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.

A systems biology view of wood formation in Eucalyptus grandis trees submitted to different potassium and water regimes

“…A subset of genes in M1–M6, associated with primary metabolism, were negatively correlated with the SCW‐associated genes and upregulated in K‐fertilized trees. Among them, we found EgrNAC12 , a putative ortholog of ANAC002 , an ABA‐inducible key TF that is strongly upregulated in response to cellular carbon depletion in Arabidopsis and responsive to stress including drought (Garapati et al ., ). Given that K‐fertilization triggers drought stress signaling in our conditions, one possible hypothesis could be that K‐fertilized trees develop strategies to mitigate drought stress such as stomatal closure to reduce transpiration, resulting in a reduction of carbon fixation by photosynthesis.…”

Dynamic and diverse sugar signaling

“…In Arabidopsis , KIN10/11 protein kinases provide catalytic activities in the SNRK1 complex and orchestrate global gene expression changes to activate catabolism but repress anabolism [21,23, 24,70]. Recent exciting progresses have identified new transcription factors as Arabidopsis KIN10 phosphorylation targets, including bZIP63, MYC2, NAC2/ATAF1, FUS3 and IDD transcription factors involved in low energy responses in darkness, submergence, starvation, and flowering [15,84,86,87*, 88*,89]. Direct phosphorylation by KIN10 protein kinase promotes bZIP63-bZIPS dimerization and the transcriptional activation of bZIPs, NAC2 and FUS3 [84,87*, 88*].…”

“…Recent exciting progresses have identified new transcription factors as Arabidopsis KIN10 phosphorylation targets, including bZIP63, MYC2, NAC2/ATAF1, FUS3 and IDD transcription factors involved in low energy responses in darkness, submergence, starvation, and flowering [15,84,86,87*, 88*,89]. Direct phosphorylation by KIN10 protein kinase promotes bZIP63-bZIPS dimerization and the transcriptional activation of bZIPs, NAC2 and FUS3 [84,87*, 88*]. Phosphorylation by KIN10 reduces MYC2 protein stability and transcriptional activity of IDD8 [86].…”

In situ transcriptomic and metabolomic study of the loss of photosynthesis in the leaves of mixotrophic plants exploiting fungi

“…Other metabolic changes were strikingly parallel to those during the carbon starvation response, in a way also conserved in variegated plants (Figure ). Some metabolic changes closely resembled features of carbon‐starving cells: increase in sugars and amino acid transporters (Contento et al ., ; Buchanan‐Wollaston et al ., ), increase in sucrose‐degrading enzymes (Buchanan‐Wollaston et al ., ; Baena‐González et al ., ), alteration of trehalose metabolism (Baena‐González et al ., ; Lunn et al ., ; Garapati et al ., ), increase in free amino acids (Brouquisse et al ., ; Araújo et al ., ; Hirota et al ., ), induction of asparagine synthetase (Brouquisse et al ., ; Baena‐González et al ., ), higher catabolism of amino acids (Contento et al ., ; Baena‐González et al ., ; Araújo et al ., ; Garapati et al ., ; Hirota et al ., ), induction of lipases (Buchanan‐Wollaston et al ., ; Baena‐González et al ., ), fatty acid β‐oxidation enzymes (Pistelli et al ., ; Baena‐González et al ., ), glyoxylate cycle enzymes (Pistelli et al ., ; Chen et al ., ; but not in Charlton et al ., ), and higher expression (respectively repression) of autophagy‐promoting (respectively inhibiting) genes (Garapati et al ., ; Üstün et al ., ; Hirota et al ., ). Carbon‐starved cells actively degrade their components, especially by enclosing them in autophagosomes addressed to the vacuole, where proteolysis releases amino acids as nutrients (Brouquisse et al ., ; Diaz‐Mendoza et al ., ; Hirota et al ., ).…”