Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes

Enhancing crop tolerance to waterlogging is critical for improving food and biofuel security. In waterlogged soils, roots are exposed to a low oxygen environment. The group VII ethylene response factors (ERFVII<i>s</i>) were recently identified as key regulators of plant low oxygen respo...

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Main Authors: Piyada Juntawong, Pimprapai Butsayawarapat, Pattralak Songserm, Ratchaneeporn Pimjan, Supachai Vuttipongchaikij
Format: Article
Language:English
Published: MDPI AG 2020-08-01
Series:Plants
Subjects:
Online Access:https://www.mdpi.com/2223-7747/9/9/1068
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author Piyada Juntawong
Pimprapai Butsayawarapat
Pattralak Songserm
Ratchaneeporn Pimjan
Supachai Vuttipongchaikij
author_facet Piyada Juntawong
Pimprapai Butsayawarapat
Pattralak Songserm
Ratchaneeporn Pimjan
Supachai Vuttipongchaikij
author_sort Piyada Juntawong
collection DOAJ
description Enhancing crop tolerance to waterlogging is critical for improving food and biofuel security. In waterlogged soils, roots are exposed to a low oxygen environment. The group VII ethylene response factors (ERFVII<i>s</i>) were recently identified as key regulators of plant low oxygen response. Oxygen-dependent N-end rule pathways can regulate the stability of ERFVIIs. This study aims to characterize the function of the <i>Jatropha curcas ERFVIIs</i> and the impact of N-terminal modification that stabilized the protein toward low oxygen response. This study revealed that all three JcERFVII proteins are substrates of the N-end rule pathway. Overexpression of <i>JcERFVII2</i> conferred tolerance to low oxygen stress in Arabidopsis. In contrast, the constitutive overexpression of stabilized <i>JcERFVII2</i> reduced low oxygen tolerance. RNA-seq was performed to elucidate the functional roles of <i>JcERFVII2</i> and the impact of its N-terminal modification. Overexpression of both wildtype and stabilized <i>JcERFVII2</i> constitutively upregulated the plant core hypoxia-responsive genes. Besides, overexpression of the stabilized <i>JcERFVII2</i> further upregulated various genes controlling fermentative metabolic processes, oxidative stress, and pathogen responses under aerobic conditions. In summary, JcERFVII2 is an N-end rule regulated waterlogging-responsive transcription factor that modulates the expression of multiple stress-responsive genes; therefore, it is a potential candidate for molecular breeding of multiple stress-tolerant crops.
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spelling doaj.art-57b16568e0aa4792b196d7ab384f8e662023-11-20T10:48:52ZengMDPI AGPlants2223-77472020-08-0199106810.3390/plants9091068Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive GenesPiyada Juntawong0Pimprapai Butsayawarapat1Pattralak Songserm2Ratchaneeporn Pimjan3Supachai Vuttipongchaikij4Department of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, ThailandDepartment of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, ThailandDepartment of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, ThailandDepartment of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, ThailandDepartment of Genetics, Faculty of Science, Kasetsart University, Bangkok 10900, ThailandEnhancing crop tolerance to waterlogging is critical for improving food and biofuel security. In waterlogged soils, roots are exposed to a low oxygen environment. The group VII ethylene response factors (ERFVII<i>s</i>) were recently identified as key regulators of plant low oxygen response. Oxygen-dependent N-end rule pathways can regulate the stability of ERFVIIs. This study aims to characterize the function of the <i>Jatropha curcas ERFVIIs</i> and the impact of N-terminal modification that stabilized the protein toward low oxygen response. This study revealed that all three JcERFVII proteins are substrates of the N-end rule pathway. Overexpression of <i>JcERFVII2</i> conferred tolerance to low oxygen stress in Arabidopsis. In contrast, the constitutive overexpression of stabilized <i>JcERFVII2</i> reduced low oxygen tolerance. RNA-seq was performed to elucidate the functional roles of <i>JcERFVII2</i> and the impact of its N-terminal modification. Overexpression of both wildtype and stabilized <i>JcERFVII2</i> constitutively upregulated the plant core hypoxia-responsive genes. Besides, overexpression of the stabilized <i>JcERFVII2</i> further upregulated various genes controlling fermentative metabolic processes, oxidative stress, and pathogen responses under aerobic conditions. In summary, JcERFVII2 is an N-end rule regulated waterlogging-responsive transcription factor that modulates the expression of multiple stress-responsive genes; therefore, it is a potential candidate for molecular breeding of multiple stress-tolerant crops.https://www.mdpi.com/2223-7747/9/9/1068abiotic stressRNA-seqtranscription factorwaterlogging
spellingShingle Piyada Juntawong
Pimprapai Butsayawarapat
Pattralak Songserm
Ratchaneeporn Pimjan
Supachai Vuttipongchaikij
Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes
Plants
abiotic stress
RNA-seq
transcription factor
waterlogging
title Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes
title_full Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes
title_fullStr Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes
title_full_unstemmed Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes
title_short Overexpression of <i>Jatropha curcas</i> <i>ERFVII2</i> Transcription Factor Confers Low Oxygen Tolerance in Transgenic Arabidopsis by Modulating Expression of Metabolic Enzymes and Multiple Stress-Responsive Genes
title_sort overexpression of i jatropha curcas i i erfvii2 i transcription factor confers low oxygen tolerance in transgenic arabidopsis by modulating expression of metabolic enzymes and multiple stress responsive genes
topic abiotic stress
RNA-seq
transcription factor
waterlogging
url https://www.mdpi.com/2223-7747/9/9/1068
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AT pimprapaibutsayawarapat overexpressionofijatrophacurcasiierfvii2itranscriptionfactorconferslowoxygentoleranceintransgenicarabidopsisbymodulatingexpressionofmetabolicenzymesandmultiplestressresponsivegenes
AT pattralaksongserm overexpressionofijatrophacurcasiierfvii2itranscriptionfactorconferslowoxygentoleranceintransgenicarabidopsisbymodulatingexpressionofmetabolicenzymesandmultiplestressresponsivegenes
AT ratchaneepornpimjan overexpressionofijatrophacurcasiierfvii2itranscriptionfactorconferslowoxygentoleranceintransgenicarabidopsisbymodulatingexpressionofmetabolicenzymesandmultiplestressresponsivegenes
AT supachaivuttipongchaikij overexpressionofijatrophacurcasiierfvii2itranscriptionfactorconferslowoxygentoleranceintransgenicarabidopsisbymodulatingexpressionofmetabolicenzymesandmultiplestressresponsivegenes