Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana Plants

Plants are known to respond to variations in cellular oxygen availability and distribution by quickly adapting the transcription rate of a number of genes, generally associated to improved energy usage pathways, oxygen homeostasis and protection from harmful products of anaerobic metabolism. In terr...

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Main Authors: Pierdomenico Perata, Beatrice Giuntoli, Francesco Licausi, Hans van Veen
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-04-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fpls.2017.00591/full
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author Pierdomenico Perata
Beatrice Giuntoli
Francesco Licausi
Francesco Licausi
Hans van Veen
author_facet Pierdomenico Perata
Beatrice Giuntoli
Francesco Licausi
Francesco Licausi
Hans van Veen
author_sort Pierdomenico Perata
collection DOAJ
description Plants are known to respond to variations in cellular oxygen availability and distribution by quickly adapting the transcription rate of a number of genes, generally associated to improved energy usage pathways, oxygen homeostasis and protection from harmful products of anaerobic metabolism. In terrestrial plants, such coordinated gene expression program is promoted by a conserved subfamily of ethylene responsive transcription factors called ERF-VII, which act as master activators of hypoxic gene transcription. Their abundance is directly regulated by oxygen through a mechanism of targeted proteolysis present under aerobic conditions, which is triggered by ERF-VII protein oxidation. Beside this, in Arabidopsis thaliana, the activity of the ERF-VII factor RAP2.12 has been shown to be restrained and made transient by the hypoxia-inducible transcription factor HRA1. This feedback mechanism has been proposed to modulate ERF-VII activity in the plant under fluctuating hypoxia, thereby enhancing the flexibility of the response. So far, functional balancing between RAP2.12 and HRA1 has been assessed in isolated leaf protoplasts, resulting in an inverse relationship between HRA1 amount and activation of RAP2.12 target promoters. In the present work, we showed that HRA1 is effective in balancing RAP2.12 activity in whole arabidopsis plants. Examination of a segregating population, generated from RAP2.12 and HRA1 over-expressing plants, led to the first quantitative proof that, over a range of either transgene expression levels, HRA1 counteracts the phenotypic and transcriptional effects of RAP2.12. This report supports the occurrence of fine-tuned regulation of the hypoxic response under physiological growth conditions.
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spelling doaj.art-b46bce82729344d4be2c618e913ddc802022-12-22T03:30:58ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2017-04-01810.3389/fpls.2017.00591258344Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana PlantsPierdomenico Perata0Beatrice Giuntoli1Francesco Licausi2Francesco Licausi3Hans van Veen4Plant Lab, Institute of Life Sciences, Scuola Superiore Sant'AnnaPisa, ItalyPlant Lab, Institute of Life Sciences, Scuola Superiore Sant'AnnaPisa, ItalyPlant Lab, Institute of Life Sciences, Scuola Superiore Sant'AnnaPisa, ItalyBiology Department, University of PisaPisa, ItalyPlant Lab, Institute of Life Sciences, Scuola Superiore Sant'AnnaPisa, ItalyPlants are known to respond to variations in cellular oxygen availability and distribution by quickly adapting the transcription rate of a number of genes, generally associated to improved energy usage pathways, oxygen homeostasis and protection from harmful products of anaerobic metabolism. In terrestrial plants, such coordinated gene expression program is promoted by a conserved subfamily of ethylene responsive transcription factors called ERF-VII, which act as master activators of hypoxic gene transcription. Their abundance is directly regulated by oxygen through a mechanism of targeted proteolysis present under aerobic conditions, which is triggered by ERF-VII protein oxidation. Beside this, in Arabidopsis thaliana, the activity of the ERF-VII factor RAP2.12 has been shown to be restrained and made transient by the hypoxia-inducible transcription factor HRA1. This feedback mechanism has been proposed to modulate ERF-VII activity in the plant under fluctuating hypoxia, thereby enhancing the flexibility of the response. So far, functional balancing between RAP2.12 and HRA1 has been assessed in isolated leaf protoplasts, resulting in an inverse relationship between HRA1 amount and activation of RAP2.12 target promoters. In the present work, we showed that HRA1 is effective in balancing RAP2.12 activity in whole arabidopsis plants. Examination of a segregating population, generated from RAP2.12 and HRA1 over-expressing plants, led to the first quantitative proof that, over a range of either transgene expression levels, HRA1 counteracts the phenotypic and transcriptional effects of RAP2.12. This report supports the occurrence of fine-tuned regulation of the hypoxic response under physiological growth conditions.http://journal.frontiersin.org/article/10.3389/fpls.2017.00591/fulllow oxygenregulation of anaerobic gene expressionERF-VII transcription factorstrihelix transcription factor familytranscription factor balancing
spellingShingle Pierdomenico Perata
Beatrice Giuntoli
Francesco Licausi
Francesco Licausi
Hans van Veen
Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana Plants
Frontiers in Plant Science
low oxygen
regulation of anaerobic gene expression
ERF-VII transcription factors
trihelix transcription factor family
transcription factor balancing
title Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana Plants
title_full Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana Plants
title_fullStr Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana Plants
title_full_unstemmed Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana Plants
title_short Functional Balancing of the Hypoxia Regulators RAP2.12 and HRA1 Takes Place in vivo in Arabidopsis thaliana Plants
title_sort functional balancing of the hypoxia regulators rap2 12 and hra1 takes place in vivo in arabidopsis thaliana plants
topic low oxygen
regulation of anaerobic gene expression
ERF-VII transcription factors
trihelix transcription factor family
transcription factor balancing
url http://journal.frontiersin.org/article/10.3389/fpls.2017.00591/full
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