Thioredoxin, a master regulator of the tricarboxylic acid cycle in plant mitochondria

Authors
Daloso, Danilo M.; Müller, Karolin; Obata, Toshihiro; Florian, Alexandra; Tohge, Takayuki; Bottcher, Alexandra; Riondet, Christophe; Bariat, Laetitia; Carrari, Fernando Oscar; Nunes Nesi, Adriano; Buchanan, Bob B.; Reichheld, Jean-Philippe; Araújo, Wagner L.; Fernie, Alisdair R.
Publication Year
2015
Language
English
Format
article
Status
Published version
Description
Plant mitochondria have a fully operational tricarboxylic acid (TCA) cycle that plays a central role in generating ATP and providing carbon skeletons for a range of biosynthetic processes in both heterotrophic and photosynthetic tissues. The cycle enzyme-encoding genes have been well characterized in terms of transcriptional and effector-mediated regulation and have also been subjected to reverse genetic analysis. However, despite this wealth of attention, a central question remains unanswered: "What regulates flux through this pathway in vivo?" Previous proteomic experiments with Arabidopsis discussed below have revealed that a number of mitochondrial enzymes, including members of the TCA cycle and affiliated pathways, harbor thioredoxin (TRX)-binding sites and are potentially redox-regulated. We have followed up on this possibility and found TRX to be a redox-sensitive mediator of TCA cycle flux. In this investigation, we first characterized, at the enzyme and metabolite levels, mutants of the mitochondrial TRX pathway in Arabidopsis: the NADP-TRX reductase a and b double mutant (ntra ntrb) and the mitochondrially located thioredoxin o1 (trxo1) mutant. These studies were followed by a comparative evaluation of the redistribution of isotopes when 13C-glucose, 13C-malate, or 13C-pyruvate was provided as a substrate to leaves of mutant or WT plants. In a complementary approach, we evaluated the in vitro activities of a range of TCA cycle and associated enzymes under varying redox states. The combined dataset suggests that TRX may deactivate both mitochondrial succinate dehydrogenase and fumarase and activate the cytosolic ATP-citrate lyase in vivo, acting as a direct regulator of carbon flow through the TCA cycle and providing a mechanism for the coordination of cellular function.
Fil: Daloso, Danilo M.. Institut Max Planck Fur Molekulare Physiologie; Alemania. Universidade Federal de Vicosa; Brasil
Fil: Müller, Karolin. Institut Max Planck Fur Molekulare Physiologie; Alemania
Fil: Obata, Toshihiro. Institut Max Planck Fur Molekulare Physiologie; Alemania
Fil: Florian, Alexandra. Institut Max Planck Fur Molekulare Physiologie; Alemania
Fil: Tohge, Takayuki. Institut Max Planck Fur Molekulare Physiologie; Alemania
Fil: Bottcher, Alexandra. Institut Max Planck Fur Molekulare Physiologie; Alemania
Fil: Riondet, Christophe. Centre National de la Recherche Scientifique; Francia
Fil: Bariat, Laetitia. Centre National de la Recherche Scientifique; Francia
Fil: Carrari, Fernando Oscar. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina. Instituto Nacional de Tecnología Agropecuaria. Centro de Investigación en Ciencias Veterinarias y Agronómicas. Instituto de Biotecnología; Argentina
Fil: Nunes Nesi, Adriano. Universidade Federal de Vicosa; Brasil
Fil: Buchanan, Bob B.. University of California at Berkeley; Estados Unidos
Fil: Reichheld, Jean-Philippe. Centre National de la Recherche Scientifique; Francia
Fil: Araújo, Wagner L.. Universidade Federal de Vicosa; Brasil
Fil: Fernie, Alisdair R.. Institut Max Planck Fur Molekulare Physiologie; Alemania
Subject
ARABIDOPSIS
ATP-CITRATE LYASE
CITRIC ACID CYCLE REGULATION
REDOX REGULATION
THIOREDOXIN TCA CYCLE REGULATION
Otras Ciencias Biológicas
Ciencias Biológicas
CIENCIAS NATURALES Y EXACTAS
Access level
Restricted access
License
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repository
CONICET Digital (CONICET)
Institution
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identifier
oai:ri.conicet.gov.ar:11336/38435