Plant distribution and the temperature coefficient of metabolism

The spatial distribution of a plant species is limited by the range of climatic conditions to which the species can adapt. Temperature is one of the most significant determinants of plant distribution, but except for the effects of lethal limits, little is known about physiological changes in responses to differences in environmental temperature. In this study, temperature coefficients of non-photosynthetic metabolism have been determined in the normal environmental temperature range for selected annual and perennial plants. Distinct differences were found in the temperature coefficient of metabolism of woody perennial plants from high latitudes and high elevations and closely related low-latitude and low-elevation plants. Low-latitude and low-elevation woody perennials have Arrhenius temperature coefficients for metabolism that are larger than those for congeneric high-latitude and high-elevation plants. The Arrhenius temperature coefficient is not rapidly adapted to new environments. A simple function was developed relating Arrhenius temperature coefficient to latitude and elevation for accessions of three, woody, perennial species complexes of plants collected from a wide geographic range but grown in common gardens. Within these taxa, plants that experience broader ranges of temperature during growth in their native habitat have smaller temperature coefficients. Temperature coefficients also varied with growth stage or season. No similar relationship was found for annuals and herbaceous perennials. For the plants tested, Arrhenius temperature coefficients are high during early spring growth, but shift to lower values later in the season. The shift in Arrhenius temperature coefficients occurs early in the season for southern and low-elevation plants and progressively later for plants from further north or higher elevation. The changes in Arrhenius temperature coefficients result largely from increases in plant metabolic rates at lower temperatures while little change occurs in the rates at higher temperatures. Altering the temperature dependence of the control of metabolic rate is apparently an important means of response to climate change.     

Respiration in postharvest sugarbeet roots is not limited by respiratory capacity or adenylates

Control of respiration has largely been studied with growing and/or photosynthetic tissues or organs, but has rarely been examined in harvested and stored plant products. As nongrowing, heterotrophic organs that are reliant on respiration to provide all of their metabolic needs, harvested plant products differ dramatically in their metabolism and respiratory needs from growing and photosynthetically active plant organs, and it cannot be assumed that the same mechanism controls respiration in both actively growing and harvested plant organs. To elucidate mechanisms of respiratory control for a harvested and stored plant product, sugarbeet (Beta vulgaris L.) root respiration was characterized with respect to respiratory capacity, adenylate levels and cellular energy status in roots whose respiration was altered by wounding or cold treatment (1 degrees C) and in response to potential effectors of respiration. Respiration rate was induced by wounding in roots stored at 10 degrees C and by cold temperature in roots stored at 1 degrees C for 11-13d. Alterations in respiration rate due to wounding or storage temperature were unrelated to changes in total respiratory capacity, the capacities of the cytochrome c oxidase (COX) or alternative oxidase (AOX) pathways, adenylate concentrations or cellular energy status, measured by the ATP:ADP ratio. In root tissue, respiration was induced by exogenous NADH indicating that respiratory capacity was capable of oxidizing additional electrons fed into the electron transport chain via an external NADH dehydrogenase. Respiration was not induced by addition of ADP or a respiratory uncoupler. These results suggest that respiration rate in stored sugarbeet roots is not limited by respiratory capacity, ADP availability or cellular energy status. Since respiration in plants can be regulated by substrate availability, respiratory capacity or energy status, it is likely that a substrate, other than ADP, limits respiration in stored sugarbeet roots.     

Three parameters comprehensively describe the temperature response of respiratory oxygen reduction

Using an exponential model that relies on Arrhenius kinetics, we explored Type I, Type II and dynamic (e.g. declining Q ₁₀ with increasing temperature) responses of respiration to temperature. Our Arrhenius model provides three parameters: R _REF (the base of the exponential model, nmol g⁻¹ s⁻¹), E ₀ (the overall activation energy of oxygen reduction that dominates its temperature sensitivity, kJ mol⁻¹) and δ (that describes dynamic responses of E ₀ to measurement temperature, 10³ K²). Two parameters, E ₀ and δ , are tightly linked. Increases in overall activation energy at a reference temperature were inversely related to changes in δ . At an E ₀ of ca. 45 kJ mol⁻¹, δ approached zero, and respiratory temperature response was strictly Arrhenius-like. Physiologically, these observations suggest that as contributions of AOX to combined oxygen reduction increase, E ₀( REF ) decreases because of different temperature sensitivities for V _max, and δ increases because of different temperature sensitivities for K _1/2 of AOX and COX. The balance between COX and AOX activity helps regulate plant metabolism by adjusting the demand for ATP to that for reducing power and carbon skeleton intermediates. Our approach enables determination of respiratory capacity in vivo and opens a path to development of process-based models of plant respiration.     

The Dual Arrhenius and Michaelis–Menten kinetics model for decomposition of soil organic matter at hourly to seasonal time scales

Decomposition of soil carbon stocks is one of the largest potential biotic feedbacks to climate change. Models of decomposition of soil organic matter and of soil respiration rely on empirical functions that relate variation in temperature and soil water content to rates of microbial metabolism using soil‐C substrates. Here, we describe a unifying modeling framework to combine the effects of temperature, soil water content, and soluble substrate supply on decomposition of soluble soil‐C substrates using simple functions based on process concepts. The model's backbone is the Michaelis–Menten equation, which describes the relationship between reaction velocity and soluble organic‐C and O₂ substrate concentrations at an enzyme's reactive site, which are determined by diffusivity functions based on soil water content. Temperature sensitivity is simulated by allowing the maximum velocity of the reaction (V_max) to vary according to Arrhenius function. The Dual Arrhenius and Michaelis–Menten kinetics (DAMM) model core was able to predict effectively observations from of laboratory enzyme assays of β‐glucosidase and phenol‐oxidase across a range of substrate concentrations and incubation temperatures. The model also functioned as well or better than purely empirical models for simulating hourly and seasonal soil respiration data from a trenched plot in a deciduous forest at the Harvard Forest, in northeastern United States. The DAMM model demonstrates that enzymatic processes can be intrinsically temperature sensitive, but environmental constrains of substrate supply under soil moisture extremes can prevent that response to temperature from being observed. We discuss how DAMM could serve as a core module that is informed by other modules regarding microbial dynamics and supply of soluble‐C substrates from plant inputs and from desorption of physically stabilized soil‐C pools. Most importantly, it presents a way forward from purely empirical representation of temperature and moisture responses and integrates temperature‐sensitive enzymatic processes with constraints of substrate supply.     

Plant peroxisomes: biogenesis and function

Peroxisomes are eukaryotic organelles that are highly dynamic both in morphology and metabolism. Plant peroxisomes are involved in numerous processes, including primary and secondary metabolism, development, and responses to abiotic and biotic stresses. Considerable progress has been made in the identification of factors involved in peroxisomal biogenesis, revealing mechanisms that are both shared with and diverged from non-plant systems. Furthermore, recent advances have begun to reveal an unexpectedly large plant peroxisomal proteome and have increased our understanding of metabolic pathways in peroxisomes. Coordination of the biosynthesis, import, biochemical activity, and degradation of peroxisomal proteins allows for highly dynamic responses of peroxisomal metabolism to meet the needs of a plant. Knowledge gained from plant peroxisomal research will be instrumental to fully understanding the organelle's dynamic behavior and defining peroxisomal metabolic networks, thus allowing the development of molecular strategies for rational engineering of plant metabolism, biomass production, stress tolerance, and pathogen defense.     

Global patterns in lake ecosystem responses to warming based on the temperature dependence of metabolism

Climate warming is expected to have large effects on ecosystems in part due to the temperature dependence of metabolism. The responses of metabolic rates to climate warming may be greatest in the tropics and at low elevations because mean temperatures are warmer there and metabolic rates respond exponentially to temperature (with exponents >1). However, if warming rates are sufficiently fast in higher latitude/elevation lakes, metabolic rate responses to warming may still be greater there even though metabolic rates respond exponentially to temperature. Thus, a wide range of global patterns in the magnitude of metabolic rate responses to warming could emerge depending on global patterns of temperature and warming rates. Here we use the Boltzmann–Arrhenius equation, published estimates of activation energy, and time series of temperature from 271 lakes to estimate long‐term (1970–2010) changes in 64 metabolic processes in lakes. The estimated responses of metabolic processes to warming were usually greatest in tropical/low‐elevation lakes even though surface temperatures in higher latitude/elevation lakes are warming faster. However, when the thermal sensitivity of a metabolic process is especially weak, higher latitude/elevation lakes had larger responses to warming in parallel with warming rates. Our results show that the sensitivity of a given response to temperature (as described by its activation energy) provides a simple heuristic for predicting whether tropical/low‐elevation lakes will have larger or smaller metabolic responses to warming than higher latitude/elevation lakes. Overall, we conclude that the direct metabolic consequences of lake warming are likely to be felt most strongly at low latitudes and low elevations where metabolism‐linked ecosystem services may be most affected.     

Effects of Temperature on Electron Transport in Arum maculatum Mitochondria

The effects of temperature upon the respiratory pathways of Arum maculatum mitochondria have been studied. The alternate oxidase sustained a greater proportion of the total respiration at low temperatures than at higher temperatures. Arrhenius plots of respiratory activities show two discontinuities, one at 14°C and one at 21°C. The lower temperature discontinuity was associated with electron transport from succinate dehydrogenase to the alternative oxidase, enzymes that face the inner side of the membrane while the higher temperature discontinuity was associated with electron transport from the external NADH dehydrogenase to cytochrome c oxidase, which face the outer side of the membrane. Both discontinuities resulted in a decrease in the activation energy for electron transport on one side of the membrane. Arrhenius plots of transmembrane electron transport showed discontinuities at both 14° and 21°C but the upper discontinuity resulted in an increase in the activation energy. Activation energies determined for the respiratory activities show that above 21°C the exogenous NADH-cytochrome pathway and the succinate-alternative oxidase pathway were lower than those for the NADH-alternative pathway or the succinate cytochrome pathway.     

On the role of plant mitochondrial metabolism and its impact on photosynthesis in both optimal and sub-optimal growth conditions

Given that the pathways of photosynthesis and respiration catalyze partially opposing processes, it follows that their relative activities must be carefully regulated within plant cells. Recent evidence has shown that the components of the mitochondrial electron transport chain are essential for the proper maintenance of intracellular redox gradients, to allow considerable rates of photorespiration and in turn efficient photosynthesis. Thus considerable advances have been made in understanding the interaction between respiration and photosynthesis during the last decades and the potential mechanisms linking mitochondrial function and photosynthetic efficiency will be reviewed. Despite the fact that manipulation of various steps of mitochondrial metabolism has been demonstrated to alter photosynthesis under optimal growth conditions, it is likely that these changes will, by and large, not be maintained under sub-optimal situations. Therefore producing plants to meet this aim remains a critical challenge. It is clear, however, that although there have been a range of studies analysing changes in respiratory and photosynthetic rates in response to light, temperature and CO₂, our knowledge of the environmental impact on these processes and its linkage still remains fragmented. We will also discuss the metabolic changes associated to plant respiration and photosynthesis as important components of the survival strategy as they considerably extend the period that a plant can withstand to a stress situation.     

Reducing maintenance metabolism by metabolic engineering of respiration improves riboflavin production by Bacillus subtilis

We present redirection of electron flow to more efficient proton pumping branches within respiratory chains as a generally applicable metabolic engineering strategy, which tailors microbial metabolism to the specific requirements of high cell density processes by improving product and biomass yields. For the example of riboflavin production by Bacillus subtilis, we reduced the rate of maintenance metabolism by about 40% in a cytochrome bd oxidase knockout mutant. Since the putative Yth and the caa(3) oxidases were of minor importance, the most likely explanation for this improvement is translocation of two protons per transported electron via the remaining cytochrome aa(3) oxidase, instead of only one proton via the bd oxidase. The reduction of maintenance metabolism, in turn, significantly improved the yield of recombinant riboflavin and B. subtilis biomass in fed-batch cultures.     

Towards kinetic modeling of genome-scale metabolic networks without sacrificing stoichiometric,thermodynamic and physiological constraints

Mathematical modeling is an essential tool for the comprehensive understanding of cell metabolism and its interactions with the environmental and process conditions. Recent developments in the construction and analysis of stoichiometric models made it possible to define limits on steady-state metabolic behavior using flux balance analysis. However, detailed information on enzyme kinetics and enzyme regulation is needed to formulate kinetic models that can accurately capture the dynamic metabolic responses. The use of mechanistic enzyme kinetics is a difficult task due to uncertainty in the kinetic properties of enzymes. Therefore, the majority of recent works considered only mass action kinetics for reactions in metabolic networks. Herein, we applied the optimization and risk analysis of complex living entities (ORACLE) framework and constructed a large-scale mechanistic kinetic model of optimally grown Escherichia coli. We investigated the complex interplay between stoichiometry, thermodynamics, and kinetics in determining the flexibility and capabilities of metabolism. Our results indicate that enzyme saturation is a necessary consideration in modeling metabolic networks and it extends the feasible ranges of metabolic fluxes and metabolite concentrations. Our results further suggest that enzymes in metabolic networks have evolved to function at different saturation states to ensure greater flexibility and robustness of cellular metabolism.     

Connecting salt stress signalling pathways with salinity‐induced changes in mitochondrial metabolic processes in C3 plants

Salinity exerts a severe detrimental effect on crop yields globally. Growth of plants in saline soils results in physiological stress, which disrupts the essential biochemical processes of respiration, photosynthesis, and transpiration. Understanding the molecular responses of plants exposed to salinity stress can inform future strategies to reduce agricultural losses due to salinity; however, it is imperative that signalling and functional response processes are connected to tailor these strategies. Previous research has revealed the important role that plant mitochondria play in the salinity response of plants. Review of this literature shows that 2 biochemical processes required for respiratory function are affected under salinity stress: the tricarboxylic acid cycle and the transport of metabolites across the inner mitochondrial membrane. However, the mechanisms by which components of these processes are affected or react to salinity stress are still far from understood. Here, we examine recent findings on the signal transduction pathways that lead to adaptive responses of plants to salinity and discuss how they can be involved in and be affected by modulation of the machinery of energy metabolism with attention to the role of the tricarboxylic acid cycle enzymes and mitochondrial membrane transporters in this process.     

Short-Term Metabolome Dynamics and Carbon, Electron, and ATP Balances in Chemostat-Grown Saccharomyces cerevisiae CEN.PK 113-7D following a Glucose Pulse

The in vivo kinetics in Saccharomyces cerevisiae CEN.PK 113-7D was evaluated during a 300-second transient period after applying a glucose pulse to an aerobic, carbon-limited chemostat culture. We quantified the responses of extracellular metabolites, intracellular intermediates in primary metabolism, intracellular free amino acids, and in vivo rates of O₂ uptake and CO₂ evolution. With these measurements, dynamic carbon, electron, and ATP balances were set up to identify major carbon, electron, and energy sinks during the postpulse period. There were three distinct metabolic phases during this time. In phase I (0 to 50 seconds after the pulse), the carbon/electron balances closed up to 85%. The accumulation of glycolytic and storage compounds accounted for 60% of the consumed glucose, caused an energy depletion, and may have led to a temporary decrease in the anabolic flux. In phase II (50 to 150 seconds), the fermentative metabolism gradually became the most important carbon/electron sink. In phase III (150 to 300 seconds), 29% of the carbon uptake was not identified in the measurements, and the ATP balance had a large surplus. These results indicate an increase in the anabolic flux, which is consistent with macroscopic balances of extracellular fluxes and the observed increase in CO₂ evolution associated with nonfermentative metabolism. The identified metabolic processes involving major carbon, electron, and energy sinks must be taken into account in in vivo kinetic models based on short-term dynamic metabolome responses.     

Short-term metabolome dynamics and carbon, electron, and ATP balances in chemostat-grown Saccharomyces cerevisiae CEN.PK 113-7D following a glucose pulse

The in vivo kinetics in Saccharomyces cerevisiae CEN.PK 113-7D was evaluated during a 300-second transient period after applying a glucose pulse to an aerobic, carbon-limited chemostat culture. We quantified the responses of extracellular metabolites, intracellular intermediates in primary metabolism, intracellular free amino acids, and in vivo rates of O(2) uptake and CO(2) evolution. With these measurements, dynamic carbon, electron, and ATP balances were set up to identify major carbon, electron, and energy sinks during the postpulse period. There were three distinct metabolic phases during this time. In phase I (0 to 50 seconds after the pulse), the carbon/electron balances closed up to 85%. The accumulation of glycolytic and storage compounds accounted for 60% of the consumed glucose, caused an energy depletion, and may have led to a temporary decrease in the anabolic flux. In phase II (50 to 150 seconds), the fermentative metabolism gradually became the most important carbon/electron sink. In phase III (150 to 300 seconds), 29% of the carbon uptake was not identified in the measurements, and the ATP balance had a large surplus. These results indicate an increase in the anabolic flux, which is consistent with macroscopic balances of extracellular fluxes and the observed increase in CO(2) evolution associated with nonfermentative metabolism. The identified metabolic processes involving major carbon, electron, and energy sinks must be taken into account in in vivo kinetic models based on short-term dynamic metabolome responses.     

Temperature‐dependent body size effects determine population responses to climate warming

Current understanding of animal population responses to rising temperatures is based on the assumption that biological rates such as metabolism, which governs fundamental ecological processes, scale independently with body size and temperature, despite empirical evidence for interactive effects. Here, we investigate the consequences of interactive temperature‐ and size scaling of vital rates for the dynamics of populations experiencing warming using a stage‐structured consumer‐resource model. We show that interactive scaling alters population and stage‐specific responses to rising temperatures, such that warming can induce shifts in population regulation and stage‐structure, influence community structure and govern population responses to mortality. Analysing experimental data for 20 fish species, we found size–temperature interactions in intraspecific scaling of metabolic rate to be common. Given the evidence for size–temperature interactions and the ubiquity of size structure in animal populations, we argue that accounting for size‐specific temperature effects is pivotal for understanding how warming affects animal populations and communities.