A Dominant Mutation in the HT1 Kinase Uncovers Roles of MAP Kinases and GHR1 in CO2-Induced Stomatal Closure.
Activation of the guard cell S-type anion channel SLAC1 is important for stomatal closure in response to diverse stimuli, including elevated CO2The majority of known SLAC1 activation mechanisms depend on abscisic acid (ABA) signaling. Several lines of evidence point to a parallel ABA-independent mechanism of CO2-induced stomatal regulation; however, molecular details of this pathway remain scarce. Here, we isolated a dominant mutation in the protein kinase HIGH LEAF TEMPERATURE1 (HT1), an essential regulator of stomatal CO2responses, in an ozone sensitivity screen of Arabidopsis thaliana The mutation caused constitutively open stomata and impaired stomatal CO2responses. We show that the mitogen-activated protein kinases (MPKs) MPK4 and MPK12 can inhibit HT1 activity in vitro and this inhibition is decreased for the dominant allele of HT1. We also show that HT1 inhibits the activation of the SLAC1 anion channel by the protein kinases OPEN STOMATA1 and GUARD CELL HYDROGEN PEROXIDE-RESISTANT1 (GHR1) in Xenopus laevis oocytes. Notably, MPK12 can restore SLAC1 activation in the presence of HT1, but not in the presence of the dominant allele of HT1. Based on these data, we propose a model for sequential roles of MPK12, HT1, and GHR1 in the ABA-independent regulation of SLAC1 during CO2-induced stomatal closure.
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Hanna
0000-0002-6392-859X
H
Hõrak
Division of Plant Biology, Viikki Plant Science Centre, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Maija
M
Sierla
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Kadri
K
Tõldsepp
Division of Biological Sciences, Cell and Developmental Biology Section, University of California San Diego, La Jolla, California 92093-0116.
Cun
0000-0001-6975-0959
C
Wang
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Yuh-Shuh
YS
Wang
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Maris
M
Nuhkat
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Ervin
E
Valk
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Priit
P
Pechter
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Ebe
E
Merilo
Division of Plant Biology, Viikki Plant Science Centre, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Jarkko
0000-0002-4096-6278
J
Salojärvi
Division of Plant Biology, Viikki Plant Science Centre, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Kirk
0000-0002-7398-3453
K
Overmyer
Institute of Technology, University of Tartu, Tartu 50411, Estonia.
Mart
M
Loog
Institute of Technology, University of Tartu, Tartu 50411, Estonia.|Division of Plant Biology, Viikki Plant Science Centre, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.
Mikael
0000-0002-1135-2496
M
Brosché
Division of Biological Sciences, Cell and Developmental Biology Section, University of California San Diego, La Jolla, California 92093-0116.
Julian I
0000-0002-3283-5972
JI
Schroeder
Division of Plant Biology, Viikki Plant Science Centre, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland.|Distinguished Scientist Fellowship Program, College of Science, King Saud University, Riyadh 11451, Saudi Arabia.
Jaakko
0000-0002-8959-1809
J
Kangasjärvi
Institute of Technology, University of Tartu, Tartu 50411, Estonia hannes.kollist@ut.ee.
Hannes
0000-0002-6895-3583
H
Kollist
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002245:Carbon Dioxide / Q000378:metabolism; D008565:Membrane Proteins / Q000235:genetics / Q000378:metabolism; D020928:Mitogen-Activated Protein Kinases / Q000235:genetics / Q000378:metabolism*; D009154:Mutation / Q000235:genetics; D054046:Plant Stomata / Q000235:genetics / Q000378:metabolism*; D011494:Protein Kinases / Q000235:genetics / Q000378:metabolism*; D015398:Signal Transduction / Q000235:genetics / Q000502:physiology
D029681:Arabidopsis Proteins; D008565:Membrane Proteins; C528438:SLAC1 protein, Arabidopsis; D002245:Carbon Dioxide; C000610355:HT1 protein, Arabidopsis; D011494:Protein Kinases; C576574:GHR1 protein, Arabidopsis; C472139:OST1 protein, Arabidopsis; C583609:MPK12 protein, Arabidopsis; D020928:Mitogen-Activated Protein Kinases
Plant Cell. 2008 Dec;20(12):3210-26
19114538
Mol Plant. 2015 Apr;8(4):657-9
25620768
Nature. 2008 Mar 27;452(7186):483-6
18305482
Proc Natl Acad Sci U S A. 2013 May 14;110(20):8296-301
23630285
Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21419-24
19955427
Plant Cell. 2009 Oct;21(10):3170-84
19855047
Plant Cell. 2002 Dec;14(12):3089-99
12468729
Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17588-93
19805022
Science. 2009 May 22;324(5930):1068-71
19407142
Curr Biol. 2015 Oct 19;25(20):2709-16
26455301
Plant J. 2008 Aug;55(4):698-708
18452588
Nat Commun. 2015 Jan 20;6:6057
25599916
Plant Cell. 2012 Jun;24(6):2546-61
22730405
Plant Physiol. 2014 May;165(1):15-29
24647477
Plant Cell Environ. 2010 Jun;33(6):914-25
20082669
New Phytol. 2015 Dec;208(4):1126-37
26192339
Plant Cell. 2000 Oct;12(10):1849-62
11041881
Plant J. 1998 Dec;16(6):735-43
10069079
Nature. 2009 Dec 3;462(7273):660-4
19924127
PLoS Biol. 2016 Dec 6;14(12):e2000322
27923039
Plant Cell. 2016 Feb;28(2):557-67
26764376
Plant J. 2010 May;62(3):442-53
20128877
Trends Plant Sci. 2002 Jul;7(7):301-8
12119167
Cell. 2000 Dec 22;103(7):1111-20
11163186
Proc Natl Acad Sci U S A. 2014 Feb 18;111(7):2836-41
24550314
Proc Natl Acad Sci U S A. 2009 Mar 31;106(13):5412-7
19279211
New Phytol. 2014 Jul;203(1):44-62
24800691
Plant Physiol. 2013 Jul;162(3):1652-68
23703845
Plant Physiol. 2015 Oct;169(2):1168-78
26243620
Plant Physiol. 2003 Oct;133(2):462-9
14555774
Nucleic Acids Res. 2006;34(18):e122
17000637
Annu Rev Plant Biol. 2010;61:621-49
20441529
Sci Signal. 2011 May 17;4(173):ra32
21586729
Nat Cell Biol. 2010 Jan;12(1):87-93; sup pp 1-18
20010812
Proc Natl Acad Sci U S A. 2010 Apr 27;107(17):8023-8
20385816
Nat Cell Biol. 2006 Apr;8(4):391-7
16518390
Cell Motil Cytoskeleton. 2004 Oct;59(2):79-93
15362112
Proc Natl Acad Sci U S A. 2012 Jun 26;109(26):10593-8
22689970
J Exp Bot. 2016 May;67(11):3251-61
27034327
Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21425-30
19955405
Plant Cell Environ. 2008 Sep;31(9):1237-49
18518918
Curr Biol. 2009 Feb 10;19(3):229-34
19185498
EMBO J. 2011 Apr 20;30(8):1645-58
21423149
Nature. 2008 Mar 27;452(7186):487-91
18305484
Science. 2009 May 22;324(5930):1064-8
19407143
Nat Methods. 2012 Jul;9(7):671-5
22930834
Proc Natl Acad Sci U S A. 2009 Dec 1;106(48):20520-5
19910530
Plant J. 2006 Aug;47(4):532-46
16813576
Plant Cell. 2012 Oct;24(10):4281-93
23115249
Plant Cell. 2016 Feb;28(2):568-82
26764375