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Department of Plant Biotechnology
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Regulation of Primary Metabolism

Sink-Source Interactions

Department of Plant Biotechnology

How different organs of a plant can interact

Quantitatively, plants are the only relevant primary producers on earth. Thus, they constitute the base for all life on the planet. However, production is restricted to the light phase, because light provides energy for reduction of CO₂. During the night, plants themselfes consume reduced carbon to fuel maintenance of their organs.

The figure on the right shows a diurnal profile of CO₂ exchange of aerial organs in nmol/h*g fresh weight of an Arabidopsis thaliana plant during vegetative growth. The light phase starts at 8:00 am (480 min) and lasts until 4:00 pm (960 min). It becomse clear that during the light phase, more carbon is aquired than what is lost during the night. Thus, the aerial organs can export reduced carbon to supply sink organs like, e.g., the root. It is not easy to measure root respiration, because in soil, roots are associated with micro organisms that make a strong contribution to respiratory activity. We have developed a special technique to measure root respiration in an aeroponic system, and this allows us to study the full carbon balance of a plant over diurnal cycles.

During the light phase, plants produce carbohydrates that serve as building blocks for biomass and provide energy. Green leaves produce more carbohydrates than they need for their own metabolism, and they export the surplus to heterotrophic organs: young, growing leaves, roots that provide water and minerals, and flowers that asure reproduction.

Organs that export carbohydrates are called "sources", while those that import are called "sinks". Sources and sinks closely cooperate: only what is available can be consumed for growth and maintenance; but how much is produced also depends on demand.

We investigate, how supply and demand are regulated: do the sources dictate what will be available, or do they have to produce, what is needed?

In the relationship between sinks and sources, transport processes in the phloem, but also storage compounds play important roles. We investigate, if efficient storage of sugars in plant cells could stimulate photosynthesis. With respect to sugar storage, subcellular compartmentation is very important: while the large vacuole constitutes a nearly exhaustless reservoir, e.g., for fructans, storage of starch in the plastids can restrain photosynthesis. Nevertheless, in most plants, starch is the dominating carbon store. We investigate, how plants the detrmine the optimal amount of starch they produce to optimize diurnal change of light and dark phases.

Because carbohydrates function as transport as well as storage compounds, their diurnal dynamics are highly complex. To study organization of carbohydrate metabolism, we therefore use mathematical methods that allow simulation of non-intuitive processes.

A further level of complexity is given by the fact that carbohydrates also also involved in osmo-regulation of the cell. Thus, their concentrations are strongly influenced by environmental factors such as low temperature: during cold acclimation, large amounts of soluble sugars are accumulated that have protective functions. These environment interactions build another focus of our research.

Relevant Publications

Kraemer, K., Kepp, G., Brock, J., Stutz, S., Heyer, A.G.: Acclimation to elevated CO2 affects the C/N balance by reducing de novo N-assimilation. Physiologia Plantarum. 174, e13615 (2022). https://doi.org/10.1111/ppl.13615.
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@article{noauthororeditor2021acclimation, author = {Kraemer, Konrad and Kepp, Gabi and Brock, Judith and Stutz, Simon and Heyer, Arnd G.}, doi = {10.1111/ppl.13615}, journal = {Physiologia Plantarum}, number = 1, pages = {e13615}, title = {Acclimation to elevated CO2 affects the C/N balance by reducing de novo N-assimilation}, url = {https://onlinelibrary.wiley.com/doi/full/10.1111/ppl.13615}, volume = 174, year = 2022 }
Link
https://onlinelibrary.wiley.com/doi/full/10.1111/ppl.13615
Kraemer, K., Brock, J., Heyer, A.G.: Interaction of Nitrate Assimilation and Photorespiration at Elevated CO2. Frontiers in Plant Science. 13, (2022). https://doi.org/10.3389/fpls.2022.897924.
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@article{kraemer2022interaction, abstract = {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.}, author = {Kraemer, Konrad and Brock, Judith and Heyer, Arnd G.}, doi = {10.3389/fpls.2022.897924}, journal = {Frontiers in Plant Science}, month = {07}, title = {Interaction of Nitrate Assimilation and Photorespiration at Elevated CO2}, url = {https://www.frontiersin.org/article/10.3389/fpls.2022.897924}, volume = 13, year = 2022 }
Link
https://www.frontiersin.org/article/10.3389/fpls.2022.897924
Küstner, L., Nägele, T., Heyer, A.G.: Mathematical modeling of diurnal patterns of carbon allocation to shoot and root in Arabidopsis thaliana. npj Systems Biology and Applications. 5, 4-- (2019). https://doi.org/10.1038/s41540-018-0080-1.
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@article{kustner2019, abstract = {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.}, author = {Küstner, Lisa and Nägele, Thomas and Heyer, Arnd G.}, doi = {10.1038/s41540-018-0080-1}, issn = {20567189}, journal = {npj Systems Biology and Applications}, number = 1, pages = {4--}, refid = {Küstner2019}, title = {Mathematical modeling of diurnal patterns of carbon allocation to shoot and root in Arabidopsis thaliana}, url = {https://doi.org/10.1038/s41540-018-0080-1}, volume = 5, year = 2019 }
Link
https://doi.org/10.1038/s41540-018-0080-1
Küstner, L., Fürtauer, L., Weckwerth, W., Nägele, T., Heyer, A.G.: Subcellular dynamics of proteins and metabolites under abiotic stress reveal deferred response of the Arabidopsis thaliana hexokinase‐1 mutant gin2‐1 to high light. Plant Journal. 100, 456–472 (2019). https://doi.org/10.1111/tpj.14491.
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@article{kustner2019subcellular, abstract = {Stress responses in plants imply spatio‐temporal changes in enzymes and metabolites, including subcellular compartment‐specific reallocation 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 to 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 redistribution 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.}, author = {Küstner, Lisa and Fürtauer, Lisa and Weckwerth, Wolfram and Nägele, Thomas and Heyer, Arnd G.}, doi = {10.1111/tpj.14491}, journal = {Plant Journal}, month = {08}, pages = {456-472}, title = {Subcellular dynamics of proteins and metabolites under abiotic stress reveal deferred response of the Arabidopsis thaliana hexokinase‐1 mutant gin2‐1 to high light}, url = {https://doi.org/10.1111/tpj.14491}, volume = 100, year = 2019 }
Link
https://doi.org/10.1111/tpj.14491
Fürtauer, L., Küstner, L., Weckwerth, W., Heyer, A.G., Nägele, T.: Resolving subcellular plant metabolism. Plant Journal. 100, 438–455 (2019). https://doi.org/10.1111/tpj.14472.
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@article{furtauer2019resolving, abstract = {Plant cells are characterized by a high degree of compartmentalization and a diverse proteome and metabolome. Only a very limited number of studies has addressed combined subcellular proteomics and metabolomics which strongly limits biochemical and physiological interpretation of large‐scale omics data. Our study presents a methodological combination of non‐aqueous fractionation, shotgun proteomics, enzyme activities and metabolomics to reveal subcellular diurnal dynamics of plant metabolism. Subcellular marker protein sets were identified and enzymatically validated to resolve metabolism in a 4‐compartment model comprising chloroplasts, cytosol, vacuole and mitochondria. These marker sets are now available for future studies which aim to monitor subcellular metabolome and proteome dynamics. Comparing subcellular dynamics in wild type plants and HXK1‐deficient gin2‐1 mutants revealed a strong impact of HXK1 activity on metabolome dynamics in multiple compartments. Glucose accumulation in the cytosol of gin2‐1 was accompanied by diminished vacuolar glucose levels. Subcellular dynamics of pyruvate, succinate and fumarate amount was significantly affected in gin2‐1 which coincided with differential mitochondrial proteome dynamics. Lowered mitochondrial glycine and serine amount in gin2‐1 together with reduced abundance of photorespiratory proteins indicated an effect of the gin2‐1 mutation on photorespiratory capacity. Our findings highlight the necessity to resolve plant metabolism to a subcellular level in order to provide a causal relationship between metabolites, proteins and metabolic pathway regulation.}, author = {Fürtauer, Lisa and Küstner, Lisa and Weckwerth, Wolfram and Heyer, Arnd G. and Nägele, Thomas}, doi = {10.1111/tpj.14472}, journal = {Plant Journal}, month = {07}, pages = {438-455}, title = {Resolving subcellular plant metabolism}, url = {https://doi.org/10.1111/tpj.14472}, volume = 100, year = 2019 }
Link
https://doi.org/10.1111/tpj.14472
Brauner, K., Birami, B., Brauner, H.A., Heyer, A.G.: Diurnal periodicity of assimilate transport shapes resource allocation and whole-plant carbon balance. The Plant Journal. 94, 776–789 (2018). https://doi.org/10.1111/tpj.13898.
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@article{doi:10.1111/tpj.13898, abstract = {Summary Whole-plant carbon balance comprises diurnal fluctuations of photosynthetic carbon gain and respiratory losses, as well as partitioning of assimilates between phototrophic and heterotrophic organs. Because it is difficult to access, the root system is frequently neglected in growth models, or its metabolism is rated based on generalizations from other organs. Here, whole-plant cuvettes were used for investigating total-plant carbon exchange with the environment over full diurnal cycles. Dynamics of primary metabolism and diurnally resolved phloem exudation profiles, as proxy of assimilate transport, were combined to obtain a full picture of resource allocation. This uncovered a strong impact of periodicity of inter-organ transport on the efficiency of carbon gain. While a sinusoidal fluctuation of the transport rate, with minor diel deflections, minimized respiratory losses in Arabidopsis wild-type plants, triangular or rectangular patterns of transport, found in mutants defective in either starch or sucrose metabolism, increased root respiration at the end or beginning of the day, respectively. Power spectral density and cross-correlation analysis revealed that only the rate of starch synthesis was strictly correlated to the rate of net photosynthesis in wild-type, while in a sucrose-phosphate synthase mutant (spsa1), this applied also to carboxylate synthesis, serving as an alternative carbon pool. In the starchless mutant of plastidial phospho-gluco mutase (pgm), none of these rates, but concentrations of sucrose and glucose in the root, followed the pattern of photosynthesis, indicating direct transduction of shoot sugar levels to the root. The results demonstrate that starch metabolism alone is insufficient to buffer diurnal fluctuations of carbon exchange.}, author = {Brauner, Katrin and Birami, Benjamin and Brauner, Horst A. and Heyer, Arnd G.}, doi = {10.1111/tpj.13898}, eprint = {https://onlinelibrary.wiley.com/doi/pdf/10.1111/tpj.13898}, journal = {The Plant Journal}, number = 5, pages = {776-789}, title = {Diurnal periodicity of assimilate transport shapes resource allocation and whole-plant carbon balance}, url = {https://onlinelibrary.wiley.com/doi/abs/10.1111/tpj.13898}, volume = 94, year = 2018 }
Link
https://onlinelibrary.wiley.com/doi/abs/10.1111/tpj.13898
Birami, B., Gattmann, M., Heyer, A.G., Grote, R., Arneth, A., Ruehr, N.: Heat waves alter carbon allocation and increase mortality of Aleppo pine under dry conditions. Frontiers in Forests and Global Change. 1, 8 (2018). https://doi.org/doi: 10.3389/ffgc.2018.00008.
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@article{birami2018waves, abstract = {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 investigates 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-day-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 decrease 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 mortality was high and the few surviving seedlings showed reduced gas exchange rates and low root NSC content, while leaf nitrate and proline remained elevated even three weeks after heat release. Shoot ψ indicated that hydraulic failure was not the reason for mortality in the heat-drought exposed seedlings. Instead, we hypothesize that low transpiration rates, which resulted in needle temperatures >47 °C during heat stress (6 °C above air temperature) have led to 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.}, author = {Birami, Benjamin and Gattmann, Marielle and Heyer, Arnd G. and Grote, Rüdiger and Arneth, Almut and Ruehr, Nadine}, day = 27, doi = {doi: 10.3389/ffgc.2018.00008}, journal = {Frontiers in Forests and Global Change}, month = {11}, pages = 8, title = {Heat waves alter carbon allocation and increase mortality of Aleppo pine under dry conditions}, url = {https://www.frontiersin.org/articles/10.3389/ffgc.2018.00008/abstract}, volume = 1, year = 2018 }
Link
https://www.frontiersin.org/articles/10.3389/ffgc.2018.00008/abstract
Brauner, K., Stutz, S., Paul, M., Heyer, A.G.: Measuring whole plant CO2 exchange with the environment reveals opposing effects of the gin2–1 mutation in shoots and roots of Arabidopsis thaliana. Plant Signaling Behav. 10, e973822 (2015). https://doi.org/10.4161/15592324.2014.973822.
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@article{Brauner2015, abstract = { Using a cuvette for simultaneous measurement of net photosynthesis in above ground plant organs and root respiration we investigated the effect of reduced leaf glucokinase activity on plant carbon balance. The gin2–1 mutant of Arabidopsis thaliana is characterized by a 50\% reduction of glucokinase activity in the shoot, while activity in roots is about fivefold higher and similar to wild type plants. High levels of sucrose accumulating in leaves during the light period correlated with elevated root respiration in gin2–1. Despite substantial respiratory losses in roots, growth retardation was moderate, probably because photosynthetic carbon fixation was simultaneously elevated in gin2–1. Our data indicate that futile cycling of sucrose in shoots exerts a reduction on net CO2 gain, but this is over-compensated by the prevention of exaggerated root respiration resulting from high sucrose concentration in leaf tissue. }, author = {Brauner, Katrin and Stutz, Simon and Paul, Martin and Heyer, Arnd G}, doi = {10.4161/15592324.2014.973822}, eprint = {http://dx.doi.org/10.4161/15592324.2014.973822}, journal = {Plant Signaling Behav.}, note = {PMID: 25482780}, number = 1, pages = {e973822}, title = {Measuring whole plant CO2 exchange with the environment reveals opposing effects of the gin2–1 mutation in shoots and roots of Arabidopsis thaliana}, url = {http://dx.doi.org/10.4161/15592324.2014.973822 }, volume = 10, year = 2015 }
Link
http://dx.doi.org/10.4161/15592324.2014.973822
Brauner, K., Hörmiller, I., Nägele, T., Heyer, A.G.: Exaggerated root respiration accounts for growth retardation in a starchless mutant of Arabidopsis thaliana. Plant J. 79, 82--91 (2014). https://doi.org/10.1111/tpj.12555.
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@article{Brauner2014, abstract = {The knock-out mutation of plastidial phosphoglucomutase (pgm) causes a starchless phenotype in Arabidopsis thaliana, and results in a severe growth reduction of plants cultivated under diurnal conditions. It has been speculated that high soluble sugar levels accumulating during the light phase in leaf mesophyll might cause a reduction of photosynthetic activity or that shortage of reduced carbon during the night is the reason for the slow biomass gain of pgm. Separate simultaneous measurements of leaf net photosynthesis and root respiration demonstrate that photosynthetic activity per unit fresh weight is not reduced in pgm, whereas root respiration is strongly elevated. Comparison with a mutant defective in the dominating vacuolar invertase (AtβFruct4) revealed that high sucrose concentration in the cytosol, but not in the vacuole, of leaf cells is responsible for elevated assimilate transport to the root. Increased sugar supply to the root, as observed in pgm mutants, forces substantial respiratory losses. Because root respiration accounts for 80% of total plant respiration under long-day conditions, this gives rise to retarded biomass formation. In contrast, reduced vacuolar invertase activity leads to reduced net photosynthesis in the shoot and lowered root respiration, and affords an increased root/shoot ratio. The results demonstrate that roots have very limited capacity for carbon storage but exert rigid control of supply for their maintenance metabolism.}, author = {Brauner, Katrin and Hörmiller, Imke and Nägele, Thomas and Heyer, Arnd G.}, doi = {10.1111/tpj.12555}, issn = {1365-313X}, journal = {Plant J.}, number = 1, owner = {heyer}, pages = {82--91}, title = {Exaggerated root respiration accounts for growth retardation in a starchless mutant of \textit{Arabidopsis thaliana}}, url = {http://dx.doi.org/10.1111/tpj.12555}, volume = 79, year = 2014 }
Link
http://dx.doi.org/10.1111/tpj.12555
Nägele, T., Stutz, S., Hörmiller, I.I., Heyer, A.G.: Identification of a metabolic bottleneck for cold acclimation in Arabidopsis thaliana. Plant J. 72, 102–114 (2012). https://doi.org/10.1111/j.1365-313X.2012.05064.x.
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@article{Naegele2012a, abstract = {Central carbohydrate metabolism of Arabidopsis thaliana is known to play a crucial role during cold acclimation and the acquisition of freezing tolerance. During cold exposure, many carbohydrates accumulate and a new metabolic homeostasis evolves. In the present study, we analyse the diurnal dynamics of carbohydrate homeostasis before and after cold exposure in three natural accessions showing distinct cold acclimation capacity. Diurnal dynamics of soluble carbohydrates were found to be significantly different in cold-sensitive and cold-tolerant accessions. Although experimentally determined maximum turnover rates for sucrose phosphate synthase in cold-acclimated leaves were higher for cold-tolerant accessions, model simulations of diurnal carbohydrate dynamics revealed similar fluxes. This implied a significantly higher capacity for sucrose synthesis in cold-tolerant than cold-sensitive accessions. Based on this implication resulting from mathematical model simulation, a critical temperature for sucrose synthesis was calculated using the Arrhenius equation and experimentally validated in the cold-sensitive accession C24. At the critical temperature suggested by model simulation, an imbalance in photosynthetic carbon fixation ultimately resulting in oxidative stress was observed. It is therefore concluded that metabolic capacities at least in part determine the ability of accessions of Arabidopsis thaliana to cope with changes in environmental conditions}, author = {Nägele, T. and Stutz, Simon and Hörmiller, Imke I. and Heyer, Arnd G.}, doi = {10.1111/j.1365-313X.2012.05064.x}, issn = {1365-313X}, journal = {Plant J.}, month = {05}, number = 102, owner = {heyer}, pages = {102-114}, refid = {44}, title = {Identification of a metabolic bottleneck for cold acclimation in \textit{Arabidopsis thaliana}}, url = {http://dx.doi.org/10.1111/j.1365-313X.2012.05064.x}, volume = 72, year = 2012 }
Link
http://dx.doi.org/10.1111/j.1365-313X.2012.05064.x
Zuther, E., Hoermiller, I.I., Heyer, A.G.: Evidence against sink limitation by the sucrose-to-starch route in potato plants expressing fructosyltransferases. Physiol. Plant. 143, 115--125 (2011). https://doi.org/10.1111/j.1399-3054.2011.01495.x.
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@article{Zuther2011, abstract = {To investigate whether the route from sucrose to starch limits sink strength of potato tubers, we established an additional storage carbohydrate pool and analyzed allocation of imported assimilates to the different pools. Tuber specific expression of the fructan biosynthetic enzymes of globe artichoke resulted in accumulation of fructans to about 5% of the starch level, but did not increase tuber dry weight per plant. While partial repression of starch synthesis caused yield reduction in wild-type plants, it stimulated fructan accumulation, and yield losses were ameliorated in tubers expressing fructosyltransferases. However, a nearly complete block of the starch pathway by inhibition of sucrose synthase could not be compensated by the fructan pathway. Although fructan concentrations rose, yield reduction was even enhanced, probably because of a futile cycle of fructan synthesis and degradation by invertase, which is induced when sucrose synthase is knocked out. The data do not support a limitation of sink strength by enzyme activities of the starch pathway but point to an energy limitation of storage carbohydrate formation in potato tubers.}, author = {Zuther, Ellen and Hoermiller, Imke I. and Heyer, Arnd G.}, doi = {10.1111/j.1399-3054.2011.01495.x}, issn = {1399-3054}, journal = {Physiol. Plant.}, number = 2, pages = {115--125}, publisher = {Blackwell Publishing Ltd}, title = {Evidence against sink limitation by the sucrose-to-starch route in potato plants expressing fructosyltransferases}, url = {http://dx.doi.org/10.1111/j.1399-3054.2011.01495.x}, volume = 143, year = 2011 }
Link
http://dx.doi.org/10.1111/j.1399-3054.2011.01495.x
Wingenter, K., Trentmann, O., Winschuh, I., Hörmiller, I.I., Heyer, A.G., Reinders, J., Schulz, A., Geiger, D., Hedrich, R., Neuhaus, H.E.: A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake. Plant J. 68, 890--900 (2011). https://doi.org/10.1111/j.1365-313X.2011.04739.x.
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@article{Wingenter2011, abstract = {Vacuolar solute accumulation is an important process during plant development, growth and stress responses. Although several vacuolar carriers have been identified recently, knowledge regarding the regulation of transport is still limited. Solute accumulation may be controlled by various factors, such as alterations in carrier abundance or activity. Phosphorylation via kinases is a well-known principle for activation or deactivation of proteins. Several phosphorylated proteins have been identified in the tonoplast proteome; however, kinases that catalyse the phosphorylation of tonoplast proteins are currently unknown. The tonoplast monosaccaride transporter from Arabidopsis (AtTMT1) and its homologue from barley have multiple phosphorylation sites in their extremely large loops. Here we demonstrate that the loop of AtTMT1 interacts with a mitogen-activated triple kinase-like protein kinase (VIK), that an aspartate-rich loop domain is required for effective interaction, and that the presence of VIK stimulates glucose import into isolated vacuoles. Furthermore, the phenotype of VIK loss-of-function plants strikingly resembles that of plants lacking AtTMT1/2. These data suggest that VIK-mediated phosphorylation of the AtTMT1 loop enhances carrier activity and consequently vacuolar sugar accumulation. As many phosphorylated proteins have been identified in the tonoplast, differential phosphorylation may be a general mechanism regulating vacuolar solute import.}, author = {Wingenter, Karina and Trentmann, Oliver and Winschuh, Irina and Hörmiller, Imke I. and Heyer, Arnd G. and Reinders, Jörg and Schulz, Alexander and Geiger, Dietmar and Hedrich, Rainer and Neuhaus, H. Ekkehard}, doi = {10.1111/j.1365-313X.2011.04739.x}, issn = {1365-313X}, journal = {Plant J.}, number = 5, pages = {890--900}, publisher = {Blackwell Publishing Ltd}, title = {A member of the mitogen-activated protein 3-kinase family is involved in the regulation of plant vacuolar glucose uptake}, url = {http://dx.doi.org/10.1111/j.1365-313X.2011.04739.x}, volume = 68, year = 2011 }
Link
http://dx.doi.org/10.1111/j.1365-313X.2011.04739.x
Henkel, S., Nägele, T., Hörmiller, I., Sauter, T., Sawodny, O., Ederer, M., Heyer, A.G.: A systems biology approach to analyse leaf carbohydrate metabolism in Arabidopsis thaliana. EURASIP Journal on Bioinformatics and Systems Biology. 2011, 2 (2011). https://doi.org/10.1186/1687-4153-2011-2.
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@article{Henkel_2011, author = {Henkel, Sebastian and Nägele, Thomas and Hörmiller, Imke and Sauter, Thomas and Sawodny, Oliver and Ederer, Michael and Heyer, Arnd G}, doi = {10.1186/1687-4153-2011-2}, journal = {{EURASIP} Journal on Bioinformatics and Systems Biology}, month = {06}, number = 1, pages = 2, publisher = {Springer Nature}, title = {A systems biology approach to analyse leaf carbohydrate metabolism in Arabidopsis thaliana}, url = {https://doi.org/10.1186%2F1687-4153-2011-2}, volume = 2011, year = 2011 }
Link
https://doi.org/10.1186%2F1687-4153-2011-2
Wingenter, K., Schulz, A., Wormit, A., Wic, S., Trentmann, O., Hoermiller, I.I., Heyer, A.G., Marten, I., Hedrich, R., Neuhaus, H.E.: Increased Activity of the Vacuolar Monosaccharide Transporter TMT1 Alters Cellular Sugar Partitioning, Sugar Signaling, and Seed Yield in Arabidopsis. Plant Physiol. 154, 665--677 (2010). https://doi.org/10.1104/pp.110.162040.
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@article{Wingenter2010, abstract = {The extent to which vacuolar sugar transport activity affects molecular, cellular, and developmental processes in Arabidopsis (Arabidopsis thaliana) is unknown. Electrophysiological analysis revealed that overexpression of the tonoplast monosaccharide transporter TMT1 in a tmt1-2::tDNA mutant led to increased proton-coupled monosaccharide import into isolated mesophyll vacuoles in comparison with wild-type vacuoles. TMT1 overexpressor mutants grew faster than wild-type plants on soil and in high-glucose (Glc)-containing liquid medium. These effects were correlated with increased vacuolar monosaccharide compartmentation, as revealed by nonaqueous fractionation and by chlorophyll(ab)-binding protein1 and nitrate reductase1 gene expression studies. Soil-grown TMT1 overexpressor plants respired less Glc than wild-type plants and only about half the amount of Glc respired by tmt1-2::tDNA mutants. In sum, these data show that TMT activity in wild-type plants limits vacuolar monosaccharide loading. Remarkably, TMT1 overexpressor mutants produced larger seeds and greater total seed yield, which was associated with increased lipid and protein content. These changes in seed properties were correlated with slightly decreased nocturnal CO2 release and increased sugar export rates from detached source leaves. The SUC2 gene, which codes for a sucrose transporter that may be critical for phloem loading in leaves, has been identified as Glc repressed. Thus, the observation that SUC2 mRNA increased slightly in TMT1 overexpressor leaves, characterized by lowered cytosolic Glc levels than wild-type leaves, provided further evidence of a stimulated source capacity. In summary, increased TMT activity in Arabidopsis induced modified subcellular sugar compartmentation, altered cellular sugar sensing, affected assimilate allocation, increased the biomass of Arabidopsis seeds, and accelerated early plant development}, author = {Wingenter, K. and Schulz, A. and Wormit, A. and Wic, S. and Trentmann, O. and Hoermiller, I.I. and Heyer, A.G. and Marten, I. and Hedrich, R. and Neuhaus, H.E.}, comment = {J}, doi = {10.1104/pp.110.162040}, issn = {0032-0889}, journal = {Plant Physiol.}, number = 2, owner = {heyer}, pages = {665--677}, privnote = {J}, refid = {38}, title = {Increased Activity of the Vacuolar Monosaccharide Transporter TMT1 Alters Cellular Sugar Partitioning, Sugar Signaling, and Seed Yield in \textit{Arabidopsis}}, url = {http://www.plantphysiol.org/content/154/2/665}, volume = 154, year = 2010 }
Link
http://www.plantphysiol.org/content/154/2/665
Nägele, T., Henkel, S., Hörmiller, I., Sauter, T., Sawodny, O., Ederer, M., Heyer, A.G.: Mathematical modeling of the central carbohydrate metabolism in Arabidopsis reveals a substantial regulatory influence of vacuolar invertase on whole plant carbon metabolism. Plant Physiol. 153, 260--272 (2010). https://doi.org/10.1104/pp.110.154443.
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@article{Naegele2010, abstract = {A mathematical model representing metabolite interconversions in the central carbohydrate metabolism of Arabidopsis (Arabidopsis thaliana) was developed to simulate the diurnal dynamics of primary carbon metabolism in a photosynthetically active plant leaf. The model groups enzymatic steps of central carbohydrate metabolism into blocks of interconverting reactions that link easily measurable quantities like CO2 exchange and quasi-steady-state levels of soluble sugars and starch. When metabolite levels that fluctuate over diurnal cycles are used as a basic condition for simulation, turnover rates for the interconverting reactions can be calculated that approximate measured metabolite dynamics and yield kinetic parameters of interconverting reactions. We used experimental data for Arabidopsis wild-type plants, accession Columbia, and a mutant defective in vacuolar invertase, At beta Fruct4, as input data. Reducing invertase activity to mutant levels in the wild-type model led to a correct prediction of increased sucrose levels. However, additional changes were needed to correctly simulate levels of hexoses and sugar phosphates, indicating that invertase knockout causes subsequent changes in other enzymatic parameters. Reduction of invertase activity caused a decline in photosynthesis and export of reduced carbon to associated metabolic pathways and sink organs (e. g. roots), which is in agreement with the reported contribution of vacuolar invertase to sink strength. According to model parameters, there is a role for invertase in leaves, where futile cycling of sucrose appears to have a buffering effect on the pools of sucrose, hexoses, and sugar phosphates. Our data demonstrate that modeling complex metabolic pathways is a useful tool to study the significance of single enzyme activities in complex, nonintuitive networks}, author = {Nägele, T. and Henkel, S. and Hörmiller, I. and Sauter, T. and Sawodny, O. and Ederer, M. and Heyer, A.G.}, comment = {J}, doi = {10.1104/pp.110.154443}, issn = {0032-0889}, journal = {Plant Physiol.}, number = 1, owner = {heyer}, pages = {260--272}, privnote = {J}, refid = {39}, title = {Mathematical modeling of the central carbohydrate metabolism in \textit{Arabidopsis} reveals a substantial regulatory influence of vacuolar invertase on whole plant carbon metabolism}, url = {http://www.plantphysiol.org/content/153/1/260?keytype=ref&ijkey=fjFkF7ugYYBybHo}, volume = 153, year = 2010 }
Link
http://www.plantphysiol.org/content/153/1/260?keytype=ref&ijkey=fjFkF7ugYYBybHo
Livingston, D.P., Hincha, D.K., Heyer, A.G.: Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences. 66, 2007--2023 (2009). https://doi.org/10.1007/s00018-009-0002-x.
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@article{Livingston2009, abstract = {Numerous studies have been published that attempted to correlate fructan concentrations with freezing and drought tolerance. Studies investigating the effect of fructan on liposomes indicated that a direct interaction between membranes and fructan was possible. This new area of research began to move fructan and its association with stress beyond mere correlation by confirming that fructan has the capacity to stabilize membranes during drying by inserting at least part of the polysaccharide into the lipid headgroup region of the membrane. This helps prevent leakage when water is removed from the system either during freezing or drought. When plants were transformed with the ability to synthesize fructan, a concomitant increase in drought and/or freezing tolerance was confirmed. These experiments indicate that besides an indirect effect of supplying tissues with hexose sugars, fructan has a direct protective effect that can be demonstrated by both model systems and genetic transformation.}, author = {Livingston, David P. and Hincha, Dirk K. and Heyer, Arnd G.}, day = 01, doi = {10.1007/s00018-009-0002-x}, issn = {1420-9071}, journal = {Cellular and Molecular Life Sciences}, month = {07}, number = 13, pages = {2007--2023}, title = {Fructan and its relationship to abiotic stress tolerance in plants}, url = {https://doi.org/10.1007/s00018-009-0002-x}, volume = 66, year = 2009 }
Link
https://doi.org/10.1007/s00018-009-0002-x
Hincha, D.K., Livingston, D.P., Premakumar, R., Zuther, E., Obel, N., Cacela, C., Heyer, A.G.: Fructans from oat and rye: Composition and effects on membrane stability during drying. Biochimica et Biophysica Acta (BBA) - Biomembranes. 1768, 1611--1619 (2007). https://doi.org/10.1016/j.bbamem.2007.03.011.
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@article{Hincha_2007, author = {Hincha, Dirk K. and Livingston, David P. and Premakumar, Ramaswamy and Zuther, Ellen and Obel, Nicolai and Cacela, Constan{\c{c}}a and Heyer, Arnd G.}, doi = {10.1016/j.bbamem.2007.03.011}, journal = {Biochimica et Biophysica Acta ({BBA}) - Biomembranes}, month = {06}, number = 6, pages = {1611--1619}, publisher = {Elsevier {BV}}, title = {Fructans from oat and rye: Composition and effects on membrane stability during drying}, url = {https://doi.org/10.1016%2Fj.bbamem.2007.03.011}, volume = 1768, year = 2007 }
Link
https://doi.org/10.1016%2Fj.bbamem.2007.03.011
Hannah, M.A., Kramer, K.M., Geffroy, V., Kopka, J., Blair, M.W., Erban, A., Vallejos, C.E., Heyer, A.G., Sanders, F.E.T., Millner, P.A., Pilbeam, D.J.: Hybrid weakness controlled by the dosage-dependent lethal (DL) gene system in common bean (Phaseolus vulgaris) is caused by a shoot-derived inhibitory signal leading to salicylic acid-associated root death. New Phytol. 176, 537--549 (2007). https://doi.org/10.1111/j.1469-8137.2007.02215.x.
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@article{Hannah2007, abstract = {Certain crosses of common bean (Phaseolus vulgaris) result in temperature-dependent hybrid weakness associated with a severe root phenotype. This is controlled by the interaction of the root- and shoot-expressed semidominant alleles dosage-dependent lethal 1 (DL1) and DL2, which communicate via long-distance signaling. Previously, apparent reciprocal effects on root growth and the restoration of normal root growth by exogenous sucrose led to the hypothesis that the dosage-dependent lethal (DL) system may control root-shoot carbon partitioning. Here, recombinant inbred lines were used to map the DL loci and physiological and biochemical analysis, including metabolite profiling, was used to gain new insights into the signaling interaction and the root phenotype. It is shown that the DL system does not control root-shoot carbon partitioning and that roots are unlikely to die from carbon starvation. Instead, root death likely occurs by defense-related programmed cell death, as indicated by salicylic acid accumulation. DL2-expressing cotyledons supply a potent inhibitory signal that is sufficient to cause such death in DL1-expressing roots. These data implicate the DL system in defense-related signaling and provide support for the recent hypothesis of defense-related autoimmunity as a potential isolating mechanism in plant speciation, in particular, setting a precedence for the potential roles of long-distance signaling and temperature dependence. [References: 38]}, author = {Hannah, M.A. and Kramer, K.M. and Geffroy, V. and Kopka, J. and Blair, M.W. and Erban, A. and Vallejos, C.E. and Heyer, A.G. and Sanders, F.E.T. and Millner, P.A. and Pilbeam, D.J.}, comment = {DB - Current Contents PT - Article <4>}, doi = {10.1111/j.1469-8137.2007.02215.x}, journal = {New Phytol.}, number = 3, owner = {heyer}, pages = {537--549}, privnote = {DB - Current Contents PT - Article <4>}, refid = {3}, title = {Hybrid weakness controlled by the dosage-dependent lethal (DL) gene system in common bean (\textit{Phaseolus vulgaris}) is caused by a shoot-derived inhibitory signal leading to salicylic acid-associated root death}, url = {https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/j.1469-8137.2007.02215.x}, volume = 176, year = 2007 }
Link
https://nph.onlinelibrary.wiley.com/doi/abs/10.1111/j.1469-8137.2007.02215.x
Hannah, M.A., Zuther, E., Buchel, K., Heyer, A.G.: Transport and metabolism of raffinose family oligosaccharides in transgenic potato. J. Exp. Bot. 57, 3801--3811 (2006). https://doi.org/10.1093/jxb/erl152.
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@article{Hannah2006a, abstract = {Raffinose family oligosaccharides (RFOs) are involved in the storage and transport of carbon and serve as compatible solutes for protection against abiotic stresses like drought or cold. RFOs are usually transported in plant species that load sugars symplastically into the phloem. Loading probably occurs by a polymer trapping mechanism which establishes a concentration gradient of assimilates between the mesophyll and the vasculature. Transgenic approaches have demonstrated phloem transport of small molecules produced in the companion cells of apoplastic loading species, but these molecules have been non-native transport substances to plants. In this study, transgenic potato plants with constitutive or companion cell specific overexpression of galactinol synthase (GS) or GS plus raffinose synthase (RS) are characterized, which together provide new insights into the metabolism and transport of RFOs in plants. It is demonstrated that raffinose and galactinol are both transported in the phloem and that, whilst the effect of GS overexpression is promoter-independent, that of RS is dependent on the promoter used. The presence of significant amounts of galactinol in the phloem is shown and also that transgenic potato is unable to transport large amounts of raffinose despite high RS expression and substrate concentrations. These data indicate that there may be additional features of intermediary cells, the specialized companion cells of RFO transporting plants, required for significant RFO synthesis and transport that are currently not well-understood. [References: 35]}, author = {Hannah, M.A. and Zuther, E. and Buchel, K. and Heyer, A.G.}, comment = {DB - Current Contents PT - Article <5>}, doi = {10.1093/jxb/erl152}, journal = {J. Exp. Bot.}, month = {11}, number = 14, owner = {heyer}, pages = {3801--3811}, privnote = {DB - Current Contents PT - Article <5>}, refid = {4}, title = {Transport and metabolism of raffinose family oligosaccharides in transgenic potato}, url = {https://academic.oup.com/jxb/article/57/14/3801/586863}, volume = 57, year = 2006 }
Link
https://academic.oup.com/jxb/article/57/14/3801/586863
Zuther, E., Kwart, M., Willmitzer, L., Heyer, A.G.: Expression of a yeast-derived invertase in companion cells results in long-distance transport of a trisaccharide in an apoplastic loader and influences sucrose transport. Planta. 218, 759--766 (2004). https://doi.org/10.1007/s00425-003-1148-7.
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@article{Zuther2004, abstract = {Companion cell-specific expression of a cytosolic invertase from yeast (Saccharomyces cerevisiae) was used as a tool to synthesise oligosaccharides in the sieve element/companion cell complex and study whether oligosaccharides could be transported in the phloem of an apoplastically loading species. Potato (Solanum tuberosum L.) plants expressing the invertase under the control of the Agrobacterium tumefaciens rolC promoter produced the trisaccharide 6-kestose in leaves, which was transported via the phloem and accumulated in tubers of transgenic plants. In graft experiments with rolC invertase plants as scion and wild-type rootstocks, 6-kestose accumulated in tubers to levels comparable to sucrose. This shows that long-distance transport of oligosaccharides is possible in apoplastically loading plants, which normally transport only sucrose. The additional transport route for assimilates neither led to elevated photosynthetic activity nor to increased tuber yield. Enhanced sucrose turnover in companion cells caused large amounts of glucose and fructose to be exuded from leaf petioles, and elevated levels of sucrose were detected in phloem exudates. While the latter indicates a higher capacity for sucrose loading into the phloem due to increased metabolic activity of companion cells, the massive release of hexoses catalysed by the invertase seemed to interfere with assimilate delivery to sink organs.}, author = {Zuther, Ellen and Kwart, Marion and Willmitzer, Lothar and Heyer, Arnd G.}, day = 01, doi = {10.1007/s00425-003-1148-7}, issn = {1432-2048}, journal = {Planta}, month = {03}, number = 5, pages = {759--766}, title = {Expression of a yeast-derived invertase in companion cells results in long-distance transport of a trisaccharide in an apoplastic loader and influences sucrose transport}, url = {https://doi.org/10.1007/s00425-003-1148-7}, volume = 218, year = 2004 }
Link
https://doi.org/10.1007/s00425-003-1148-7
Heyer, A.G., Raap, M., Schroeer, B., Marty, B., Willmitzer, L.: Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana. Plant Journal. 39, 161–169 (2004). https://doi.org/10.1111/j.1365-313X.2004.02124.x.
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@article{noauthororeditor, abstract = {Summary Resource allocation is a major determinant of plant fitness and is influenced by external as well as internal stimuli. We have investigated the effect of cell wall invertase activity on the transition from vegetative to reproductive growth, inflorescence architecture, and reproductive output, i.e. seed production, in the model plant Arabidopsis thaliana by expressing a cell wall invertase under a meristem-specific promoter. Increased cell wall invertase activity causes accelerated flowering and an increase in seed yield by nearly 30\%. This increase is caused by an elevation of the number of siliques, which results from enhanced branching of the inflorescence. On the contrary, as cytosolic enzyme, the invertase causes delayed flowering, reduced seed yield, and branching. This demonstrates that invertases not only are important in determining sink strength of storage organs but also play a role in regulating developmental processes.}, author = {Heyer, Arnd G. and Raap, Maik and Schroeer, Birgit and Marty, Bruno and Willmitzer, Lothar}, doi = {10.1111/j.1365-313X.2004.02124.x}, journal = {Plant Journal}, number = 2, pages = {161-169}, title = {Cell wall invertase expression at the apical meristem alters floral, architectural, and reproductive traits in Arabidopsis thaliana}, url = {https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02124.x}, volume = 39, year = 2004 }
Link
https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-313X.2004.02124.x
Heyer, A.G., Wendenburg, R.: Gene Cloning and Functional Characterization by Heterologous Expression of the Fructosyltransferase of Aspergillus sydowi IAM 2544. Applied and Environmental Microbiology. 67, 363–370 (2001). https://doi.org/10.1128/AEM.67.1.363-370.2001.
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@article{heyer2001, abstract = {We have purified a fructosyltransferase from conidia of the inulin-producing fungus Aspergillus sydowi IAM 2544 and obtained peptide sequences from proteolytic fragments of the protein. With degenerated primers, we amplified a PCR fragment that was used to screen a cDNA library. The fructosyltransferase gene fromAspergillus sydowi (EMBL accession no. AJ289046) is expressed in conidia, while no expression could be detected in mycelia by Northern blot analysis of mycelial RNA. The gene encodes a protein with a calculated molecular mass of 75 kDa that is different from all fructosyltransferases in the databases. The only homology that could be detected was to the invertase of Aspergillus niger (EMBL accession no. L06844). The gene was functionally expressed inEscherichia coli, yeast, and potato plants. With protein extracts from transgenic bacteria and yeast, fructooligosaccharides could be produced in vitro. In transgenic potato plants, inulin molecules of up to 40 hexose units were synthesized in vivo. While in vitro experiments with protein extracts from conidia ofAspergillus sydowi yielded the same pattern of oligosaccharides as extracts from transformed bacteria and yeast, in vivo inulin synthesis with fungal conidia leads to the production of a high-molecular-weight polymer. }, author = {Heyer, Arnd G. and Wendenburg, Regina}, doi = {10.1128/AEM.67.1.363-370.2001}, journal = {Applied and Environmental Microbiology}, pages = {363-370}, series = 1, title = {Gene Cloning and Functional Characterization by Heterologous Expression of the Fructosyltransferase of Aspergillus sydowi IAM 2544}, url = {https://aem.asm.org/content/aem/67/1/363.full.pdf}, volume = 67, year = 2001 }
Link
https://aem.asm.org/content/aem/67/1/363.full.pdf
Wolff, D., Czapla, S., Heyer, A.G., Radosta, S., Mischnick, P., Springer, J.: Globular shape of high molar mass inulin revealed by static light scattering and viscometry. Polymer. 41, 8009--8016 (2000). https://doi.org/10.1016/s0032-3861(00)00168-3.
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@article{Wolff_2000, author = {Wolff, D. and Czapla, S. and Heyer, A.G. and Radosta, S. and Mischnick, P. and Springer, J.}, doi = {10.1016/s0032-3861(00)00168-3}, journal = {Polymer}, month = {10}, number = 22, pages = {8009--8016}, publisher = {Elsevier {BV}}, title = {Globular shape of high molar mass inulin revealed by static light scattering and viscometry}, url = {https://doi.org/10.1016%2Fs0032-3861%2800%2900168-3}, volume = 41, year = 2000 }
Link
https://doi.org/10.1016%2Fs0032-3861%2800%2900168-3
Hellwege, E.M., Czapla, S., Jahnke, A., Willmitzer, L., Heyer, A.G.: Transgenic potato (Solanum tuberosum) tubers synthesize the full spectrum of inulin molecules naturally occurring in globe artichoke (Cynara scolymus) roots. Proceedings of the National Academy of Sciences. 97, 8699–8704 (2000). https://doi.org/10.1073/pnas.150043797.
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@article{hellwege2000, abstract = {The ability to synthesize high molecular weight inulin was transferred to potato plants via constitutive expression of the 1-SST (sucrose:sucrose 1-fructosyltransferase) and the 1-FFT (fructan: fructan 1-fructosyltransferase) genes of globe artichoke (Cynara scolymus). The fructan pattern of tubers from transgenic potato plants represents the full spectrum of inulin molecules present in artichoke roots as shown by high-performance anion exchange chromatography, as well as size exclusion chromatography. These results demonstrate in planta that the enzymes sucrose:sucrose 1-fructosyltransferase and fructan:fructan 1-fructosyltransferase are sufficient to synthesize inulin molecules of all chain lengths naturally occurring in a given plant species. Inulin made up 5% of the dry weight of transgenic tubers, and a low level of fructan production also was observed in fully expanded leaves. Although inulin accumulation did not influence the sucrose concentration in leaves or tubers, a reduction in starch content occurred in transgenic tubers, indicating that inulin synthesis did not increase the storage capacity of the tubers. 1-SST,sucrose:sucrose 1-fructosyltransferase;1-FFT,fructan:fructan 1-fructosyltransferase;HPAEC,high-performance anion exchange chromatography;SEC,size exclusion chromatography;DP,degree of polymerization }, author = {Hellwege, Elke M. and Czapla, Sylvia and Jahnke, Anuschka and Willmitzer, Lothar and Heyer, Arnd G.}, doi = {10.1073/pnas.150043797}, journal = {Proceedings of the National Academy of Sciences}, pages = {8699-8704}, series = 15, title = {Transgenic potato (Solanum tuberosum) tubers synthesize the full spectrum of inulin molecules naturally occurring in globe artichoke (Cynara scolymus) roots}, url = {http://www.pnas.org/content/pnas/97/15/8699.full.pdf}, volume = 97, year = 2000 }
Link
http://www.pnas.org/content/pnas/97/15/8699.full.pdf

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