Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells

Handle URI:
http://hdl.handle.net/10754/597733
Title:
Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells
Authors:
Hu, Honghong; Boisson-Dernier, Aurélien; Israelsson-Nordström, Maria; Böhmer, Maik; Xue, Shaowu; Ries, Amber; Godoski, Jan; Kuhn, Josef M.; Schroeder, Julian I.
Abstract:
The continuing rise in atmospheric CO2 causes stomatal pores in leaves to close and thus globally affects CO2 influx into plants, water use efficiency and leaf heat stress. However, the CO2-binding proteins that control this response remain unknown. Moreover, which cell type responds to CO2, mesophyll or guard cells, and whether photosynthesis mediates this response are matters of debate. We demonstrate that Arabidopsis thaliana double-mutant plants in the beta-carbonic anhydrases betaCA1 and betaCA4 show impaired CO2-regulation of stomatal movements and increased stomatal density, but retain functional abscisic-acid and blue-light responses. betaCA-mediated CO2-triggered stomatal movements are not, in first-order, linked to whole leaf photosynthesis and can function in guard cells. Furthermore, guard cell betaca-overexpressing plants exhibit instantaneous enhanced water use efficiency. Guard cell expression of mammalian alphaCAII complements the reduced sensitivity of ca1 ca4 plants, showing that carbonic anhydrase-mediated catalysis is an important mechanism for betaCA-mediated CO2-induced stomatal closure and patch clamp analyses indicate that CO2/HCO3- transfers the signal to anion channel regulation. These findings, together with ht1-2 (ref. 9) epistasis analysis demonstrate that carbonic anhydrases function early in the CO2 signalling pathway, which controls gas-exchange between plants and the atmosphere.
Citation:
Hu H, Boisson-Dernier A, Israelsson-Nordström M, Böhmer M, Xue S, et al. (2009) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12: 87–93. Available: http://dx.doi.org/10.1038/ncb2009.
Publisher:
Springer Nature
Journal:
Nature Cell Biology
KAUST Grant Number:
KUS-F1-021-31
Issue Date:
13-Dec-2009
DOI:
10.1038/ncb2009
PubMed ID:
20010812
PubMed Central ID:
PMC2906259
Type:
Article
ISSN:
1465-7392; 1476-4679
Sponsors:
We thank M. Maktabi, J. Young and C. Engineer for preliminary analyses of aca mutants, R. Xu for assistance, S. Zeeman for suggestions and K. Iba (Kyushu University, Japan) for providing ht1-2 seeds. This research was supported by NSF (MCB0918220), NIH (GM060396) and in part by DOE (DE-FG02-03ER15449) grants (to J. I. S.) and by fellowships from the Swedish Research Council Formas (to M. I. -N.), the Deutsche Forschungsgemeinschaft (to M. B.), EMBO (to J. M. K.) and in part from the King Abdullah University of Science and Technology (KAUST; No. KUS-F1-021-31 to H. H.).
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Full metadata record

DC FieldValue Language
dc.contributor.authorHu, Honghongen
dc.contributor.authorBoisson-Dernier, Aurélienen
dc.contributor.authorIsraelsson-Nordström, Mariaen
dc.contributor.authorBöhmer, Maiken
dc.contributor.authorXue, Shaowuen
dc.contributor.authorRies, Amberen
dc.contributor.authorGodoski, Janen
dc.contributor.authorKuhn, Josef M.en
dc.contributor.authorSchroeder, Julian I.en
dc.date.accessioned2016-02-25T12:55:45Zen
dc.date.available2016-02-25T12:55:45Zen
dc.date.issued2009-12-13en
dc.identifier.citationHu H, Boisson-Dernier A, Israelsson-Nordström M, Böhmer M, Xue S, et al. (2009) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12: 87–93. Available: http://dx.doi.org/10.1038/ncb2009.en
dc.identifier.issn1465-7392en
dc.identifier.issn1476-4679en
dc.identifier.pmid20010812en
dc.identifier.doi10.1038/ncb2009en
dc.identifier.urihttp://hdl.handle.net/10754/597733en
dc.description.abstractThe continuing rise in atmospheric CO2 causes stomatal pores in leaves to close and thus globally affects CO2 influx into plants, water use efficiency and leaf heat stress. However, the CO2-binding proteins that control this response remain unknown. Moreover, which cell type responds to CO2, mesophyll or guard cells, and whether photosynthesis mediates this response are matters of debate. We demonstrate that Arabidopsis thaliana double-mutant plants in the beta-carbonic anhydrases betaCA1 and betaCA4 show impaired CO2-regulation of stomatal movements and increased stomatal density, but retain functional abscisic-acid and blue-light responses. betaCA-mediated CO2-triggered stomatal movements are not, in first-order, linked to whole leaf photosynthesis and can function in guard cells. Furthermore, guard cell betaca-overexpressing plants exhibit instantaneous enhanced water use efficiency. Guard cell expression of mammalian alphaCAII complements the reduced sensitivity of ca1 ca4 plants, showing that carbonic anhydrase-mediated catalysis is an important mechanism for betaCA-mediated CO2-induced stomatal closure and patch clamp analyses indicate that CO2/HCO3- transfers the signal to anion channel regulation. These findings, together with ht1-2 (ref. 9) epistasis analysis demonstrate that carbonic anhydrases function early in the CO2 signalling pathway, which controls gas-exchange between plants and the atmosphere.en
dc.description.sponsorshipWe thank M. Maktabi, J. Young and C. Engineer for preliminary analyses of aca mutants, R. Xu for assistance, S. Zeeman for suggestions and K. Iba (Kyushu University, Japan) for providing ht1-2 seeds. This research was supported by NSF (MCB0918220), NIH (GM060396) and in part by DOE (DE-FG02-03ER15449) grants (to J. I. S.) and by fellowships from the Swedish Research Council Formas (to M. I. -N.), the Deutsche Forschungsgemeinschaft (to M. B.), EMBO (to J. M. K.) and in part from the King Abdullah University of Science and Technology (KAUST; No. KUS-F1-021-31 to H. H.).en
dc.publisherSpringer Natureen
dc.titleCarbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cellsen
dc.typeArticleen
dc.identifier.journalNature Cell Biologyen
dc.identifier.pmcidPMC2906259en
dc.contributor.institutionDivision of Biological Sciences, Cell and Developmental Biology Section, University of California San Diego, La Jolla, CA 92093-0116, USA.en
kaust.grant.numberKUS-F1-021-31en

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