Exogenous Hydrogen Peroxide Contributes to Heme Oxygenase-1 Delaying Programmed Cell Death in Isolated Aleurone Layers of Rice Subjected to Drought Stress in a cGMP-Dependent Manner

Abstract

Hydrogen peroxide (H2O2) is a reactive oxygen species (ROS) that plays a dual role in plant cells. Here, we discovered that drought (20% polyethylene glycol-6000, PEG)-triggered decreases of HO-1 transcript expression and HO activity. However, exogenous H2O2 contributed toward the increase in HO-1 gene expression and activity of the enzyme under drought stress. Meanwhile, the HO-1 inducer hematin could mimic the effects of the H2O2 scavengers ascorbic acid (AsA) and dimethylthiourea (DMTU) and the H2O2 synthesis inhibitor diphenyleneiodonium (DPI) for scavenging or diminishing drought-induced endogenous H2O2. Conversely, the zinc protoporphyrin IX (ZnPPIX), an HO-1-specific inhibitor, reversed the effects of hematin. We further analyzed the endogenous H2O2 levels and HO-1 transcript expression levels of aleurone layers treated with AsA, DMTU, and DPI in the presence of exogenous H2O2 under drought stress, respectively. The results showed that in aleurone layers subjected to drought stress, when the endogenous H2O2 level was inhibited, the effect of exogenous H2O2 on the induction of HO-1 was enhanced. Furthermore, exogenous H2O2-activated HO-1 effectively enhanced amylase activity. Application of 8-bromoguanosine 3′,5′-cyclic guanosine monophosphate (8-Br-cGMP) (the membrane permeable cGMP analog) promoted the effect of exogenous H2O2-delayed PCD of aleurone layers in response to drought stress. More importantly, HO-1 delayed the programmed cell death (PCD) of aleurone layers by cooperating with nitric oxide (NO), and the delayed effect of NO on PCD was achieved via mediation by cGMP under drought stress. In short, in rice aleurone layers, exogenous H2O2 (as a signaling molecule) triggered HO-1 and delayed PCD via cGMP which possibly induced amylase activity under drought stress. In contrast, as a toxic by-product of cellular metabolism, the drought-generated H2O2 promoted cell death.

DNA damage and reactive oxygen species cause cell death in the rice local lesions 1 mutant under high light and high temperature

“…DMTU and AsA are commonly used as H 2 O 2 scavengers (Casano et al ., ; Wang & Kao, ; Wang et al ., ). To investigate whether the accumulation of ROS plays a crucial role in the local lesions phenotype of the ls1 mutant, ls1 plants were treated with 1 mM AsA or 5 mM DMTU when they were transferred from the N22 condition to the H32 condition at the two‐leaf stage.…”

“…The ls1 plants at the two‐leaf stage were treated with 1 mM AsA (Macklin) or 5 mM dimethythiourea (DMTU) (Macklin), after which they were transferred from the N22 to H32 condition (Casano et al ., ; Wang & Kao, ; Wang et al ., ). The ls1 mutant seedlings without antioxidant treatment were used as the control (CK/ ls1 ).…”

Ectopic Expression of Grapevine Gene VaRGA1 in Arabidopsis Improves Resistance to Downy Mildew and Pseudomonas syringae pv. tomato DC3000 But Increases Susceptibility to Botrytis cinerea

“…NBS-LRR genes can recognize the effectors secreted by biotrophic pathogens to mediate resistance [36]. They usually cause hypersensitivity in the place of infection, followed by ROS production, accumulation of plant hormones related to disease resistance, expression of defense-related genes, and phytophane synthesis [51,52]. The production of ROS is a necessary condition for cell death, which can restrict biotrophic pathogens from obtaining nutrients from plants [53,54].…”

Improving crop drought resistance with plant growth regulators and rhizobacteria: Mechanisms, applications, and perspectives

“…(2019) GlyBet sweet potato ( Ipomoea batatas ) maintained osmotic potential Tisarum et al. (2020) H 2 O 2 rice ( Oryza sativa L.) induced amylase activity under drought stress Wang et al. (2018) NO/GSNO sugarcane ( Saccharum spp.)…”

“…H 2 O 2 is an ROS that plays a dual role in plant cells. In rice aleurone layers, exogenous H 2 O 2 (as a signaling molecule) triggered heme oxygenase-1 (HO-1, EC.1.14.99.3) and delayed programmed cell death via cyclic guanosine monophosphate, which possibly induced amylase activity under drought stress ( Wang et al., 2018 ). In addition, β-cyclocitral (the main oxidation product of β-carotene), β-sitosterol, ascorbic acid, GSNO (the main NO reservoir in cells), NO, glycine betaine, and PopW (a hairpin protein from Ralstonia solanacearum ZJ3721) have been shown to maintain plant photosynthesis and RWC and to promote osmotic adjustment and antioxidant defense, thereby enhancing plant drought resistance ( Latif et al., 2016 ; Silveira et al., 2016 ; Elkeilsh et al., 2019 ; Deshpande et al., 2020 ; Rasheed et al., 2020 ; Tisarum et al., 2020 ; Zhou et al., 2020 ).…”