title: Transcription Factor Arabidopsis Activating Factor1 Integrates Carbon Starvation Responses with Trehalose Metabolism.
abstract: Plants respond to low carbon supply by massive reprogramming of the transcriptome and metabolome. We show here that the carbon starvation-induced NAC (for NO APICAL MERISTEM/ARABIDOPSIS TRANSCRIPTION ACTIVATION FACTOR/CUP-SHAPED COTYLEDON) transcription factor Arabidopsis (Arabidopsis thaliana) Transcription Activation Factor1 (ATAF1) plays an important role in this physiological process. We identified TREHALASE1, the only trehalase-encoding gene in Arabidopsis, as a direct downstream target of ATAF1. Overexpression of ATAF1 activates TREHALASE1 expression and leads to reduced trehalose-6-phosphate levels and a sugar starvation metabolome. In accordance with changes in expression of starch biosynthesis- and breakdown-related genes, starch levels are generally reduced in ATAF1 overexpressors but elevated in ataf1 knockout plants. At the global transcriptome level, genes affected by ATAF1 are broadly associated with energy and carbon starvation responses. Furthermore, transcriptional responses triggered by ATAF1 largely overlap with expression patterns observed in plants starved for carbon or energy supply. Collectively, our data highlight the existence of a positively acting feedforward loop between ATAF1 expression, which is induced by carbon starvation, and the depletion of cellular carbon/energy pools that is triggered by the transcriptional regulation of downstream gene regulatory networks by ATAF1.
authors.affiliation: Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany (P.G., S.B., B.M.-R.); Plant Signaling Group (P.G., S.B., B.M.-R.) and System Regulation Group (R.F., J.E.L.), Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany; and Department of Molecular Microbiology, VIB and Laboratory of Molecular Cell Biology, KU Leuven, B-3001 Leuven, Belgium (P.V.D.).
authors.forename: Prashanth
authors.initials: P
authors.lastname: Garapati
authors.affiliation: Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany (P.G., S.B., B.M.-R.); Plant Signaling Group (P.G., S.B., B.M.-R.) and System Regulation Group (R.F., J.E.L.), Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany; and Department of Molecular Microbiology, VIB and Laboratory of Molecular Cell Biology, KU Leuven, B-3001 Leuven, Belgium (P.V.D.).
authors.forename: Regina
authors.initials: R
authors.lastname: Feil
authors.affiliation: Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany (P.G., S.B., B.M.-R.); Plant Signaling Group (P.G., S.B., B.M.-R.) and System Regulation Group (R.F., J.E.L.), Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany; and Department of Molecular Microbiology, VIB and Laboratory of Molecular Cell Biology, KU Leuven, B-3001 Leuven, Belgium (P.V.D.).
authors.forename: John Edward
authors.initials: JE
authors.lastname: Lunn
authors.affiliation: Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany (P.G., S.B., B.M.-R.); Plant Signaling Group (P.G., S.B., B.M.-R.) and System Regulation Group (R.F., J.E.L.), Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany; and Department of Molecular Microbiology, VIB and Laboratory of Molecular Cell Biology, KU Leuven, B-3001 Leuven, Belgium (P.V.D.).
authors.forename: Patrick
authors.identifier: http://orcid.org/0000-0002-1542-897X
authors.initials: P
authors.lastname: Van Dijck
authors.affiliation: Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany (P.G., S.B., B.M.-R.); Plant Signaling Group (P.G., S.B., B.M.-R.) and System Regulation Group (R.F., J.E.L.), Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany; and Department of Molecular Microbiology, VIB and Laboratory of Molecular Cell Biology, KU Leuven, B-3001 Leuven, Belgium (P.V.D.) balazadeh@mpimp-golm.mpg.de bmr@uni-potsdam.de.
authors.forename: Salma
authors.identifier: http://orcid.org/0000-0002-5789-4071
authors.initials: S
authors.lastname: Balazadeh
authors.affiliation: Institute of Biochemistry and Biology, University of Potsdam, 14476 Potsdam-Golm, Germany (P.G., S.B., B.M.-R.); Plant Signaling Group (P.G., S.B., B.M.-R.) and System Regulation Group (R.F., J.E.L.), Max Planck Institute of Molecular Plant Physiology, 14476 Potsdam-Golm, Germany; and Department of Molecular Microbiology, VIB and Laboratory of Molecular Cell Biology, KU Leuven, B-3001 Leuven, Belgium (P.V.D.) balazadeh@mpimp-golm.mpg.de bmr@uni-potsdam.de.
authors.forename: Bernd
authors.identifier: http://orcid.org/0000-0002-1410-464X
authors.initials: B
authors.lastname: Mueller-Roeber
mesh_terms: D017360:Arabidopsis / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000378:metabolism*; D001343:Autophagy / Q000235:genetics; D002244:Carbon / Q000378:metabolism*; D057486:Carbon Cycle / Q000235:genetics; D004734:Energy Metabolism / Q000235:genetics; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D055442:Metabolome; D008954:Models, Biological; D012097:Repressor Proteins / Q000378:metabolism*; D013213:Starch / Q000378:metabolism; D013403:Sugar Phosphates / Q000378:metabolism*; D059467:Transcriptome / Q000235:genetics; D014198:Trehalase / Q000378:metabolism; D014199:Trehalose / Q000031:analogs & derivatives* / Q000378:metabolism; D015854:Up-Regulation / Q000235:genetics
chemical_list: C517610:ATAF1 protein, Arabidopsis; D029681:Arabidopsis Proteins; D012097:Repressor Proteins; D013403:Sugar Phosphates; C082722:trehalose-6-phosphate; D002244:Carbon; D013213:Starch; D014199:Trehalose; D014198:Trehalase; C582823:trehalase 1, Arabidopsis