TY - JOUR A1 - Tome, Filipa A1 - Nägele, Thomas A1 - Adamo, Mattia A1 - Garg, Abhroop A1 - Marco-Ilorca, Carles A1 - Nukarinen, Ella A1 - Pedrotti, Lorenzo A1 - Peviani, Alessia A1 - Simeunovic, Andrea A1 - Tatkiewicz, Anna A1 - Tomar, Monika A1 - Gamm, Magdalena T1 - The low energy signaling network JF - Frontiers in Plant Science N2 - Stress impacts negatively on plant growth and crop productivity, causing extensive losses to agricultural production worldwide. Throughout their life, plants are often confronted with multiple types of stress that affect overall cellular energy status and activate energy-saving responses. The resulting low energy syndrome (LES) includes transcriptional, translational, and metabolic reprogramming and is essential for stress adaptation. The conserved kinases sucrose-non-fermenting-1-related protein kinase-1 (SnRK1) and target of rapamycin (TOR) play central roles in the regulation of LES in response to stress conditions, affecting cellular processes and leading to growth arrest and metabolic reprogramming. We review the current understanding of how TOR and SnRK1 are involved in regulating the response of plants to low energy conditions. The central role in the regulation of cellular processes, the reprogramming of metabolism, and the phenotypic consequences of these two kinases will be discussed in light of current knowledge and potential future developments. KW - stress KW - metabolism KW - T6P KW - energy signaling KW - TOR KW - bZIP KW - SnRK1 KW - messenger-RNA translation KW - bZIP transcription fators KW - amino-acid-metabolism Y1 - 2014 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:bvb:20-opus-115813 SN - 1664-462X VL - 5 IS - 353 ER - TY - JOUR A1 - Nukarinen, Ella A1 - Nägele, Thomas A1 - Pedrotti, Lorenzo A1 - Wurzinger, Bernhard A1 - Mair, Andrea A1 - Landgraf, Ramona A1 - Börnke, Frederik A1 - Hanson, Johannes A1 - Teige, Markus A1 - Baena-Gonzalez, Elena A1 - Dröge-Laser, Wolfgang A1 - Weckwerth, Wolfram T1 - Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation JF - Scientific Reports N2 - Since years, research on SnRK1, the major cellular energy sensor in plants, has tried to define its role in energy signalling. However, these attempts were notoriously hampered by the lethality of a complete knockout of SnRK1. Therefore, we generated an inducible amiRNA::SnRK1α2 in a snrk1α1 knock out background (snrk1α1/α2) to abolish SnRK1 activity to understand major systemic functions of SnRK1 signalling under energy deprivation triggered by extended night treatment. We analysed the in vivo phosphoproteome, proteome and metabolome and found that activation of SnRK1 is essential for repression of high energy demanding cell processes such as protein synthesis. The most abundant effect was the constitutively high phosphorylation of ribosomal protein S6 (RPS6) in the snrk1α1/α2 mutant. RPS6 is a major target of TOR signalling and its phosphorylation correlates with translation. Further evidence for an antagonistic SnRK1 and TOR crosstalk comparable to the animal system was demonstrated by the in vivo interaction of SnRK1α1 and RAPTOR1B in the cytosol and by phosphorylation of RAPTOR1B by SnRK1α1 in kinase assays. Moreover, changed levels of phosphorylation states of several chloroplastic proteins in the snrk1α1/α2 mutant indicated an unexpected link to regulation of photosynthesis, the main energy source in plants. KW - phosphoproteomics KW - SnRK1 KW - energy deprivation KW - plants Y1 - 2016 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:bvb:20-opus-167638 VL - 6 IS - 31697 ER - TY - THES A1 - Pedrotti, Lorenzo T1 - The SnRK1-C/S1-bZIPs network: a signaling hub in Arabidopsis energy metabolism regulation T1 - Das SnRK1-C/S1-bZIP-Netzwerk: ein Signalknoten in der Regulation des Arabidopsis Energie-Metabolismus N2 - The control of energy homeostasis is of pivotal importance for all living organisms. In the last years emerged the idea that many stress responses that are apparently unrelated, are actually united by a common increase of the cellular energy demand. Therefore, the so called energy signaling is activated by many kind of stresses and is responsible for the activation of the general stress response. In Arabidopsis thaliana the protein family SnF1- related protein kinases (SnRK1) is involved in the regulation of many physiological processes but is more known for its involvement in the regulation of the energy homeostasis in response to various stresses. To the SnRK1 protein family belong SnRK1.1 (also known as KIN10), SnRK1.2 (KIN11), and SnRK1.3 (KIN12). SnRK1 exerts its function regulating directly the activity of metabolic enzymes or those of key transcription factors (TFs). The only TFs regulated by SnRK1 identified so far is the basic leucine zipper (bZIP) 63. bZIP63 belongs to the C group of bZIPs (C-bZIPs) protein family together with bZIP9, bZIP10, and bZIP25. SnRK1.1 phosphorylates bZIP63 on three amino acids residues, serine (S) 29, S294, and S300. The phosphorylation of tbZIP63 is strongly related to the energy status of the plant, shifting from almost absent during the normal growth to strongly phosphorylated when the plant is exposed to extended dark. bZIPs normally bind the DNA as dimer in order to regulate the expression of their target genes. C-bZIPs preferentially form dimers with S1-bZIPs, constituting the so called C/S1- bZIPs network. The SnRk1 dependent phosphorylation of bZIP63 regulates its activation potential and its dimerization properties. In particular bZIP63 shift its dimerization preferences according to its phosphorylation status. The non-phosphorylated form of bZIP63 dimerize bZIP1, the phosphorylates ones, instead, forms dimer with bZIP1, bZIP11, and bZIP63 its self. Together with bZIP63, S1-bZIPs are important mediator of part of the huge transcriptional reprogramming induced by SnRK1 in response to extended dark. S1-bZIPs regulate, indeed, the expression of 4'000 of the 10'000 SnRK1-regulated genes in response to energy deprivation. In particular S1-bZIPs are very important for the regulation of many genes encoding for enzymes involved in the amino acid metabolism and for their use as alternative energy source. After the exposition for some hours to extended dark, indeed, the plant make use of every energy substrate and amino acids are considered an important energy source together with lipids and proteins. Interestingly, S1- bZIPs regulate the expression of ETFQO. ETFQO is a unique protein that convoglia the electrons provenienti from the branch chain amino acids catabolism into the mitochondrial electron transport chain. The dimer formed between bZIP63 and bZIP2 recruits SnRK1.1 directly on the chromatin of ETFQO promoter. The recruitment of SnRK1 on ETFQO promoter is associated with its acetylation on the lysine 14 of the histone protein 3 (K14H3). This chromatin modification is normally asociated with an euchromatic status of the DNA and therefore with its transcriptional activation. Beside the particular case of the regulation of ETFQO gene, S1-bZIPs are involved in the regulation of many other genes activated in response of different stresses. bZIP1 is for example an important mediator of the salt stress response. In particular bZIP1 regulates the primary C- and N-metabolism. The expression of bZIP1, in response of both salt ans energy stress seems to be regulated by SnRK1, as it is the expression of bZIP53 and bZIP63. Beside its involvement in the regulation of the energy stress response and salt response, SnRK1 is the primary activators of the lipids metabolism during see germination. SnRK1, indeed, controls the expression of CALEOSINs and OLEOSINs. Those proteins are very important for lipids remobilization from oil droplets. Without their expression seed germination and subsequent establishment do not take place because of the absence of fuel to sustain these highly energy costly processes, which entirely depend on the catabolism of seed storages. N2 - Die Kontrolle der Energiehomöostase ist für alle lebenden Organismen von großer Bedeutung. In den letzten Jahren kam die Idee auf, dass viele Stressantworten, die scheinbar unabhängig voneinander sind, durch den Energiebedarf doch miteinander verbunden sind. Das sogenannte Energie-Signaling wird von vielen verschiedenen Stress- Arten aktiviert und ist verantwortlich für die Aktivierung der allgemeinen Stressantwort. In Arabidopsis thaliana ist die Proteinfamilie der SnF1-verwandten Proteinkinasen (SnRK1) an der Regulation vieler physiologischer Prozesse beteiligt. Auch bei der Regulation der Energiehomöostase als Folge von Stress spielen SnRK1-Kinasen eine wichtige Rolle. Proteine aus der SnRK1-Familie sind SnRK1.1, auch als KIN10 bezeichnet, SnRK1.2 (KIN11) und SnRK1.3 (KIN12). SnRK1-Proteine können die Aktivität von metabolischen Enzyme oder bestimmten Transkriptionsfaktoren (TF) direkt regulieren. Bislang wurde nur für den basischen Leucin-Zipper (bZIP) TF bZIP63 die Regulation durch SnRK1 gezeigt. bZIP63 gehört zur Gruppe C der bZIP Proteinfamilie (C-bZIP). Ebenfalls zu Gruppe C werden bZIP9, bZIP10 und bZIP25 zugeordnet. SnRK1.1 phosphoryliert das bZIP63- Protein an Serin (S) 29, S294 und S300. Der Grad der Phosphorylierung von bZIP63 steht in direktem Zusammenhang mit dem Energiehaushalt der Pflanze. Unter normalen Bedingungen wird bZIP63 kaum phosphoryliert, während bei verlängerter Nacht bZIP63 stark phosphoryliert wird. bZIP TF bilden untereinander Dimere aus und binden so an die DNA um die Expression ihrer Zielgene zu regulieren. C-bZIP TF bilden bevorzugt Dimere mit bZIP TF der Gruppe S1, bekannt als das C/S1-bZIP-Netzwerk. Die SnRK1-abhängige Phosphorylierung von bZIP63 steuert das Aktivierungspotential und die Dimerisierungseigenschaften. Besonders bei bZIP63 ändern sich die Dimerisierungspartner in Abhängigkeit des Phosphorylierungsgrads. Nicht-phosphoryliert dimerisiert bZIP61 mit bZIP1, im phosphorylierten Zustand dagegen bildet bZIP63 Dimere neben bZIP1 auch mit bZIP11 und bZIP63. S1-bZIP TF sowie bZIP63 sind wichtige Regulatoren der transkriptionellen Reprogrammierung, die durch SnRK1 bei verlängerter Dunkelheit induziert wird. S1-bZIP TF regulieren die Expression von 4'000 der 10'000 durch SnRK1 regulierten Gene in der Energieverarmungsantwort. Besonders S1-bZIP TF sind sehr wichtig für die Regulation vieler Gene, die für Enzyme aus dem Aminosäuremetabolismus codieren und als alternative Energiequelle der Pflanze bekannt sind. Wird die Nacht für einige Stunden verlängert, greift die Pflanze auf jede mögliche Energiequelle zurück. Als Energiequelle werden besonders Aminosäuren, aber auch Lipiden und Proteinen herangezogen. Interessanterweise regulieren S1-bZIP TF die Expression von ETFQO. ETFQO ist ein besonderes Protein, das die Elektronen aus dem Metabolismus verzweigter Aminosäuren in die mitochondriale Elektronentransportkette steuert. Das Dimer aus bZIP63 und bZIP2 rekrutiert SnRK1.1 direkt an das Chromatin des ETFQO-Promotors. Dieser Rekrutierung folgt die Acetylierung des Histonproteins 3 (K14H3) am Lysin 14. Diese Modifikation des Chromatins führt normalerweise zu einem euchromatischen Status der DNA und der nachfolgenden transkriptionellen Aktivierung. Neben der Regulation des ETFQO-Gens sind S1-bZIP TF auch an der Regulation von vielen anderen Genen in Folge von verschiedenen Stressen beteiligt. bZIP1 ist beispielsweise ein wichtiger Regulator der Antwort auf Salz-Stress. Auch der primäre Kohlenstoff- und Stickstoffmetabolismus werden von bZIP1 reguliert. Es wird angenommen, dass die Expression von bZIP1 wie auch von bZIP53 und bZIP63 in der Antwort auf Salzstress und Energieverarmung durch SnRK1 gesteuert wird. Abgesehen von der Regulation der Antwort auf Energieverarmung und Salzstress spielen SnRK1-Proteine auch bei der Aktivierung des Lipidmetabolismus während der Keimung eine Rolle. SnRK1 kontrolliert die Expression von CALEOSINs und OLEOSINs. Diese beiden Proteine sind sehr wichtig für die Mobilisierung von Lipiden aus Öltröpfchen. In Abwesenheit von SnRK1 finden aufgrund von Energiemangel weder die Keimung noch die nachfolgende Entwicklung statt. KW - Ackerschmalwand KW - Homöostase KW - Proteinkinasen KW - Stress-Syndrom KW - SnRK1 KW - bZIPs KW - mitochondria KW - energy metabolism Y1 - 2018 U6 - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:bvb:20-opus-116080 ER -