Browsing by Author "Heyer, Arnd G."

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Open Access
Acclimation to elevated CO2 affects the C/N balance by reducing de novo N‐assimilation
(2021) Krämer, Konrad; Kepp, Gabi; Brock, Judith; Stutz, Simon; Heyer, Arnd G.
Plants exposed to elevated atmospheric CO2 concentrations show an increased photosynthetic activity. However, after prolonged exposure, the activity declines. This acclimation to elevated CO2 is accompanied by a rise in the carbon‐to‐nitrogen ratio of the biomass. Hence, increased sugar accumulation and sequential downregulation of photosynthetic genes, as well as nitrogen depletion and reduced protein content, have been hypothesized as the cause of low photosynthetic performance. However, the reason for reduced nitrogen content in plants at high CO2 is unclear. Here, we show that reduced photorespiration at increased CO2‐to‐O2 ratio leads to reduced de novo assimilation of nitrate, thus shifting the C/N balance. Metabolic modeling of acclimated and non‐acclimated plants revealed the photorespiratory pathway to function as a sink for already assimilated nitrogen during the light period, providing carbon skeletons for de novo assimilation. At high CO2, low photorespiratory activity resulted in diminished nitrogen assimilation and eventually resulted in reduced carbon assimilation. For the hpr1‐1 mutant, defective in reduction of hydroxy‐pyruvate, metabolic simulations show that turnover of photorespiratory metabolites is expanded into the night. Comparison of simulations for hpr1‐1 with those for the wild type allowed investigating the effect of a perturbed photorespiration on N‐assimilation.
Open Access
Cytosolic proline is required for basal freezing tolerance in Arabidopsis
(2021) Hoermiller, Imke I.; Funck, Dietmar; Schönewolf, Lilli; May, Henrik; Heyer, Arnd G.
The amino acid proline accumulates in many plant species under abiotic stress conditions, and various protective functions have been proposed. During cold stress, however, proline content in Arabidopsis thaliana does not correlate with freezing tolerance. Freezing sensitivity of a starchless plastidic phosphoglucomutase mutant (pgm) indicated that localization of proline in the cytosol might stabilize the plasma membrane during freeze-thaw events. Here, we show that re‐allocation of proline from cytosol to vacuole was similar in the pyrroline‐5‐carboxylate synthase 2-1 (p5cs2-1) mutant and the pgm mutant and caused similar reduction of basal freezing tolerance. In contrast, the starch excess 1-1 mutant (sex1‐1) had even lower freezing tolerance than pgm but did not affect sub‐cellular localization of proline. Freezing sensitivity of sex1‐1 mutants affected primarily the photosynthetic electron transport and was enhanced in a sex1‐1::p5cs2-1 double mutant. These findings indicate that several independent factors determine basal freezing tolerance. In a pgm::p5cs2-1 double mutant, freezing sensitivity and proline allocation to the vacuole were the same as in the parental lines, indicating that the lack of cytosolic proline was the common cause of reduced basal freezing tolerance in both mutants. We conclude that cytosolic proline is an important factor in freezing tolerance of non‐acclimated plants.
Open Access
Flux calculation for primary metabolism reveals changes in allocation of nitrogen to different amino acid families when photorespiratory activity changes
(2024) Friedrichs, Nils; Shokouhi, Danial; Heyer, Arnd G.
Photorespiration, caused by oxygenation of the enzyme Rubisco, is considered a wasteful process, because it reduces photosynthetic carbon gain, but it also supplies amino acids and is involved in amelioration of stress. Here, we show that a sudden increase in photorespiratory activity not only reduced carbon acquisition and production of sugars and starch, but also affected diurnal dynamics of amino acids not obviously involved in the process. Flux calculations based on diurnal metabolite profiles suggest that export of proline from leaves increases, while aspartate family members accumulate. An immense increase is observed for turnover in the cyclic reaction of glutamine synthetase/glutamine-oxoglutarate aminotransferase (GS/GOGAT), probably because of increased production of ammonium in photorespiration. The hpr1-1 mutant, defective in peroxisomal hydroxypyruvate reductase, shows substantial alterations in flux, leading to a shift from the oxoglutarate to the aspartate family of amino acids. This is coupled to a massive export of asparagine, which may serve in exchange for serine between shoot and root.
Open Access
Frosttoleranz bei Pflanzen - Fliehen, vermeiden oder einfach durchhalten!
(2005) Heyer, Arnd G.
Nur etwa ein Drittel der Fläche des Planeten Erde ist dauerhaft frostfrei: in den tropischen Regenwaldgebieten des Amazonasbeckens, in Kongo, an der afrikanischen Westküste, auf dem Indomalayischen Archipel, in einem kleinen Teil Australiens und auf den pazifischen Inseln in Äquatornähe fällt die Temperatur nie unter etwa 15 Grad. Der Temperaturunterschied zwischen Tag und Nacht ist hier größer als der zwischen Sommer und Winter. Fast die Hälfte aller Pflanzenarten – 115.000 von 250.000 bekannten Blütenpflanzen – kommen nur hier vor. Daraus lässt sich bereits ablesen, dass der Umgang mit niedrigen Temperaturen eine Herausforderung für lebende Organismen ist, der sich nicht jeder stellen mag. Andererseits locken die kälteren Gegenden mit einem großen Flächen- und Mineralstoffangebot – einer Ressource, die für Pflanzen äußerst attraktiv ist.
Open Access
Heat waves alter carbon allocation and increase mortality of Aleppo pine under dry conditions
(2018) Birami, Benjamin; Gattmann, Marielle; Heyer, Arnd G.; Grote, Rüdiger; Arneth, Almut; Ruehr, Nadine K.
Climate extremes are likely to occur more frequently in the future, including a combination of heat waves and drought. However, the responses of trees to combined stress and their post-stress recovery are not fully understood yet. Therefore, this study investigated the responses of semi-arid Pinus halepensis seedlings to moderate drought, heat and combined heat-drought stress, as well as post-stress recovery. The seedlings were grown under controlled conditions and exposed to two 4-days-long heat periods, reaching air temperature maxima of 42°C and vapor pressure deficit (VPD) of 7 kPa. Day- and nighttime canopy gas exchange was measured and differences in shoot and root allocation of non-structural carbohydrate (NSC) compounds (soluble sugars, starch, cyclitols, and carboxylic acids) assessed. Fluorescence parameters, nitrate levels, proline content and shoot water potential (ψ) provided additional indicators for stress severity and recovery performance. During the heat periods, net photosynthesis and stomatal conductance decreased immediately. This decline was modest under well-watered conditions, with transpiration and dark respiration rates remaining high and despite reductions in root NSC content, trees recovered following heat release. This was not the case in the heat-drought treatment, where stress resulted in high mortality rates and the few surviving seedlings showed reduced gas exchange rates and low root NSC content, while leaf nitrate and proline remained elevated even 3 weeks after heat release. Shoot ψ indicated that hydraulic failure was not the reason for mortality in the heat-drought seedlings. Instead, we argue that low transpiration rates, which resulted in needle temperatures >47°C during heat stress (6°C above air temperature) have caused irreversible damage. In summary, it could be demonstrated that heat waves in combination with moderate drought can either result in increased mortality or, if the seedlings survive, in delayed recovery. This highlights the potential of an increase in heat wave temperatures to trigger forest decline in semi-arid regions.
Open Access
Interaction of nitrate assimilation and photorespiration at elevated CO2
(2022) Krämer, Konrad; Brock, Judith; Heyer, Arnd G.
It has been shown repeatedly that exposure to elevated atmospheric CO2 causes an increased C/N ratio of plant biomass that could result from either increased carbon or - in relation to C acquisition - reduced nitrogen assimilation. Possible reasons for diminished nitrogen assimilation are controversial, but an impact of reduced photorespiration at elevated CO2 has frequently been implied. Using a mutant defective in peroxisomal hydroxy-pyruvate reductase (hpr1-1) that is hampered in photorespiratory turnover, we show that indeed, photorespiration stimulates the glutamine-synthetase 2 (GS) / glutamine-oxoglutarate-aminotransferase (GOGAT) cycle, which channels ammonia into amino acid synthesis. However, mathematical flux simulations demonstrated that nitrate assimilation was not reduced at elevated CO2, pointing to a dilution of nitrogen containing compounds by assimilated carbon at elevated CO2. The massive growth reduction in the hpr1-1 mutant does not appear to result from nitrogen starvation. Model simulations yield evidence for a loss of cellular energy that is consumed in supporting high flux through the GS/GOGAT cycle that results from inefficient removal of photorespiratory intermediates. This causes a futile cycling of glycolate and hydroxy-pyruvate. In addition to that, accumulation of serine and glycine as well as carboxylates in the mutant creates a metabolic imbalance that could contribute to growth reduction.
Open Access
Mathematical modeling of diurnal patterns of carbon allocation to shoot and root in Arabidopsis thaliana
(2019) Küstner, Lisa; Nägele, Thomas; Heyer, Arnd G.
We developed a mathematical model to simulate dynamics of central carbon metabolism over complete diurnal cycles for leaves of Arabidopsis thaliana exposed to either normal (120 µmol⋅m-2⋅s-1) or high light intensities (1200 µmol⋅m-2⋅s-1). The main objective was to obtain a high-resolution time series for metabolite dynamics as well as for shoot structural carbon formation (compounds with long residence time) and assimilate export of aerial organs to the sink tissue. Model development comprised a stepwise increment of complexity to finally approach the in vivo situation. The correct allocation of assimilates to either sink export or shoot structural carbon formation was a central goal of model development. Diurnal gain of structural carbon was calculated based on the daily increment in total photosynthetic carbon fixation, and this was the only parameter for structural carbon formation implemented in the model. Simulations of the dynamics of central metabolite pools revealed that shoot structural carbon formation occurred solely during the light phase but not during the night. The model allowed simulation of shoot structural carbon formation as a function of central leaf carbon metabolism under different environmental conditions without structural modifications. Model simulations were performed for the accession Landsberg erecta (Ler) and its hexokinase null-mutant gin2-1. This mutant displays a slow growth phenotype especially at increasing light intensities. Comparison of simulations revealed that the retarded shoot growth in the mutant resulted from an increased assimilate transport to sink organs. Due to its central function in sucrose cycling and sugar signaling, our findings suggest an important role of hexokinase-1 for carbon allocation to either shoot growth or assimilate export.
Open Access
Subcellular dynamics of proteins and metabolites under abiotic stress reveal deferred response of the Arabidopsis thaliana hexokinase-1 mutant gin2-1 to high light
(2019) Küstner, Lisa; Fürtauer, Lisa; Weckwerth, Wolfram; Nägele, Thomas; Heyer, Arnd G.
Stress responses in plants imply spatio‐temporal changes in enzymes and metabolites, including subcellular compartment‐specific re‐allocation processes triggered by sudden changes in environmental parameters. To investigate interactions of primary metabolism with abiotic stress, the gin2‐1 mutant, defective in the sugar sensor hexokinase 1 (HXK1) was compared with its wildtype Landsberg erecta (Ler) based on time resolved, compartment‐specific metabolome and proteome data obtained over a full diurnal cycle. The high light sensitive gin2‐1 mutant was substantially delayed in subcellular re‐distribution of metabolites upon stress, and this correlated with a massive reduction in proteins belonging to the ATP producing electron transport chain under high light, while fewer changes occurred in the cold. In the wildtype, compounds specifically protecting individual compartments could be identified, e.g., maltose and raffinose in plastids, myo‐inositol in mitochondria, but gin2‐1 failed to recruit these substances to the respective compartments, or responded only slowly to high irradiance. No such delay was obtained in the cold. At the whole cell level, concentrations of the amino acids, glycine and serine, provided strong evidence for an important role of the photorespiratory pathway during stress exposure, and different subcellular allocation of serine may contribute to the slow growth of the gin2‐1 mutant under high irradiance.
Open Access
A systems biology approach to analyse leaf carbohydrate metabolism in Arabidopsis thaliana
(2011) Henkel, Sebastian; Nägele, Thomas; Hörmiller, Imke; Sauter, Thomas; Sawodny, Oliver; Ederer, Michael; Heyer, Arnd G.
Plant carbohydrate metabolism comprises numerous metabolite interconversions, some of which form cycles of metabolite degradation and re-synthesis and are thus referred to as futile cycles. In this study, we present a systems biology approach to analyse any possible regulatory principle that operates such futile cycles based on experimental data for sucrose (Scr) cycling in photosynthetically active leaves of the model plant Arabidopsis thaliana. Kinetic parameters of enzymatic steps in Scr cycling were identified by fitting model simulations to experimental data. A statistical analysis of the kinetic parameters and calculated flux rates allowed for estimation of the variability and supported the predictability of the model. A principal component analysis of the parameter results revealed the identifiability of the model parameters. We investigated the stability properties of Scr cycling and found that feedback inhibition of enzymes catalysing metabolite interconversions at different steps of the cycle have differential influence on stability. Applying this observation to futile cycling of Scr in leaf cells points to the enzyme hexokinase as an important regulator, while the step of Scr degradation by invertases appears subordinate.