2011.68.
Publisher:
Wiley-Blackwell
Journal:
The EMBO Journal
KAUST Grant Number:
KUS-F1-021-31
Issue Date:
18-Mar-2011
DOI:
10.1038/emboj.2011.68
PubMed ID:
21423149
PubMed Central ID:
PMC3102275
Type:
Article
ISSN:
0261-4189
Sponsors:
We thank Dr Cawas Engineer and Dr Rama Vaidyanathan for critical reading of the manuscript and Dr Kristiina Laanements for confirmation of whole-plant gas exchange data in the Ler ost1 mutants. We also thank Drs Nan Sang, Yanxi Pei and Shuqing Zhao for help during revision of the manuscript. This work was supported by grants from the National Science Foundation (MCB0918220), the National Institutes of Health (GM060396), Bayer Crop Sciences, the Chemical Sciences, Geosciences, and Biosciences Division of the Office of Basic Energy Sciences at the US Department of Energy (DOE-DE-FG02-03ER15449) and the Human Frontiers in Science Program to JIS and a fellowship from the King Abdullah University of Science and Technology (KAUST; No. KUS-F1-021-31) to HH, and in part supported by grants from the National Science Foundation of China (20701028) to SX and from the Estonian Science Foundation 7763 and SF0180071S07 to HK.
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Full metadata record

DC FieldValue Language
dc.contributor.authorXue, Shaowuen
dc.contributor.authorHu, Honghongen
dc.contributor.authorRies, Amberen
dc.contributor.authorMerilo, Ebeen
dc.contributor.authorKollist, Hannesen
dc.contributor.authorSchroeder, Julian Ien
dc.date.accessioned2016-02-25T12:55:57Zen
dc.date.available2016-02-25T12:55:57Zen
dc.date.issued2011-03-18en
dc.identifier.citationXue S, Hu H, Ries A, Merilo E, Kollist H, et al. (2011) Central functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO 2 signal transduction in guard cell . The EMBO Journal 30: 1645–1658. Available: http://dx.doi.org/10.1038/emboj.2011.68.en
dc.identifier.issn0261-4189en
dc.identifier.pmid21423149en
dc.identifier.doi10.1038/emboj.2011.68en
dc.identifier.urihttp://hdl.handle.net/10754/597745en
dc.description.abstractPlants respond to elevated CO(2) via carbonic anhydrases that mediate stomatal closing, but little is known about the early signalling mechanisms following the initial CO(2) response. It remains unclear whether CO(2), HCO(3)(-) or a combination activates downstream signalling. Here, we demonstrate that bicarbonate functions as a small-molecule activator of SLAC1 anion channels in guard cells. Elevated intracellular [HCO(3)(-)](i) with low [CO(2)] and [H(+)] activated S-type anion currents, whereas low [HCO(3)(-)](i) at high [CO(2)] and [H(+)] did not. Bicarbonate enhanced the intracellular Ca(2+) sensitivity of S-type anion channel activation in wild-type and ht1-2 kinase mutant guard cells. ht1-2 mutant guard cells exhibited enhanced bicarbonate sensitivity of S-type anion channel activation. The OST1 protein kinase has been reported not to affect CO(2) signalling. Unexpectedly, OST1 loss-of-function alleles showed strongly impaired CO(2)-induced stomatal closing and HCO(3)(-) activation of anion channels. Moreover, PYR/RCAR abscisic acid (ABA) receptor mutants slowed but did not abolish CO(2)/HCO(3)(-) signalling, redefining the convergence point of CO(2) and ABA signalling. A new working model of the sequence of CO(2) signalling events in gas exchange regulation is presented.en
dc.description.sponsorshipWe thank Dr Cawas Engineer and Dr Rama Vaidyanathan for critical reading of the manuscript and Dr Kristiina Laanements for confirmation of whole-plant gas exchange data in the Ler ost1 mutants. We also thank Drs Nan Sang, Yanxi Pei and Shuqing Zhao for help during revision of the manuscript. This work was supported by grants from the National Science Foundation (MCB0918220), the National Institutes of Health (GM060396), Bayer Crop Sciences, the Chemical Sciences, Geosciences, and Biosciences Division of the Office of Basic Energy Sciences at the US Department of Energy (DOE-DE-FG02-03ER15449) and the Human Frontiers in Science Program to JIS and a fellowship from the King Abdullah University of Science and Technology (KAUST; No. KUS-F1-021-31) to HH, and in part supported by grants from the National Science Foundation of China (20701028) to SX and from the Estonian Science Foundation 7763 and SF0180071S07 to HK.en
dc.publisherWiley-Blackwellen
dc.subjectabscisic aciden
dc.subjectbicarbonateen
dc.subjectcalciumen
dc.subjectcarbon dioxideen
dc.subjectstomatal conductanceen
dc.titleCentral functions of bicarbonate in S-type anion channel activation and OST1 protein kinase in CO 2 signal transduction in guard cellen
dc.typeArticleen
dc.identifier.journalThe EMBO Journalen
dc.identifier.pmcidPMC3102275en
dc.contributor.institutionDivision of Biological Sciences, Cell and Developmental Biology Section, University of California, San Diego, La Jolla, CA, USA.en
kaust.grant.numberKUS-F1-021-31en

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