The receptor-like pseudokinase GHR1 is required for stomatal closure

Maija Elina Sierla, Hanna Hõrak, Kirk Loren Overmyer, Cezary Marcin Waszczak, Dmitry Yarmolinsky, Tobias Maierhofer, Julia Vainonen, Konstantin Denessiouk, Jarkko Tapani Salojärvi, Kristiina Laanemets, Kadri Tõldsepp, Triin Vahisalu, Adrien Guy Bernard Gauthier, Tuomas Puukko, Lars Paulin, Petri Olli Viljami Auvinen, Dietmar Geiger, Rainer Hedrich, Hannes Kollist, Jaakko Sakari Kangasjärvi

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Guard cells control the aperture of stomatal pores to balance photosynthetic carbon dioxide uptake with evaporative water loss. Stomatal closure is triggered by several stimuli that initiate complex signaling networks to govern the activity of ion channels. Activation of SLOW ANION CHANNEL1 (SLAC1) is central to the process of stomatal closure and requires the leucine-rich repeat receptor-like kinase (LRR-RLK) GUARD CELL HYDROGEN PEROXIDE-RESISTANT1 (GHR1), among other signaling components. Here, based on functional analysis of nine Arabidopsis thaliana ghr1 mutant alleles identified in two independent forward-genetic ozone-sensitivity screens, we found that GHR1 is required for stomatal responses to apoplastic reactive oxygen species, abscisic acid, high CO2 concentrations, and diurnal light/dark transitions. Furthermore, we show that the amino acid residues of GHR1 involved in ATP binding are not required for stomatal closure in Arabidopsis or the activation of SLAC1 anion currents in Xenopus laevis oocytes and present supporting in silico and in vitro evidence suggesting that GHR1 is an inactive pseudokinase. Biochemical analyses suggested that GHR1-mediated activation of SLAC1 occurs via interacting proteins and that CALCIUM-DEPENDENT PROTEIN KINASE3 interacts with GHR1. We propose that GHR1 acts in stomatal closure as a scaffolding component.

Original languageEnglish
JournalPlant Cell
Volume30
Issue number11
Pages (from-to)2813-2837
Number of pages25
ISSN1040-4651
DOIs
Publication statusPublished - Nov 2018
MoE publication typeA1 Journal article-refereed

Fields of Science

  • 2C PROTEIN PHOSPHATASES
  • ABSCISIC-ACID
  • ANION CHANNEL SLAC1
  • ARABIDOPSIS
  • CELL-DEATH
  • HYDROGEN-PEROXIDE
  • KINASE BIK1
  • NADPH OXIDASE RBOHD
  • REDUCED AIR HUMIDITY
  • SIGNAL-TRANSDUCTION
  • 1182 Biochemistry, cell and molecular biology
  • 1183 Plant biology, microbiology, virology

Cite this

Sierla, Maija Elina ; Hõrak, Hanna ; Overmyer, Kirk Loren ; Waszczak, Cezary Marcin ; Yarmolinsky, Dmitry ; Maierhofer, Tobias ; Vainonen, Julia ; Denessiouk, Konstantin ; Salojärvi, Jarkko Tapani ; Laanemets, Kristiina ; Tõldsepp, Kadri ; Vahisalu, Triin ; Gauthier, Adrien Guy Bernard ; Puukko, Tuomas ; Paulin, Lars ; Auvinen, Petri Olli Viljami ; Geiger, Dietmar ; Hedrich, Rainer ; Kollist, Hannes ; Kangasjärvi, Jaakko Sakari. / The receptor-like pseudokinase GHR1 is required for stomatal closure. In: Plant Cell. 2018 ; Vol. 30, No. 11. pp. 2813-2837.
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title = "The receptor-like pseudokinase GHR1 is required for stomatal closure",
abstract = "Guard cells control the aperture of stomatal pores to balance photosynthetic carbon dioxide uptake with evaporative water loss. Stomatal closure is triggered by several stimuli that initiate complex signaling networks to govern the activity of ion channels. Activation of SLOW ANION CHANNEL1 (SLAC1) is central to the process of stomatal closure and requires the leucine-rich repeat receptor-like kinase (LRR-RLK) GUARD CELL HYDROGEN PEROXIDE-RESISTANT1 (GHR1), among other signaling components. Here, based on functional analysis of nine Arabidopsis thaliana ghr1 mutant alleles identified in two independent forward-genetic ozone-sensitivity screens, we found that GHR1 is required for stomatal responses to apoplastic reactive oxygen species, abscisic acid, high CO2 concentrations, and diurnal light/dark transitions. Furthermore, we show that the amino acid residues of GHR1 involved in ATP binding are not required for stomatal closure in Arabidopsis or the activation of SLAC1 anion currents in Xenopus laevis oocytes and present supporting in silico and in vitro evidence suggesting that GHR1 is an inactive pseudokinase. Biochemical analyses suggested that GHR1-mediated activation of SLAC1 occurs via interacting proteins and that CALCIUM-DEPENDENT PROTEIN KINASE3 interacts with GHR1. We propose that GHR1 acts in stomatal closure as a scaffolding component.",
keywords = "2C PROTEIN PHOSPHATASES, ABSCISIC-ACID, ANION CHANNEL SLAC1, ARABIDOPSIS, CELL-DEATH, HYDROGEN-PEROXIDE, KINASE BIK1, NADPH OXIDASE RBOHD, REDUCED AIR HUMIDITY, SIGNAL-TRANSDUCTION, 1182 Biochemistry, cell and molecular biology, 1183 Plant biology, microbiology, virology",
author = "Sierla, {Maija Elina} and Hanna H{\~o}rak and Overmyer, {Kirk Loren} and Waszczak, {Cezary Marcin} and Dmitry Yarmolinsky and Tobias Maierhofer and Julia Vainonen and Konstantin Denessiouk and Saloj{\"a}rvi, {Jarkko Tapani} and Kristiina Laanemets and Kadri T{\~o}ldsepp and Triin Vahisalu and Gauthier, {Adrien Guy Bernard} and Tuomas Puukko and Lars Paulin and Auvinen, {Petri Olli Viljami} and Dietmar Geiger and Rainer Hedrich and Hannes Kollist and Kangasj{\"a}rvi, {Jaakko Sakari}",
year = "2018",
month = "11",
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language = "English",
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pages = "2813--2837",
journal = "Plant Cell",
issn = "1040-4651",
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Sierla, ME, Hõrak, H, Overmyer, KL, Waszczak, CM, Yarmolinsky, D, Maierhofer, T, Vainonen, J, Denessiouk, K, Salojärvi, JT, Laanemets, K, Tõldsepp, K, Vahisalu, T, Gauthier, AGB, Puukko, T, Paulin, L, Auvinen, POV, Geiger, D, Hedrich, R, Kollist, H & Kangasjärvi, JS 2018, 'The receptor-like pseudokinase GHR1 is required for stomatal closure' Plant Cell, vol. 30, no. 11, pp. 2813-2837. https://doi.org/10.1105/tpc.18.00441

The receptor-like pseudokinase GHR1 is required for stomatal closure. / Sierla, Maija Elina; Hõrak, Hanna; Overmyer, Kirk Loren; Waszczak, Cezary Marcin; Yarmolinsky, Dmitry; Maierhofer, Tobias; Vainonen, Julia; Denessiouk, Konstantin; Salojärvi, Jarkko Tapani; Laanemets, Kristiina; Tõldsepp, Kadri; Vahisalu, Triin; Gauthier, Adrien Guy Bernard; Puukko, Tuomas ; Paulin, Lars; Auvinen, Petri Olli Viljami; Geiger, Dietmar; Hedrich, Rainer; Kollist, Hannes; Kangasjärvi, Jaakko Sakari.

In: Plant Cell, Vol. 30, No. 11, 11.2018, p. 2813-2837.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - The receptor-like pseudokinase GHR1 is required for stomatal closure

AU - Sierla, Maija Elina

AU - Hõrak, Hanna

AU - Overmyer, Kirk Loren

AU - Waszczak, Cezary Marcin

AU - Yarmolinsky, Dmitry

AU - Maierhofer, Tobias

AU - Vainonen, Julia

AU - Denessiouk, Konstantin

AU - Salojärvi, Jarkko Tapani

AU - Laanemets, Kristiina

AU - Tõldsepp, Kadri

AU - Vahisalu, Triin

AU - Gauthier, Adrien Guy Bernard

AU - Puukko, Tuomas

AU - Paulin, Lars

AU - Auvinen, Petri Olli Viljami

AU - Geiger, Dietmar

AU - Hedrich, Rainer

AU - Kollist, Hannes

AU - Kangasjärvi, Jaakko Sakari

PY - 2018/11

Y1 - 2018/11

N2 - Guard cells control the aperture of stomatal pores to balance photosynthetic carbon dioxide uptake with evaporative water loss. Stomatal closure is triggered by several stimuli that initiate complex signaling networks to govern the activity of ion channels. Activation of SLOW ANION CHANNEL1 (SLAC1) is central to the process of stomatal closure and requires the leucine-rich repeat receptor-like kinase (LRR-RLK) GUARD CELL HYDROGEN PEROXIDE-RESISTANT1 (GHR1), among other signaling components. Here, based on functional analysis of nine Arabidopsis thaliana ghr1 mutant alleles identified in two independent forward-genetic ozone-sensitivity screens, we found that GHR1 is required for stomatal responses to apoplastic reactive oxygen species, abscisic acid, high CO2 concentrations, and diurnal light/dark transitions. Furthermore, we show that the amino acid residues of GHR1 involved in ATP binding are not required for stomatal closure in Arabidopsis or the activation of SLAC1 anion currents in Xenopus laevis oocytes and present supporting in silico and in vitro evidence suggesting that GHR1 is an inactive pseudokinase. Biochemical analyses suggested that GHR1-mediated activation of SLAC1 occurs via interacting proteins and that CALCIUM-DEPENDENT PROTEIN KINASE3 interacts with GHR1. We propose that GHR1 acts in stomatal closure as a scaffolding component.

AB - Guard cells control the aperture of stomatal pores to balance photosynthetic carbon dioxide uptake with evaporative water loss. Stomatal closure is triggered by several stimuli that initiate complex signaling networks to govern the activity of ion channels. Activation of SLOW ANION CHANNEL1 (SLAC1) is central to the process of stomatal closure and requires the leucine-rich repeat receptor-like kinase (LRR-RLK) GUARD CELL HYDROGEN PEROXIDE-RESISTANT1 (GHR1), among other signaling components. Here, based on functional analysis of nine Arabidopsis thaliana ghr1 mutant alleles identified in two independent forward-genetic ozone-sensitivity screens, we found that GHR1 is required for stomatal responses to apoplastic reactive oxygen species, abscisic acid, high CO2 concentrations, and diurnal light/dark transitions. Furthermore, we show that the amino acid residues of GHR1 involved in ATP binding are not required for stomatal closure in Arabidopsis or the activation of SLAC1 anion currents in Xenopus laevis oocytes and present supporting in silico and in vitro evidence suggesting that GHR1 is an inactive pseudokinase. Biochemical analyses suggested that GHR1-mediated activation of SLAC1 occurs via interacting proteins and that CALCIUM-DEPENDENT PROTEIN KINASE3 interacts with GHR1. We propose that GHR1 acts in stomatal closure as a scaffolding component.

KW - 2C PROTEIN PHOSPHATASES

KW - ABSCISIC-ACID

KW - ANION CHANNEL SLAC1

KW - ARABIDOPSIS

KW - CELL-DEATH

KW - HYDROGEN-PEROXIDE

KW - KINASE BIK1

KW - NADPH OXIDASE RBOHD

KW - REDUCED AIR HUMIDITY

KW - SIGNAL-TRANSDUCTION

KW - 1182 Biochemistry, cell and molecular biology

KW - 1183 Plant biology, microbiology, virology

U2 - 10.1105/tpc.18.00441

DO - 10.1105/tpc.18.00441

M3 - Article

VL - 30

SP - 2813

EP - 2837

JO - Plant Cell

JF - Plant Cell

SN - 1040-4651

IS - 11

ER -