Jasmonic acid-regulated putrescine biosynthesis attenuates cold-induced oxidative stress in tomato plants

•Cold promotes accumulation of putrescine (Put) and jasmonic acid (JA).•JA increases Put accumulation and cold tolerance.•Suppression of JA signaling reduces Put accumulation.•JA-regulated Put biosynthesis attenuates cold-triggered oxidative stress. Previous studies have shown that jasmonic acid (JA...

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Published inScientia horticulturae Vol. 288; p. 110373
Main Authors Ding, Fei, Wang, Chuang, Xu, Ning, Wang, Meiling, Zhang, Shuoxin
Format Journal Article
LanguageEnglish
Published Elsevier B.V 15.10.2021
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Abstract •Cold promotes accumulation of putrescine (Put) and jasmonic acid (JA).•JA increases Put accumulation and cold tolerance.•Suppression of JA signaling reduces Put accumulation.•JA-regulated Put biosynthesis attenuates cold-triggered oxidative stress. Previous studies have shown that jasmonic acid (JA) and putrescine (Put), a major polyamine, are both accumulated in tomato plants upon cold treatment. However, it is unclear whether JA regulates Put biosynthesis in tomato plants under the cold condition. The goal of the present work was to determine whether JA regulates Put biosynthesis and how JA-regulated Put accumulation affects cold tolerance in tomato plants. We found that among three major polyamines, putrescine was predominantly accumulated in cold-stressed tomato plants and exogenous putrescine markedly alleviated cold-induced oxidative stress, indicating an important role of putrescine in tomato cold response. We then identified ADC1 as a major putrescine biosynthetic gene in response to cold and JA. Further experiments using a JA biosynthesis inhibitor sodium diethyldithiocarbamate (DIECA), MeJA and an ADC (arginine decarboxylase 1) enzyme inhibitor difluoromethylarginine (DFMA) confirmed that JA functions in the putrescine biosynthesis by acting on ADC. Finally, we found that RNAi-mediated suppression of MYC2, a master regulator of JA signaling, decreased the expression of ADC1, reduced putrescine accumulation and enhanced cold-induced oxidative damages, implying that JA-induced putrescine biosynthesis relies, at least partially, on MYC2 in tomato plants. Our study thus establishes a link between JA signaling and polyamine metabolism in tomato plants under cold stress. Our data support that JA signaling is crucial for putrescine biosynthesis during cold stress and JA-induced accumulation of putrescine mitigates cold-induced oxidative stress in plants.
AbstractList •Cold promotes accumulation of putrescine (Put) and jasmonic acid (JA).•JA increases Put accumulation and cold tolerance.•Suppression of JA signaling reduces Put accumulation.•JA-regulated Put biosynthesis attenuates cold-triggered oxidative stress. Previous studies have shown that jasmonic acid (JA) and putrescine (Put), a major polyamine, are both accumulated in tomato plants upon cold treatment. However, it is unclear whether JA regulates Put biosynthesis in tomato plants under the cold condition. The goal of the present work was to determine whether JA regulates Put biosynthesis and how JA-regulated Put accumulation affects cold tolerance in tomato plants. We found that among three major polyamines, putrescine was predominantly accumulated in cold-stressed tomato plants and exogenous putrescine markedly alleviated cold-induced oxidative stress, indicating an important role of putrescine in tomato cold response. We then identified ADC1 as a major putrescine biosynthetic gene in response to cold and JA. Further experiments using a JA biosynthesis inhibitor sodium diethyldithiocarbamate (DIECA), MeJA and an ADC (arginine decarboxylase 1) enzyme inhibitor difluoromethylarginine (DFMA) confirmed that JA functions in the putrescine biosynthesis by acting on ADC. Finally, we found that RNAi-mediated suppression of MYC2, a master regulator of JA signaling, decreased the expression of ADC1, reduced putrescine accumulation and enhanced cold-induced oxidative damages, implying that JA-induced putrescine biosynthesis relies, at least partially, on MYC2 in tomato plants. Our study thus establishes a link between JA signaling and polyamine metabolism in tomato plants under cold stress. Our data support that JA signaling is crucial for putrescine biosynthesis during cold stress and JA-induced accumulation of putrescine mitigates cold-induced oxidative stress in plants.
Previous studies have shown that jasmonic acid (JA) and putrescine (Put), a major polyamine, are both accumulated in tomato plants upon cold treatment. However, it is unclear whether JA regulates Put biosynthesis in tomato plants under the cold condition. The goal of the present work was to determine whether JA regulates Put biosynthesis and how JA-regulated Put accumulation affects cold tolerance in tomato plants. We found that among three major polyamines, putrescine was predominantly accumulated in cold-stressed tomato plants and exogenous putrescine markedly alleviated cold-induced oxidative stress, indicating an important role of putrescine in tomato cold response. We then identified ADC1 as a major putrescine biosynthetic gene in response to cold and JA. Further experiments using a JA biosynthesis inhibitor sodium diethyldithiocarbamate (DIECA), MeJA and an ADC (arginine decarboxylase 1) enzyme inhibitor difluoromethylarginine (DFMA) confirmed that JA functions in the putrescine biosynthesis by acting on ADC. Finally, we found that RNAi-mediated suppression of MYC2, a master regulator of JA signaling, decreased the expression of ADC1, reduced putrescine accumulation and enhanced cold-induced oxidative damages, implying that JA-induced putrescine biosynthesis relies, at least partially, on MYC2 in tomato plants. Our study thus establishes a link between JA signaling and polyamine metabolism in tomato plants under cold stress. Our data support that JA signaling is crucial for putrescine biosynthesis during cold stress and JA-induced accumulation of putrescine mitigates cold-induced oxidative stress in plants.
ArticleNumber 110373
Author Xu, Ning
Zhang, Shuoxin
Wang, Meiling
Ding, Fei
Wang, Chuang
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  surname: Wang
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  givenname: Ning
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  fullname: Wang, Meiling
  organization: School of Life Sciences, Liaocheng University, Liaocheng 252000, China
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  givenname: Shuoxin
  surname: Zhang
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  organization: College of Forestry, Northwest A&F University, Yangling 712100, China
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Keywords Arginine decarboxylase
Cold stress
Putrescine
Polyamines
Solanum lycopersicum
Jasmonic acid
Language English
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Snippet •Cold promotes accumulation of putrescine (Put) and jasmonic acid (JA).•JA increases Put accumulation and cold tolerance.•Suppression of JA signaling reduces...
Previous studies have shown that jasmonic acid (JA) and putrescine (Put), a major polyamine, are both accumulated in tomato plants upon cold treatment....
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SubjectTerms Arginine decarboxylase
biosynthesis
cold
Cold stress
cold tolerance
cold treatment
genes
Jasmonic acid
oxidative stress
Polyamines
Putrescine
sodium
Solanum lycopersicum
tomatoes
Title Jasmonic acid-regulated putrescine biosynthesis attenuates cold-induced oxidative stress in tomato plants
URI https://dx.doi.org/10.1016/j.scienta.2021.110373
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