Reactive Carbonyl Species Mediate Methyl Jasmonate-Induced Stomatal Closure

Abstract

Production of reactive oxygen species (ROS) is a key signal event for methyl jasmonate (MeJA)- and abscisic acid (ABA)-induced stomatal closure. We recently showed that reactive carbonyl species (RCS) stimulates stomatal closure as an intermediate downstream of hydrogen peroxide (H2O2) production in the ABA signaling pathway in guard cells of Nicotiana tabacum and Arabidopsis thaliana. In this study, we examined whether RCS functions as an intermediate downstream of H2O2 production in MeJA signaling in guard cells using transgenic tobacco plants overexpressing A. thaliana 2-alkenal reductase (n-alkanal + NAD(P)+ ⇌ 2-alkenal + NAD(P)H + H+) (AER-OE tobacco) and Arabidopsis plants. The stomatal closure induced by MeJA was impaired in the AER-OE tobacco and was inhibited by RCS scavengers, carnosine and pyridoxamine, in the wild-type (WT) tobacco plants and Arabidopsis plants. Application of MeJA significantly induced accumulation of RCS including acrolein and 4-hydroxy-(E)-2-nonenal in the WT tobacco but not in the AER-OE plants. Application of MeJA induced H2O2 production in the WT tobacco and the AER-OE plants and the H2O2 production was not inhibited by the RCS scavengers. These results suggest that RCS functions as an intermediate downstream of ROS production in MeJA signaling as well as in ABA signaling in guard cells.

Protein Carbonylation: Emerging Roles in Plant Redox Biology and Future Prospects

“…GSH is thus required downstream of ROS. Consistently, RCS production triggered by MeJA induced GSH depletion in guard cells [ 19 ], indicating that RCS targets likely lie downstream of H 2 O 2 production by RbohD and RbohF proteins in the guard cells.…”

“…Similar to ABA-induced stomatal closure, the production of ROS by NAD(P)H oxidases is also required by MeJA-induced stomatal closure in A. thaliana guard cells [ 182 , 183 , 184 , 185 , 186 ]. As with ABA, the application of MeJA induced the accumulation of RCS such as acrolein and HNE in WT tobacco plants, thus implicating RCS in MeJA-induced stomatal closure [ 19 ]. A study by Akter and colleagues revealed that stomatal closure induced by MeJA is accompanied by depletion in the level of intracellular GSH found in Arabidopsis guard cells [ 187 ], but no effect of GSH was found in MeJA-induced ROS production [ 188 ].…”

“…Exogenous application of the RCS acrolein was more effective at raising the level of [Ca 2+ ]cyt and inducing stomatal closure than exogenous H 2 O 2 application [ 181 ]. Similarly, RCS-mediated [Ca 2+ ]cyt increase was negatively regulated by GSH [ 19 ]. These suggest that GSH acts downstream of H 2 O 2 and RCS most likely by scavenging RCS to prevent them from reacting with protein targets.…”

“…GSH is a negative regulator of ABA or MeJA signaling in the guard cell-induced stomatal closure by depletion of intracellular levels of GSH. This model is based on the previous studies from the literature [ 18 , 19 , 181 , 187 , 188 , 190 , 191 , 193 ].…”

“…However, unlike protein ubiquitinylation or phosphorylation, protein carbonylation cannot be undone. Although recent genetic studies pointed to the transduction of ROS and phytohormone signals by protein carbonylation [ 16 , 17 , 18 , 19 ], it is still unclear how cells would control protein carbonylation in time and space similarly to ubiquitinylation or phosphorylation. The non-enzymatic feature of the carbonylation reaction and the fact that various endogenous lipid peroxidation-derived molecules can form adducts on proteins (see below) have considerably slowed the efforts to identify the functions regulated by protein carbonylation in plants.…”