Philipp Kreisz

Plants exhibit considerable phenotypic plasticity, allowing them to adapt their metabolism to the fluctuating energy supply in a natural environment. Using dark-induced senescence (DIS) as an experimental system, a mutant study combining phenotypic, transcriptomic and chromatin immunoprecipitation sequencing approaches identified distinct members of the Arabidopsis thaliana group S1 basic leucine zipper (bZIP) transcription factors that orchestrate the starvation response. Whereas excluding bZIP2, bZIP11, and bZIP44 to play a major role in DIS, bZIP1, and bZIP53 act partially redundantly to control a coexpression network governing amino acid catabolism and transport, gluconeogenesis and energy homeostasis. Moreover, bZIP1 and bZIP53 regulate genes involved in the asparagine–glutamine balance, two amino acids critical for carbon and nitrogen homeostasis. This transcriptional reprogramming in resource management is required for survival during starvation and regaining meristematic activity during the recovery from stress. Thus, our findings provide insights into the transcriptional control of plant resource and energy management during starvation. Overall, this work sheds light on the discrepancy between in vitro DNA binding and overexpression studies versus mutant analyses and in vivo DNA binding, providing a critical view on how to define specific transcription factor functions within large families.

Plants respond to elevated temperatures with enhanced elongation growth that depends on rapid transcriptional, post-transcriptional, and post-translational reprogramming. However, it is unclear how temperature information integrates with the splicing machinery to establish warm temperature-dependent splicing patterns. In animals, CDC2-LIKE KINASES (CLKs) function as body temperature sensors that control temperature-dependent splicing via phosphorylation of serine/arginine-rich (SR) proteins. Here we demonstrate that the CLK-homologous ARABIDOPSIS FUS3-COMPLEMENTING (AFC) kinases likewise regulate post-transcriptional RNA processing to control warm temperature-dependent growth in Arabidopsis. The contrasting temperature-activity profiles of the three AFCs depend on specific structural elements, including a conserved activation segment within the kinase domain. Combining protein structure prediction with site-directed mutagenesis, we provide insights into structural features that determine the different temperature-activity profiles of the three AFC paralogs. Analyses of afc mutant plants demonstrate their role in establishing temperature-dependent splicing patterns and thermomorphogenic hypocotyl elongation. Finally, our data indicate SR34 and SR34a as phosphorylation targets mediating temperature-dependent hypocotyl elongation downstream of AFCs. In conclusion, our study provides evidence that temperature-controlled AFC activity is evolutionarily conserved between plants and animals and implicates AFCs in the control of thermomorphogenesis.

Plants tightly control growth of their lateral organs, which led to the concept of apical dominance. However, outgrowth of the dormant lateral primordia is sensitive to the plant’s nutritional status, resulting in an immense plasticity in plant architecture. While the impact of hormonal regulation on apical dominance is well characterized, the prime importance of sugar signaling to unleash lateral organ formation has just recently emerged. Here, we aimed to identify transcriptional regulators, which control the trade-off between growth of apical versus lateral organs. Making use of locally inducible gain-of-function as well as single and higher-order loss-of-function approaches of the sugar-responsive S ₁ -basic-leucine-zipper (S ₁ -bZIP) transcription factors, we disclosed their largely redundant function in establishing apical growth dominance. Consistently, comprehensive phenotypical and analytical studies of S ₁ -bZIP mutants show a clear shift of sugar and organic nitrogen (N) allocation from apical to lateral organs, coinciding with strong lateral organ outgrowth. Tissue-specific transcriptomics reveal specific clade III SWEET sugar transporters, crucial for long-distance sugar transport to apical sinks and the glutaminase GLUTAMINE AMIDO-TRANSFERASE 1_2.1 , involved in N homeostasis, as direct S ₁ -bZIP targets, linking the architectural and metabolic mutant phenotypes to downstream gene regulation. Based on these results, we propose that S ₁ -bZIPs control carbohydrate (C) partitioning from source leaves to apical organs and tune systemic N supply to restrict lateral organ formation by C/N depletion. Knowledge of the underlying mechanisms controlling plant C/N partitioning is of pivotal importance for breeding strategies to generate plants with desired architectural and nutritional characteristics.

Philipp Kreisz was not included as an author in the original publication

The ontogenetic regulation of shoot branching allows plants to adjust their architecture in accordance with the environment. This process is due to the regulation of axillary bud outgrowth into branches, which can be induced by increasing sugar availability to the buds through decapitation of the shoot tip. Different sugar signalling components have been identified in the induction of shoot branching. However, the molecular components that maintain bud dormancy in response to sugar starvation remain largely unknown. Here, we show at the genetic level that basic leucine zipper 11 (bZIP11), a transcription factor that plays important roles in response to sugar starvation in plants, inhibits shoot branching in Arabidopsis thaliana . Physiology experiments demonstrated that bZIP11 protein levels are decreased by decapitation. Molecular and genetic evidence suggests that bZIP11 acts in a negative feedback loop with trehalose 6-phosphate (Tre6P), a sugar signal that promotes shoot branching. Our data also suggest that the central energy sensor SUCROSE NON-FERMENTING 1 RELATED KINASE1 (SnRK1), alleviates the inhibitory effect of Tre6P on bZIP11 protein accumulation and inhibits shoot branching. Altogether, these data provide a working model that involves bZIP11, Tre6P and SnRK1 in the regulation of shoot branching.

Plants exhibit an immense plasticity in their architecture. While the impact of hormonal regulation is well-characterised, the importance of sugar-signalling has just recently emerged. Here, we addressed which sugar-signalling components mediate the trade-off between growth of apical versus lateral meristems and how they control organ sink-strength. Thereby, we unravelled a novel developmental function of the sugar-controlled S ₁ basic-leucine-zipper (S ₁ -bZIP) transcription factors in establishing global source-sink interactions. Applying comprehensive molecular, analytical, and genetic approaches, we demonstrate that S ₁ -bZIPs operate in a redundant manner to control tissue-specific expression of defined SWEET sugar-transporters and the GAT1_2.1 glutaminase. By these means, S ₁ -bZIPs control carbohydrate (C)-channelling from source leaves to apical shoot and root organs and tune systemic organic nitrogen (N)-supply to restrict lateral organ formation by C/N depletion. Knowledge of the underlying mechanisms controlling plant C/N partitioning is of pivotal importance for breeding strategies to generate plants with desired architectural and nutritional characteristics.

(1) Background: The recurrence of glioblastoma multiforme (GBM) is mainly due to invasion of the surrounding brain tissue, where organic solutes, including glucose and inositol, are abundant. Invasive cell migration has been linked to the aberrant expression of transmembrane solute-linked carriers (SLC). Here, we explore the role of glucose (SLC5A1) and inositol transporters (SLC5A3) in GBM cell migration. (2) Methods: Using immunofluorescence microscopy, we visualized the subcellular localization of SLC5A1 and SLC5A3 in two highly motile human GBM cell lines. We also employed wound-healing assays to examine the effect of SLC inhibition on GBM cell migration and examined the chemotactic potential of inositol. (3) Results: While GBM cell migration was significantly increased by extracellular inositol and glucose, it was strongly impaired by SLC transporter inhibition. In the GBM cell monolayers, both SLCs were exclusively detected in the migrating cells at the monolayer edge. In single GBM cells, both transporters were primarily localized at the leading edge of the lamellipodium. Interestingly, in GBM cells migrating via blebbing, SLC5A1 and SLC5A3 were predominantly detected in nascent and mature blebs, respectively. (4) Conclusion: We provide several lines of evidence for the involvement of SLC5A1 and SLC5A3 in GBM cell migration, thereby complementing the migration-associated transportome. Our findings suggest that SLC inhibition is a promising approach to GBM treatment.