The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in Wheat

Systemic wound response (SWR), a well-characterized systemic signaling response, plays crucial roles in plant defense responses. Progress in understanding of the SWR in abiotic stress has also been aided by the researchers. However, the function of SWR in freezing stress remains elusive. In this stu...

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Main Authors: Tong Si, Xiao Wang, Chunzhao Zhao, Mei Huang, Jian Cai, Qin Zhou, Tingbo Dai, Dong Jiang
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-03-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2018.00327/full
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author Tong Si
Tong Si
Xiao Wang
Chunzhao Zhao
Mei Huang
Jian Cai
Qin Zhou
Tingbo Dai
Dong Jiang
spellingShingle Tong Si
Tong Si
Xiao Wang
Chunzhao Zhao
Mei Huang
Jian Cai
Qin Zhou
Tingbo Dai
Dong Jiang
The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in Wheat
Frontiers in Plant Science
mechanical wounding
hydrogen peroxide
systemic wound response
wheat
freezing tolerance
author_facet Tong Si
Tong Si
Xiao Wang
Chunzhao Zhao
Mei Huang
Jian Cai
Qin Zhou
Tingbo Dai
Dong Jiang
author_sort Tong Si
title The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in Wheat
title_short The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in Wheat
title_full The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in Wheat
title_fullStr The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in Wheat
title_full_unstemmed The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in Wheat
title_sort role of hydrogen peroxide in mediating the mechanical wounding-induced freezing tolerance in wheat
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2018-03-01
description Systemic wound response (SWR), a well-characterized systemic signaling response, plays crucial roles in plant defense responses. Progress in understanding of the SWR in abiotic stress has also been aided by the researchers. However, the function of SWR in freezing stress remains elusive. In this study, we showed that local mild mechanical wounding enhanced freezing tolerance in newly occurred systemic leaves of wheat plants (Triticum aestivum L.). Wounding significantly increased the maximal photochemical efficiency of photosystem II, net photosynthetic rate, and the activities of the antioxidant enzymes under freezing stress. Wounding also alleviated freezing-induced chlorophyll decomposition, electrolyte leakage, water lose, and membrane peroxidation. In addition, wounding-induced freezing stress mitigation was closely associated with the ratio between reduced glutathione (GSH) and oxidized glutathione (GSSG), and the ratio between ascorbate (AsA) and dehydroascorbate (DHA), as well as the contents of total soluble sugars and free amino acids. Importantly, pharmacological study showed that wounding-induced freezing tolerance was substantially arrested by pretreatment of wheat leaves with the scavenger of hydrogen peroxide (H2O2) or the inhibitor of NADPH oxidase (RBOH). These results support the hypothesis that local mechanical wounding-induced SWR in newly occurred leaves is largely attributed to RBOH-dependent H2O2 production, which may subsequently induce freezing tolerance in wheat plants. This mechanism may have a potential application to reduce the yield losses of wheat under late spring freezing conditions.Highlights:In our previous research, we found that local mechanical wounding could induce freezing tolerance in the upper systemic leaves of wheat plants. Surprisingly, in this paper, we further demonstrated that local mechanical wounding could also increase freezing resistance in newly occurred leaves of wheat plants. RBOH mediated H2O2 and ascorbate–glutathione cycle participate in this systemic wound response.
topic mechanical wounding
hydrogen peroxide
systemic wound response
wheat
freezing tolerance
url http://journal.frontiersin.org/article/10.3389/fpls.2018.00327/full
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spelling doaj-c326351e86734f56a040d572c2b4bd3c2020-11-25T00:24:42ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-03-01910.3389/fpls.2018.00327336673The Role of Hydrogen Peroxide in Mediating the Mechanical Wounding-Induced Freezing Tolerance in WheatTong Si0Tong Si1Xiao Wang2Chunzhao Zhao3Mei Huang4Jian Cai5Qin Zhou6Tingbo Dai7Dong Jiang8National Technique Innovation Center for Regional Wheat Production, Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, National Engineering and Technology Center for Information Agriculture, Nanjing Agricultural University, Nanjing, ChinaDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United StatesNational Technique Innovation Center for Regional Wheat Production, Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, National Engineering and Technology Center for Information Agriculture, Nanjing Agricultural University, Nanjing, ChinaDepartment of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United StatesNational Technique Innovation Center for Regional Wheat Production, Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, National Engineering and Technology Center for Information Agriculture, Nanjing Agricultural University, Nanjing, ChinaNational Technique Innovation Center for Regional Wheat Production, Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, National Engineering and Technology Center for Information Agriculture, Nanjing Agricultural University, Nanjing, ChinaNational Technique Innovation Center for Regional Wheat Production, Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, National Engineering and Technology Center for Information Agriculture, Nanjing Agricultural University, Nanjing, ChinaNational Technique Innovation Center for Regional Wheat Production, Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, National Engineering and Technology Center for Information Agriculture, Nanjing Agricultural University, Nanjing, ChinaNational Technique Innovation Center for Regional Wheat Production, Key Laboratory of Crop Physiology and Ecology in Southern China, Ministry of Agriculture, National Engineering and Technology Center for Information Agriculture, Nanjing Agricultural University, Nanjing, ChinaSystemic wound response (SWR), a well-characterized systemic signaling response, plays crucial roles in plant defense responses. Progress in understanding of the SWR in abiotic stress has also been aided by the researchers. However, the function of SWR in freezing stress remains elusive. In this study, we showed that local mild mechanical wounding enhanced freezing tolerance in newly occurred systemic leaves of wheat plants (Triticum aestivum L.). Wounding significantly increased the maximal photochemical efficiency of photosystem II, net photosynthetic rate, and the activities of the antioxidant enzymes under freezing stress. Wounding also alleviated freezing-induced chlorophyll decomposition, electrolyte leakage, water lose, and membrane peroxidation. In addition, wounding-induced freezing stress mitigation was closely associated with the ratio between reduced glutathione (GSH) and oxidized glutathione (GSSG), and the ratio between ascorbate (AsA) and dehydroascorbate (DHA), as well as the contents of total soluble sugars and free amino acids. Importantly, pharmacological study showed that wounding-induced freezing tolerance was substantially arrested by pretreatment of wheat leaves with the scavenger of hydrogen peroxide (H2O2) or the inhibitor of NADPH oxidase (RBOH). These results support the hypothesis that local mechanical wounding-induced SWR in newly occurred leaves is largely attributed to RBOH-dependent H2O2 production, which may subsequently induce freezing tolerance in wheat plants. This mechanism may have a potential application to reduce the yield losses of wheat under late spring freezing conditions.Highlights:In our previous research, we found that local mechanical wounding could induce freezing tolerance in the upper systemic leaves of wheat plants. Surprisingly, in this paper, we further demonstrated that local mechanical wounding could also increase freezing resistance in newly occurred leaves of wheat plants. RBOH mediated H2O2 and ascorbate–glutathione cycle participate in this systemic wound response.http://journal.frontiersin.org/article/10.3389/fpls.2018.00327/fullmechanical woundinghydrogen peroxidesystemic wound responsewheatfreezing tolerance