Ethylene Inhibits Methyl Jasmonate-Induced Stomatal Closure by Modulating Guard Cell Slow-Type Anion Channel Activity via the OPEN STOMATA 1/SnRK2.6 Kinase-Independent Pathway in Arabidopsis

Shintaro Munemasa, Yukari Hirao, Kasumi Tanami, Yoshiharu Mimata, Yoshimasa Nakamura, Yoshiyuki Murata

Research output: Contribution to journalArticle

Abstract

Signal crosstalk between jasmonate and ethylene is crucial for a proper maintenance of defense responses and development. Although previous studies reported that both jasmonate and ethylene also function as modulators of stomatal movements, the signal crosstalk mechanism in stomatal guard cells remains unclear. Here, we show that the ethylene signaling inhibits jasmonate signaling as well as abscisic acid (ABA) signaling in guard cells of Arabidopsis thaliana and reveal the signaling crosstalk mechanism. Both an ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and an ethylene-releasing compound ethephon induced transient stomatal closure, and also inhibited methyl jasmonate (MeJA)-induced stomatal closure as well as ABA-induced stomatal closure. The ethylene inhibition of MeJA-induced stomatal closure was abolished in the ethylene-insensitive mutant etr1-1, whereas MeJA-induced stomatal closure was impaired in the ethylene-overproducing mutant eto1-1. Pretreatment with ACC inhibited MeJA-induced reactive oxygen species (ROS) production as well as ABA-induced ROS production in guard cells but did not suppress ABA activation of OPEN STOMATA 1 (OST1) kinase in guard cell-enriched epidermal peels. The whole-cell patch-clamp analysis revealed that ACC attenuated MeJA and ABA activation of S-type anion channels in guard cell protoplasts. However, MeJA and ABA inhibitions of Kin channels were not affected by ACC pretreatment. These results suggest that ethylene signaling inhibits MeJA signaling and ABA signaling by targeting S-type anion channels and ROS but not OST1 kinase and K+ channels in Arabidopsis guard cells.

Original languageEnglish
Pages (from-to)2263-2271
Number of pages9
JournalPlant and Cell Physiology
Volume60
Issue number10
DOIs
Publication statusPublished - Oct 1 2019

Fingerprint

methyl jasmonate
guard cells
Arabidopsis
Abscisic Acid
anions
Anions
ethylene
phosphotransferases (kinases)
Phosphotransferases
abscisic acid
1-aminocyclopropane-1-carboxylic acid
reactive oxygen species
Reactive Oxygen Species
ethylene releasers
pretreatment
stomatal movement
mutants
ethephon
potassium channels
Protoplasts

Keywords

  • Abscisic acid
  • Ethylene
  • Guard cell
  • Ion channel
  • Jasmonate
  • Stomata

ASJC Scopus subject areas

  • Physiology
  • Plant Science
  • Cell Biology

Cite this

@article{58fa722fd54a46fda8c421db90a187ad,
title = "Ethylene Inhibits Methyl Jasmonate-Induced Stomatal Closure by Modulating Guard Cell Slow-Type Anion Channel Activity via the OPEN STOMATA 1/SnRK2.6 Kinase-Independent Pathway in Arabidopsis",
abstract = "Signal crosstalk between jasmonate and ethylene is crucial for a proper maintenance of defense responses and development. Although previous studies reported that both jasmonate and ethylene also function as modulators of stomatal movements, the signal crosstalk mechanism in stomatal guard cells remains unclear. Here, we show that the ethylene signaling inhibits jasmonate signaling as well as abscisic acid (ABA) signaling in guard cells of Arabidopsis thaliana and reveal the signaling crosstalk mechanism. Both an ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and an ethylene-releasing compound ethephon induced transient stomatal closure, and also inhibited methyl jasmonate (MeJA)-induced stomatal closure as well as ABA-induced stomatal closure. The ethylene inhibition of MeJA-induced stomatal closure was abolished in the ethylene-insensitive mutant etr1-1, whereas MeJA-induced stomatal closure was impaired in the ethylene-overproducing mutant eto1-1. Pretreatment with ACC inhibited MeJA-induced reactive oxygen species (ROS) production as well as ABA-induced ROS production in guard cells but did not suppress ABA activation of OPEN STOMATA 1 (OST1) kinase in guard cell-enriched epidermal peels. The whole-cell patch-clamp analysis revealed that ACC attenuated MeJA and ABA activation of S-type anion channels in guard cell protoplasts. However, MeJA and ABA inhibitions of Kin channels were not affected by ACC pretreatment. These results suggest that ethylene signaling inhibits MeJA signaling and ABA signaling by targeting S-type anion channels and ROS but not OST1 kinase and K+ channels in Arabidopsis guard cells.",
keywords = "Abscisic acid, Ethylene, Guard cell, Ion channel, Jasmonate, Stomata",
author = "Shintaro Munemasa and Yukari Hirao and Kasumi Tanami and Yoshiharu Mimata and Yoshimasa Nakamura and Yoshiyuki Murata",
year = "2019",
month = "10",
day = "1",
doi = "10.1093/pcp/pcz121",
language = "English",
volume = "60",
pages = "2263--2271",
journal = "Plant and Cell Physiology",
issn = "0032-0781",
publisher = "Oxford University Press",
number = "10",

}

TY - JOUR

T1 - Ethylene Inhibits Methyl Jasmonate-Induced Stomatal Closure by Modulating Guard Cell Slow-Type Anion Channel Activity via the OPEN STOMATA 1/SnRK2.6 Kinase-Independent Pathway in Arabidopsis

AU - Munemasa, Shintaro

AU - Hirao, Yukari

AU - Tanami, Kasumi

AU - Mimata, Yoshiharu

AU - Nakamura, Yoshimasa

AU - Murata, Yoshiyuki

PY - 2019/10/1

Y1 - 2019/10/1

N2 - Signal crosstalk between jasmonate and ethylene is crucial for a proper maintenance of defense responses and development. Although previous studies reported that both jasmonate and ethylene also function as modulators of stomatal movements, the signal crosstalk mechanism in stomatal guard cells remains unclear. Here, we show that the ethylene signaling inhibits jasmonate signaling as well as abscisic acid (ABA) signaling in guard cells of Arabidopsis thaliana and reveal the signaling crosstalk mechanism. Both an ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and an ethylene-releasing compound ethephon induced transient stomatal closure, and also inhibited methyl jasmonate (MeJA)-induced stomatal closure as well as ABA-induced stomatal closure. The ethylene inhibition of MeJA-induced stomatal closure was abolished in the ethylene-insensitive mutant etr1-1, whereas MeJA-induced stomatal closure was impaired in the ethylene-overproducing mutant eto1-1. Pretreatment with ACC inhibited MeJA-induced reactive oxygen species (ROS) production as well as ABA-induced ROS production in guard cells but did not suppress ABA activation of OPEN STOMATA 1 (OST1) kinase in guard cell-enriched epidermal peels. The whole-cell patch-clamp analysis revealed that ACC attenuated MeJA and ABA activation of S-type anion channels in guard cell protoplasts. However, MeJA and ABA inhibitions of Kin channels were not affected by ACC pretreatment. These results suggest that ethylene signaling inhibits MeJA signaling and ABA signaling by targeting S-type anion channels and ROS but not OST1 kinase and K+ channels in Arabidopsis guard cells.

AB - Signal crosstalk between jasmonate and ethylene is crucial for a proper maintenance of defense responses and development. Although previous studies reported that both jasmonate and ethylene also function as modulators of stomatal movements, the signal crosstalk mechanism in stomatal guard cells remains unclear. Here, we show that the ethylene signaling inhibits jasmonate signaling as well as abscisic acid (ABA) signaling in guard cells of Arabidopsis thaliana and reveal the signaling crosstalk mechanism. Both an ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) and an ethylene-releasing compound ethephon induced transient stomatal closure, and also inhibited methyl jasmonate (MeJA)-induced stomatal closure as well as ABA-induced stomatal closure. The ethylene inhibition of MeJA-induced stomatal closure was abolished in the ethylene-insensitive mutant etr1-1, whereas MeJA-induced stomatal closure was impaired in the ethylene-overproducing mutant eto1-1. Pretreatment with ACC inhibited MeJA-induced reactive oxygen species (ROS) production as well as ABA-induced ROS production in guard cells but did not suppress ABA activation of OPEN STOMATA 1 (OST1) kinase in guard cell-enriched epidermal peels. The whole-cell patch-clamp analysis revealed that ACC attenuated MeJA and ABA activation of S-type anion channels in guard cell protoplasts. However, MeJA and ABA inhibitions of Kin channels were not affected by ACC pretreatment. These results suggest that ethylene signaling inhibits MeJA signaling and ABA signaling by targeting S-type anion channels and ROS but not OST1 kinase and K+ channels in Arabidopsis guard cells.

KW - Abscisic acid

KW - Ethylene

KW - Guard cell

KW - Ion channel

KW - Jasmonate

KW - Stomata

UR - http://www.scopus.com/inward/record.url?scp=85073183249&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85073183249&partnerID=8YFLogxK

U2 - 10.1093/pcp/pcz121

DO - 10.1093/pcp/pcz121

M3 - Article

C2 - 31241163

AN - SCOPUS:85073183249

VL - 60

SP - 2263

EP - 2271

JO - Plant and Cell Physiology

JF - Plant and Cell Physiology

SN - 0032-0781

IS - 10

ER -