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

Shaowu Xue, Honghong Hu, Amber Ries, Ebe Merilo, Hannes Kollist, Julian I Schroeder

Research output: Contribution to journalArticlepeer-review

167 Scopus citations

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.
Original languageEnglish (US)
Pages (from-to)1645-1658
Number of pages14
JournalThe EMBO Journal
Volume30
Issue number8
DOIs
StatePublished - Mar 18 2011
Externally publishedYes

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledged KAUST grant number(s): KUS-F1-021-31
Acknowledgements: 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.
This publication acknowledges KAUST support, but has no KAUST affiliated authors.

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