A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.

Transcriptional activation in response to hypoxia in plants is orchestrated by ethylene-responsive factor group VII (ERF-VII) transcription factors, which are stable during hypoxia but destabilized during normoxia through their targeting to the N-end rule pathway of selective proteolysis. Whereas th...

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Autores principales:	Beatrice Giuntoli, Seung Cho Lee, Francesco Licausi, Monika Kosmacz, Teruko Oosumi, Joost T van Dongen, Julia Bailey-Serres, Pierdomenico Perata
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/53fe0c793b8e4f0d914ca2653d994f8e
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spelling	oai:doaj.org-article:53fe0c793b8e4f0d914ca2653d994f8e2021-11-25T05:32:57ZA trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.1544-91731545-788510.1371/journal.pbio.1001950https://doaj.org/article/53fe0c793b8e4f0d914ca2653d994f8e2014-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.1001950https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Transcriptional activation in response to hypoxia in plants is orchestrated by ethylene-responsive factor group VII (ERF-VII) transcription factors, which are stable during hypoxia but destabilized during normoxia through their targeting to the N-end rule pathway of selective proteolysis. Whereas the conditionally expressed ERF-VII genes enable effective flooding survival strategies in rice, the constitutive accumulation of N-end-rule-insensitive versions of the Arabidopsis thaliana ERF-VII factor RAP2.12 is maladaptive. This suggests that transcriptional activation under hypoxia that leads to anaerobic metabolism may need to be fine-tuned. However, it is presently unknown whether a counterbalance of RAP2.12 exists. Genome-wide transcriptome analyses identified an uncharacterized trihelix transcription factor gene, which we named HYPOXIA RESPONSE ATTENUATOR1 (HRA1), as highly up-regulated by hypoxia. HRA1 counteracts the induction of core low oxygen-responsive genes and transcriptional activation of hypoxia-responsive promoters by RAP2.12. By yeast-two-hybrid assays and chromatin immunoprecipitation we demonstrated that HRA1 interacts with the RAP2.12 protein but with only a few genomic DNA regions from hypoxia-regulated genes, indicating that HRA1 modulates RAP2.12 through protein-protein interaction. Comparison of the low oxygen response of tissues characterized by different levels of metabolic hypoxia (i.e., the shoot apical zone versus mature rosette leaves) revealed that the antagonistic interplay between RAP2.12 and HRA1 enables a flexible response to fluctuating hypoxia and is of importance to stress survival. In Arabidopsis, an effective low oxygen-sensing response requires RAP2.12 stabilization followed by HRA1 induction to modulate the extent of the anaerobic response by negative feedback regulation of RAP2.12. This mechanism is crucial for plant survival under suboptimal oxygenation conditions. The discovery of the feedback loop regulating the oxygen-sensing mechanism in plants opens new perspectives for breeding flood-resistant crops.Beatrice GiuntoliSeung Cho LeeFrancesco LicausiMonika KosmaczTeruko OosumiJoost T van DongenJulia Bailey-SerresPierdomenico PerataPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 9, p e1001950 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Beatrice Giuntoli Seung Cho Lee Francesco Licausi Monika Kosmacz Teruko Oosumi Joost T van Dongen Julia Bailey-Serres Pierdomenico Perata A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.
description	Transcriptional activation in response to hypoxia in plants is orchestrated by ethylene-responsive factor group VII (ERF-VII) transcription factors, which are stable during hypoxia but destabilized during normoxia through their targeting to the N-end rule pathway of selective proteolysis. Whereas the conditionally expressed ERF-VII genes enable effective flooding survival strategies in rice, the constitutive accumulation of N-end-rule-insensitive versions of the Arabidopsis thaliana ERF-VII factor RAP2.12 is maladaptive. This suggests that transcriptional activation under hypoxia that leads to anaerobic metabolism may need to be fine-tuned. However, it is presently unknown whether a counterbalance of RAP2.12 exists. Genome-wide transcriptome analyses identified an uncharacterized trihelix transcription factor gene, which we named HYPOXIA RESPONSE ATTENUATOR1 (HRA1), as highly up-regulated by hypoxia. HRA1 counteracts the induction of core low oxygen-responsive genes and transcriptional activation of hypoxia-responsive promoters by RAP2.12. By yeast-two-hybrid assays and chromatin immunoprecipitation we demonstrated that HRA1 interacts with the RAP2.12 protein but with only a few genomic DNA regions from hypoxia-regulated genes, indicating that HRA1 modulates RAP2.12 through protein-protein interaction. Comparison of the low oxygen response of tissues characterized by different levels of metabolic hypoxia (i.e., the shoot apical zone versus mature rosette leaves) revealed that the antagonistic interplay between RAP2.12 and HRA1 enables a flexible response to fluctuating hypoxia and is of importance to stress survival. In Arabidopsis, an effective low oxygen-sensing response requires RAP2.12 stabilization followed by HRA1 induction to modulate the extent of the anaerobic response by negative feedback regulation of RAP2.12. This mechanism is crucial for plant survival under suboptimal oxygenation conditions. The discovery of the feedback loop regulating the oxygen-sensing mechanism in plants opens new perspectives for breeding flood-resistant crops.
format	article
author	Beatrice Giuntoli Seung Cho Lee Francesco Licausi Monika Kosmacz Teruko Oosumi Joost T van Dongen Julia Bailey-Serres Pierdomenico Perata
author_facet	Beatrice Giuntoli Seung Cho Lee Francesco Licausi Monika Kosmacz Teruko Oosumi Joost T van Dongen Julia Bailey-Serres Pierdomenico Perata
author_sort	Beatrice Giuntoli
title	A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.
title_short	A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.
title_full	A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.
title_fullStr	A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.
title_full_unstemmed	A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.
title_sort	trihelix dna binding protein counterbalances hypoxia-responsive transcriptional activation in arabidopsis.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/53fe0c793b8e4f0d914ca2653d994f8e
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A trihelix DNA binding protein counterbalances hypoxia-responsive transcriptional activation in Arabidopsis.

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