Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves

Although the role of the 2-oxoglutarate dehydrogenase complex (2-OGDHC) has previously been demonstrated in plant heterotrophic tissues its role in photosynthetically active tissues remains poorly understood. By using a combination of metabolite and transcript profiles we here investigated the funct...

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Main Authors:	Araújo, Wagner L., Tohge, Takayuki, Nunes-Nesi, Adriano, Daloso, Danilo M., Nimick, Mhairi, Krahnert, Ina, Bunik, Victoria I., Moorhead, Greg B. G., Fernie, Alisdair R.
Format:	Online
Language:	English
Published:	Frontiers Research Foundation 2012
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3410613/

id	pubmed-3410613
recordtype	oai_dc
spelling	pubmed-34106132012-08-08 Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves Araújo, Wagner L. Tohge, Takayuki Nunes-Nesi, Adriano Daloso, Danilo M. Nimick, Mhairi Krahnert, Ina Bunik, Victoria I. Moorhead, Greg B. G. Fernie, Alisdair R. Plant Science Although the role of the 2-oxoglutarate dehydrogenase complex (2-OGDHC) has previously been demonstrated in plant heterotrophic tissues its role in photosynthetically active tissues remains poorly understood. By using a combination of metabolite and transcript profiles we here investigated the function of 2-OGDHC in leaves of Arabidopsis thaliana via use of specific phosphonate inhibitors of the enzyme. Incubation of leaf disks with the inhibitors revealed that they produced the anticipated effects on the in situ enzyme activity. In vitro experiments revealed that succinyl phosphonate (SP) and a carboxy ethyl ester of SP are slow-binding inhibitors of the 2-OGDHC. Our results indicate that the reduced respiration rates are associated with changes in the regulation of metabolic and signaling pathways leading to an imbalance in carbon-nitrogen metabolism and cell homeostasis. The inducible alteration of primary metabolism was associated with altered expression of genes belonging to networks of amino acids, plant respiration, and sugar metabolism. In addition, by using isothermal titration calorimetry we excluded the possibility that the changes in gene expression resulted from an effect on 2-oxoglutarate (2OG) binding to the carbon/ATP sensing protein PII. We also demonstrated that the 2OG degradation by the 2-oxoglutarate dehydrogenase strongly influences the distribution of intermediates of the tricarboxylic acid (TCA) cycle and the GABA shunt. Our results indicate that the TCA cycle activity is clearly working in a non-cyclic manner upon 2-OGDHC inhibition during the light period. Frontiers Research Foundation 2012-06-04 /pmc/articles/PMC3410613/ /pubmed/22876250 http://dx.doi.org/10.3389/fpls.2012.00114 Text en Copyright © 2012 Araújo, Tohge, Nunes-Nesi, Daloso, Nimick, Krahnert, Bunik, Moorhead and Fernie. http://www.frontiersin.org/licenseagreement This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Araújo, Wagner L. Tohge, Takayuki Nunes-Nesi, Adriano Daloso, Danilo M. Nimick, Mhairi Krahnert, Ina Bunik, Victoria I. Moorhead, Greg B. G. Fernie, Alisdair R.
spellingShingle	Araújo, Wagner L. Tohge, Takayuki Nunes-Nesi, Adriano Daloso, Danilo M. Nimick, Mhairi Krahnert, Ina Bunik, Victoria I. Moorhead, Greg B. G. Fernie, Alisdair R. Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves
author_facet	Araújo, Wagner L. Tohge, Takayuki Nunes-Nesi, Adriano Daloso, Danilo M. Nimick, Mhairi Krahnert, Ina Bunik, Victoria I. Moorhead, Greg B. G. Fernie, Alisdair R.
author_sort	Araújo, Wagner L.
title	Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves
title_short	Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves
title_full	Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves
title_fullStr	Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves
title_full_unstemmed	Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves
title_sort	phosphonate analogs of 2-oxoglutarate perturb metabolism and gene expression in illuminated arabidopsis leaves
description	Although the role of the 2-oxoglutarate dehydrogenase complex (2-OGDHC) has previously been demonstrated in plant heterotrophic tissues its role in photosynthetically active tissues remains poorly understood. By using a combination of metabolite and transcript profiles we here investigated the function of 2-OGDHC in leaves of Arabidopsis thaliana via use of specific phosphonate inhibitors of the enzyme. Incubation of leaf disks with the inhibitors revealed that they produced the anticipated effects on the in situ enzyme activity. In vitro experiments revealed that succinyl phosphonate (SP) and a carboxy ethyl ester of SP are slow-binding inhibitors of the 2-OGDHC. Our results indicate that the reduced respiration rates are associated with changes in the regulation of metabolic and signaling pathways leading to an imbalance in carbon-nitrogen metabolism and cell homeostasis. The inducible alteration of primary metabolism was associated with altered expression of genes belonging to networks of amino acids, plant respiration, and sugar metabolism. In addition, by using isothermal titration calorimetry we excluded the possibility that the changes in gene expression resulted from an effect on 2-oxoglutarate (2OG) binding to the carbon/ATP sensing protein PII. We also demonstrated that the 2OG degradation by the 2-oxoglutarate dehydrogenase strongly influences the distribution of intermediates of the tricarboxylic acid (TCA) cycle and the GABA shunt. Our results indicate that the TCA cycle activity is clearly working in a non-cyclic manner upon 2-OGDHC inhibition during the light period.
publisher	Frontiers Research Foundation
publishDate	2012
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3410613/
_version_	1611547246533279744

Phosphonate Analogs of 2-Oxoglutarate Perturb Metabolism and Gene Expression in Illuminated Arabidopsis Leaves

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