Guard cell hydrogen peroxide and nitric oxide mediate elevated CO₂‐induced stomatal movement in tomato

Abstract

SummaryClimate change as a consequence of increasing atmospheric CO 2 influences plant photosynthesis and transpiration. Although the involvement of stomata in plant responses to elevated CO 2 has been well established, the underlying mechanism of elevated CO 2 -induced stomatal movement remains largely unknown.We used diverse techniques, including laser scanning confocal microscopy, transmission electron microscopy, biochemical methodologies and gene silencing to investigate the signaling pathway for elevated CO 2 -induced stomatal movement in tomato (Solanum lycopersicum).Elevated CO 2 -induced stomatal closure was dependent on the production of RESPIRATORY BURST OXIDASE 1 (RBOH1)-mediated hydrogen peroxide (H 2 O 2 ) and NITRATE REDUCTASE (NR)-mediated nitric oxide (NO) in guard cells in an abscisic acid (ABA)-independent manner. Silencing of OPEN STOMATA 1 (OST1) compromised the elevated CO 2 -induced accumulation of H 2 O 2 and NO, upregulation of SLOW ANION CHANNEL ASSOCIATED 1 (SLAC1) gene expression and reduction of stomatal aperture, whereas silencing of RBOH1 or NR had no effects on the expression of OST1.Our results demonstrate that as critical signaling molecules, RBOH1-dependent H 2 O 2 and NR-dependent NO act downstream of OST1 that regulate SLAC1 expression and elevated CO 2 -induced stomatal movement. This information is crucial to deepen the understanding of CO 2 signaling pathway in guard cells.

Reactive oxygen species signaling and stomatal movement in plant responses to drought stress and pathogen attack

“…Silencing of OST1 and RBOH1 in tomato reduces H 2 O 2 and NO accumulation in response to elevated CO 2 levels, whereas silencing NR only reduces the accumulation of NO. These findings indicate that OST1 and NADPH oxidase‐dependent H 2 O 2 production act upstream of NO production during CO 2 signaling in guard cells (Shi et al ). Together, these findings suggest that ABA and ROS signaling are required to enhance high CO 2 ‐induced stomatal closure.…”

A novel CO2‐responsive systemic signaling pathway controlling plant mycorrhizal symbiosis

“…Hence, eCO 2 alters cellular redox homeostasis as discussed previously (Mhamdi and Noctor, 2016). In addition, RBOH‐mediated ROS production facilitates lateral root emergence in Arabidopsis (Shi et al ., ; Orman‐Ligeza et al ., ). The data presented here demonstrates that RBOH1 expression in the roots of WT/ rboh1 plants had little effect on arbuscular mycorrhizal symbiosis and P uptake in response to changes in the concentration of atmospheric CO 2 compared to rboh /WT plants (Figs e,f, S6c, S7).…”

Reactive oxygen species signaling and stomatal movement: Current updates and future perspectives

“…OST1 also interacts and phosphorylates with plasma membrane-bound N terminus of respiratory burst oxidase homolog D (RBOHD) and F (RBOHF) protein and in the guard cells of ost1 knockout mutant, the ABA-induced ROS generation is eliminated thereby suggesting that OST1 catalyzes ROS production (H 2 O 2 ) mediated by NADPH oxidase [33], [34]. Recently, Shi et al [35] reported that OST1 compromised the CO 2 -induced H 2 O 2 and NO accumulation, upregulation of SLAC1 expression, and reduced stomatal aperture.…”