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

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 g...

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Main Authors: Guanghui Wang, Yu Xiao, Xiaojiang Deng, Heting Zhang, Tingge Li, Huiping Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-02-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2018.00084/full
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author Guanghui Wang
Guanghui Wang
Yu Xiao
Yu Xiao
Xiaojiang Deng
Xiaojiang Deng
Heting Zhang
Heting Zhang
Tingge Li
Tingge Li
Huiping Chen
Huiping Chen
author_facet Guanghui Wang
Guanghui Wang
Yu Xiao
Yu Xiao
Xiaojiang Deng
Xiaojiang Deng
Heting Zhang
Heting Zhang
Tingge Li
Tingge Li
Huiping Chen
Huiping Chen
author_sort Guanghui Wang
collection DOAJ
description 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.
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spelling doaj.art-b7420a2d298b40b1ab601aea64bca0802022-12-21T20:03:05ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-02-01910.3389/fpls.2018.00084315395Exogenous 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 MannerGuanghui Wang0Guanghui Wang1Yu Xiao2Yu Xiao3Xiaojiang Deng4Xiaojiang Deng5Heting Zhang6Heting Zhang7Tingge Li8Tingge Li9Huiping Chen10Huiping Chen11Hainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, Hainan University, Haikou, ChinaInstitute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, Hainan University, Haikou, ChinaInstitute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, Hainan University, Haikou, ChinaInstitute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, Hainan University, Haikou, ChinaInstitute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, Hainan University, Haikou, ChinaInstitute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHainan Key Laboratory for Sustainable Utilization of Tropical Bioresource, Hainan University, Haikou, ChinaInstitute of Tropical Agriculture and Forestry, Hainan University, Haikou, ChinaHydrogen 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.http://journal.frontiersin.org/article/10.3389/fpls.2018.00084/fullhydrogen peroxide (H2O2)heme oxygenase-1 (HO-1)aleurone layercyclic guanosine monophosphate (cGMP)drought stressOryza sativa
spellingShingle Guanghui Wang
Guanghui Wang
Yu Xiao
Yu Xiao
Xiaojiang Deng
Xiaojiang Deng
Heting Zhang
Heting Zhang
Tingge Li
Tingge Li
Huiping Chen
Huiping Chen
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
Frontiers in Plant Science
hydrogen peroxide (H2O2)
heme oxygenase-1 (HO-1)
aleurone layer
cyclic guanosine monophosphate (cGMP)
drought stress
Oryza sativa
title 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
title_full 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
title_fullStr 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
title_full_unstemmed 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
title_short 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
title_sort 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
topic hydrogen peroxide (H2O2)
heme oxygenase-1 (HO-1)
aleurone layer
cyclic guanosine monophosphate (cGMP)
drought stress
Oryza sativa
url http://journal.frontiersin.org/article/10.3389/fpls.2018.00084/full
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