Kinetic Mechanisms of Biological Regulation in Photosynthetic Organisms

Principles of regulation on different levels of photosynthetic apparatus are discussed. Mathematical models of isolated photosynthetic reaction centers and general system of energy transduction in chloroplast are developed. A general approach to model these complex metabolic systems is suggested. Regulatory mechanisms in plant cell are correlated with the different patterns of fluorescence induction curve at different internal physiological states of the cells and external (environmental) conditions. Light regulation inside photosynthetic reaction centers, diffusion processes in thylakoid membrane, generation of transmembrane electrochemical potential, coupling with processes of CO₂ fixation in Calvin Cycle are considered as stages of control of energy transformation in chloroplasts in their connection with kinetic patterns of fluorescence induction curves and other spectrophotometric data.     

PHOTOSYNTHESIS-IRRADIANCE PATTERNS IN BENTHIC MICROALGAE: VARIATIONS AS A FUNCTION OF ASSEMBLAGE THICKNESS AND COMMUNITY STRUCTURE

Photosynthesis-irradiance (P-I) characteristics of periphyton (microphytobenthos) have been considered primarily for entire assemblages. How P-I responses vary with mat thickness and with community composition has not been considered in detail. We used a combined approach of modeling, microscale determinations of photosynthetic rate and light attenuation, and whole-assemblage O₂ flux measurements to explore P-I relationships. The modeling approach suggested that the onset of photosynthetic saturation and photoinhibition will occur at higher irradiance and that whole-mat photoinhibition (decreased photosynthesis at very high irradiance), biomass-specific maximum photosynthetic rate, and initial slope of the P-I function (α) should decrease as assemblage thickness increases or light attenuation increases. Spherical light microsensor profiles for a variety of stream algae indicated a strongly compressed photic zone with attenuation coefficients of 70–1791 m^?1 for scalar photosynthetic photon fluence density. The O₂ microelectrode measurements showed little if any photoinhibition at 2 and 4 mm depths in one filamentous green algal (Ulothrix) assemblage, with a relatively low attenuation coefficient, and no photoinhibition in a second Ulothrix community. An assemblage dominated by a unicellular cyanobacterium exhibited little photoinhibition at 2 and 4 mm, and a dense cyanobacterial (Phormidium)/xanthophyte (Vaucheria) community exhibited no photoinhibition at all. The microelectrode data revealed increases in α over several millimeters of depth (photoacclimation). These data supported the model predictions with regard to the effects of mat optical thickness on whole-assemblage values for α and photoinhibition. Whole-community O₂ flux data from 15 intact assemblages revealed positive relationships between chlorophyll a density and maximum photosynthetic rate or α expressed per unit area; the relationships with chlorophyll a were negative when photosynthetic rates were expressed per unit chlorophyll a. None of the whole assemblages exhibited photoinhibition. Thus, the data from the whole communities were consistent with model predictions.     

On the nature of the light-induced component of dark respiration of plants

The data on the isotope composition of carbon of CO₂ of the light-induced dark respiration component have been analyzed using the oscillation model of photosynthesis. It was concluded that this component originates during the transformation of sucrose accumulated by the plant in the oxygenase phase of photosynthetic oscillations in the light period into organic acids. The transformation occurs in the dark period. It this process, C-3 and C-4 atoms, which determine the “heavy“ isotope composition of carbon of CO₂ of the light-induced dark respiration component, are split off from the hexose link of sucrose.     

SPECIALIZATION OF MESOPHYLL MORPHOLOGY IN RELATION TO C4 PHOTOSYNTHESIS IN THE POACEAE

Our current understanding of the photosynthetic process in species utilizing the C₄ photosynthetic pathway suggests that photosynthetic efficiency should be enhanced by: 1) maximizing the conductance of the gas phase transport pathway from the leaf exterior to the mesophyll cell surfaces; 2) maximizing cytoplasmic connections and metabolite transport between bundle sheath and mesophyll parenchyma cells; and 3) minimizing the conductance of the gas phase transport pathway from the bundle sheath cells to the leaf exterior. In this study we have examined several species in the Poaceae with C₄ photosynthesis to determine if there is any evidence for anatomical specialization which would lead to enhanced photosynthetic efficiency by these processes. Observations with light and scanning electron microscopes revealed specializations in mesophyll cell morphology and arrangement which include branched cells forming intercellular channels. These specializations are hypothesized to contribute to photosynthetic efficiency through its influence on the above transport processes.     

Interactive effects of light,leaf temperature,CO2 and O2 on photosynthesis in soybean

A biochemical model of C ₃photosynthesis has been developed by G.D. Farquhar et al. (1980, Planta 149, 78–90) based on Michaelis-Menten kinetics of ribulose-1,5-bisphosphate (RuBP) carboxylase-oxygenase, with a potential RuBP limitation imposed via the Calvin cycle and rates of electron transport. The model presented here is slightly modified so that parameters may be estimated from whole-leaf gas-exchange measurements. Carbon-dioxide response curves of net photosynthesis obtained using soybean plants (Glycine max (L.) Merr.) at four partial pressures of oxygen and five leaf temperatures are presented, and a method for estimating the kinetic parameters of RuBP carboxylase-oxygenase, as manifested in vivo, is discussed. The kinetic parameters so obtained compare well with kinetic parameters obtained in vitro, and the model fits to the measured data give r ²values ranging from 0.87 to 0.98. In addition, equations developed by J.D. Tenhunen et al. (1976, Oecologia 26, 89–100, 101–109) to describe the light and temperature responses of measured CO₂-saturated photosynthetic rates are applied to data collected on soybean. Combining these equations with those describing the kinetics of RuBP carboxylase-oxygenase allows one to model successfully the interactive effects of incident irradiance, leaf temperature, CO₂ and O₂ on whole-leaf photosynthesis. This analytical model may become a useful tool for plant ecologists interested in comparing photosynthetic responses of different C₃ plants or of a single species grown in contrasting environments.Abbreviations PCO photorespiratory carbon oxidation - PCR photosynthetic carbon reduction - PPFD photosynthetic photon-flux density - RuBP ribulose bisphosphate     

Chromatophore heterogeneity explains phenomena seen in Rhodobacter sphaeroides previously attributed to supercomplexes

It is generally considered that metabolic reactions are well described by homogeneous kinetic models in which the reaction phase is statistically uniform. In membranes, especially in photosynthetic systems where the protein complement is high, it has recently been recognized that effects of local heterogeneity might contribute additional factors that perturb the kinetic behavior, and require more extensive treatment. We show in this paper that statistical heterogeneity in vesicular systems can also contribute to quite marked discrepancies from the behavior expected from standard kinetic and thermodynamic models, for reactions involving free diffusion in the aqueous phase. We explain the kinetic and thermodynamic effects observed in studies of photosynthetic electron transfer in cells and chromatophores from Rhodobacter sphaeroides previously attributed to supercomplexes, in terms of a model based on heterogeneity in distribution of electron transfer components among the chromatophore population. We discuss examples of data inconsistent with the supercomplex model, but well explained by the heterogeneity model.     

Evaluation of chlorophyll fluorescence as a probe for drought stress in willow leaves

The effect of drought on the photosynthetic apparatus of leaves of Salix sp. was studied by measurements of the induction of chlorophyll fluorescence and the capacity for O₂ evolution. Using a multivariate analysis, a model was developed that could predict the degree of drought stress from the data of fluorescence kinetics. Even mild drought stress was detected with high precision; this was not always possible when the photosynthetic capacity was measured. The most clear discrimination between control and drought-stressed leaves was obtained if fluorescence induction was measured at high rather than normal CO₂ levels, and at low rather than high light levels. All information provided by fluorescence pertaining to drought was contained within the slow phase of the induction curve. It is suggested that rapid dehydration is different from drought at the mechanistic level as judged by the fluorescence characteristics.     

The photosynthetic performance of sterile and fertile sporophytes in a natural population of the fern Dryopteris affinis

We studied the photosynthetic performance of sterile and fertile sporophytes in a natural population of the fern Dryopteris affinis growing within a riparian forest (Central Italy) using chlorophyll (Chl) a fluorescence transients, the OJIP phase, where O is for the minimum fluorescence, P is for the peak (the maximum), and J and I are inflections. The “vitality” of the samples was assessed by the maximum quantum yield of primary photochemistry obtained indirectly from the fluorescence data (F_v/F_m); in the same way, the so-called performance index (PI_ABS) was obtained from fluorescence data. The photosynthetic performance (inferred from PI_ABS) of D. affinis changed significantly with the seasonal development of the fronds. The highest photosynthetic performance was recorded in the summer, corresponding to the period of spore release. The photosynthetic performance decreased in the winter, down to the minimal values of senescent fronds reached at the end of the seasonal cycle (May-June). On the whole, during the seasonal development, sterile and fertile fronds had a similar photosynthetic behaviour, as inferred from fluorescence data. At the end of spore maturation and dispersal (September-October), the fertile fronds showed somewhat lower photosynthetic performance than the sterile fronds, as revealed by PI_ABS. Being a long-lived fern, confined to humid and undisturbed sites in the Mediterranean, D. affinis deserves to be further investigated as a potential indicator of ecological continuity in Mediterranean riparian forests.     

Improving models of photosynthetic thermal acclimation: Which parameters are most important and how many should be modified?

Photosynthetic temperature acclimation could strongly affect coupled vegetation–atmosphere feedbacks in the global carbon cycle, especially as the climate warms. Thermal acclimation of photosynthesis can be modelled as changes in the parameters describing the direct effect of temperature on photosynthetic capacity (i.e., activation energy, E_a; deactivation energy, H_d; entropy parameter, ΔS) or the basal value of photosynthetic capacity (i.e., photosynthetic capacity measured at 25°C). However, the impact of acclimating these parameters (individually or in combination) on vegetative carbon gain is relatively unexplored. Here we compare the ability of 66 photosynthetic temperature acclimation scenarios to improve the ability of a spatially explicit canopy carbon flux model, MAESTRA, to predict eddy covariance data from a loblolly pine forest. We show that: (1) incorporating seasonal temperature acclimation of basal photosynthetic capacity improves the model's ability to capture seasonal changes in carbon fluxes and outperforms acclimation of other single factors (i.e., E_a or ΔS alone); (2) multifactor scenarios of photosynthetic temperature acclimation provide minimal (if any) improvement in model performance over single factor acclimation scenarios; (3) acclimation of E_a should be restricted to the temperature ranges of the data from which the equations are derived; and (4) model performance is strongly affected by the H_d parameter. We suggest that a renewed effort be made into understanding whether basal photosynthetic capacity, E_a, H_d and ΔS co‐acclimate across broad temperature ranges to determine whether and how multifactor thermal acclimation of photosynthesis occurs.     

A three-dimensional model of CO2 transport in airspaces and mesophyll cells of a silver birch leaf

A realistic numerical three‐dimensional (3D) model was constructed to study CO₂ transport inside a birch leaf. The model included chloroplasts, palisade and spongy mesophyll cells, airspaces, stomatal opening and the leaf boundary layer. Diffusion equations for CO₂ were solved for liquid(mesophyll) and gaseous(air) phases. Simulations were made in typical ambient field conditions varying stomatal opening, photosynthetic capacity and temperature. Doubled ambient CO₂ concentration was also considered. Changes in variables caused non‐linear effects in the total flux, especially when compared with the results of double CO₂ concentration. The reduction in stomatal opening size had a smaller effect on the total flux in doubled concentrations than ambient CO₂. The reduced photosynthetic capacity had a similar effect on the flux in both cases. The palisade and spongy mesophyll cells had unequal roles mainly due to the light absorption profile. Results from the 3D simulation were also compared to the classical one‐dimensional resistance approach. Liquid and gas phase resistances were estimated and found strongly variable according to changes in temperature and degree of stomatal opening. For the birch leaves modelled, intercellular airspace resistance was small (2% of the total resistance in saturating irradiance conditions at 25 °C at stomatal opening diameter of 4 µm) whereas the liquid phase resistance was significant (23% for mesophyll and chloroplasts in the same ‘base case’). The absorption of CO₂ into water at cell surfaces caused additional (strongly temperature dependent) resistance which accounted for 36% of the total resistance in the base case.     

Mechanisms underlying leaf photosynthetic acclimation to warming and elevated CO2 as inferred from least‐cost optimality theory

The mechanisms responsible for photosynthetic acclimation are not well understood, effectively limiting predictability under future conditions. Least‐cost optimality theory can be used to predict the acclimation of photosynthetic capacity based on the assumption that plants maximize carbon uptake while minimizing the associated costs. Here, we use this theory as a null model in combination with multiple datasets of C₃ plant photosynthetic traits to elucidate the mechanisms underlying photosynthetic acclimation to elevated temperature and carbon dioxide (CO₂). The model‐data comparison showed that leaves decrease the ratio of the maximum rate of electron transport to the maximum rate of Rubisco carboxylation (J_max/V_cmax) under higher temperatures. The comparison also indicated that resources used for Rubisco and electron transport are reduced under both elevated temperature and CO₂. Finally, our analysis suggested that plants underinvest in electron transport relative to carboxylation under elevated CO₂, limiting potential leaf‐level photosynthesis under future CO₂ concentrations. Altogether, our results show that acclimation to temperature and CO₂ is primarily related to resource conservation at the leaf level. Under future, warmer, high CO₂ conditions, plants are therefore likely to use less nutrients for leaf‐level photosynthesis, which may impact whole‐plant to ecosystem functioning.     

“Live” neuron and optimal learning rule

A concept of the live unit as an automatic regulation system with a few admissible states areas in the space of states is considered. Energetic profit of oscillatory behavior consisting in the consecutive transitions of system from one admissible states area to another is shown. It is stated, that external disturbances cause the energy consumption of oscillatory system to decrease. On the basis of this concept and some neurophysiological data, the live energy-consuming nonlinear three-state neuron model is proposed and the existence of energy optimal generation frequency v _opt is proved. For the realization of tendency to v _opt the optimal learning rule is proposed, which provides unsupervised learning and interlinked short-term and long-term memories with forgetting. The model proposed explains the genesis of neural network, is promising in the sense of network self-organization and allows to solve the problem of internal activity in the researches on artificial intelligence.     

Phase Dependent Sign Changes of GABAergic Synaptic Input Explored <Emphasis Type="Italic">In-Silicio</Emphasis> and <Emphasis Type="Italic">In-Vitro</Emphasis>

Inhibitory interactions play a crucial role in the synchronization of neuronal activity. Here we investigate the effect of GABAergic PSPs on spike timing in cortical neurons that exhibit an oscillatory modulation of their membrane potential. To this end we combined numerical simulations with in-vitro patch-clamp recordings from layer II/III pyramidal cells of the rat visual cortex. Special emphasis was placed on exploring how the reversal potential of the GABAergic synaptic currents (E_GABA) and the phase relations of the PSPs relative to the oscillation cycles affect the timing of spikes riding on the depolarizing peaks of the oscillations. The simulations predicted: (1) With E_GABA more negative than the oscillation minima PSPs are hyperpolarizing at all phases and thus delay or prevent spikes. (2) With E_GABA being more positive than the oscillation maxima PSPs are depolarizing in a phase-independent way and lead to a phase advance of spikes. (3) In the intermediate case where E_GABA lies within oscillation maxima and minima PSPs are either hyper- or depolarizing depending on their phase relations to the V_m oscillations and can therefore either delay or advance spikes. Experiments conducted in this most interesting last configuration with biphasic PSPs agreed with the model predictions. Additional theoretical investigations revealed the effect of these PSP induced shifts in spike timing on synchronization in neuronal circuits. The results suggest that GABAergic mechanisms can assume highly specific timing functions in oscillatory networks.Action Editor: Alain Destexhe     

Effect of Bursaphelenchus xylophilus infection on leaf photosynthetic characteristics and resource‐use efficiency of Pinus massoniana

Pine wilt disease (PWD ) is considered as the most destructive forest‐invasive alien species in China. We measured gas exchange parameters and foliar carbon isotope ratios (δ¹³C) of different infection phases of Masson pine in order to investigate the effect of Bursaphelenchus xylophilus infection on photosynthetic responses and resource‐use efficiency. The results showed that net photosynthetic rate (P _n), transpiration rate (T ), stomatal conductance (g _s), and internal CO ₂ concentrations (C _i) decreased in the infested trees at photosynthetic photon flux density (PPFD ) levels from 0 to 2,000 μmol m^?2 s^?1 compared with controls. The maximum net photosynthetic rate (P _max) was significantly declined in the infected trees than in controls (p  <  .05). There also exist significant differences in dark respiration rate (R _d) among different infection phases (p  <  .05), but the value is highest in the middle infection phase, followed by the control and then the terminal infection phase. This indicates that Pinus massoniana plants need to consume more photosynthetic products during the middle infection phase in order to defend against pine sawyer beetle feeding and PWD infection. Isotopic analysis revealed a significant decrease of the foliar δ¹³C (p  <  .05), as much as 2.5‰ lower in the infected trees. The mean leaf N content was about 12.94% less in the middle infection phase and 27.06% less in the terminal infection phase, causing a significant increase of the foliar C:N ratio in infested trees. Both of the net photosynthetic rates and foliar δ¹³C were linearly correlated with the foliar N content. We also found a significant decrease (p  <  .05) of resource‐use efficiency in PWD ‐induced P. massoniana plants, which can be attributed to the closure of stomatal pores and the inactivation or loss of both Rubisco and other key Calvin cycle enzymes. This study highlights the impact of photosynthetic characteristics, foliar carbon isotope ratios, and resource‐use efficiency of PWD ‐induced trees, which can help identify PWD infestations at the photosynthetic and physiological levels so as to better facilitate management actions.     

The role of linear and voltage-dependent ionic currents in the generation of slow wave oscillations

Neuronal oscillatory activity is generated by a combination of ionic currents, including at least one inward regenerative current that brings the cell towards depolarized voltages and one outward current that repolarizes the cell. Such currents have traditionally been assumed to require voltage-dependence. Here we test the hypothesis that the voltage dependence of the regenerative inward current is not necessary for generating oscillations. Instead, a current I _NL that is linear in the biological voltage range and has negative conductance is sufficient to produce regenerative activity. The current I _NL can be considered a linear approximation to the negative-conductance region of the current–voltage relationship of a regenerative inward current. Using a simple conductance-based model, we show that I _NL , in conjunction with a voltage-gated, non-inactivating outward current, can generate oscillatory activity. We use phase-plane and bifurcation analyses to uncover a rich variety of behaviors as the conductance of I _NL is varied, and show that oscillations emerge as a result of destabilization of the resting state of the model neuron. The model shows the need for well-defined relationships between the inward and outward current conductances, as well as their reversal potentials, in order to produce stable oscillatory activity. Our analysis predicts that a hyperpolarization-activated inward current can play a role in stabilizing oscillatory activity by preventing swings to very negative voltages, which is consistent with what is recorded in biological neurons in general. We confirm this prediction of the model experimentally in neurons from the crab stomatogastric ganglion.     

Low CO2 does not remove diffusional limitation to photosynthesis in salt stressed tomato during osmotic phase

Salinity is one of the main environmental stress for crops such as tomato which is widely spread in the Mediterranean region. It is now widely considered that in plant adaptation to salts, the time scale of the response is essential. During the initial phase of response to salinity, when the osmotic effect predominates, plant response to salts is regulated by hormones, and between them abscisic acid plays a crucial role. We showed that on tomato crops during the first phase (osmotic one) low CO₂ conditioning treatment before photosynthetic response to carbon dioxide concentration (A–Ci curve) is not applicable because diffusional limitations to photosynthesis is not removed by low CO₂ air concentration. Conditioning at low CO₂ is not sufficient to remove diffusional limitation of photosynthesis in salt stressed tomatoes during osmotic phase.     

The escape of Tritonia: dynamics of a neuromuscular control mechanism.

The results of photosynthesis experiments with ¹⁸O labelled water and carbon dioxide are commonly regarded as the strongest arguments for a light-induced water oxidation. In these experiments, however, several sources of error have not been adequately considered. The peculiarities of natural H₂OCO₂ mixtures and their enzymatically enhanced equilibration are discussed. The unequal distribution of the oxygen isotopes is considered. Relevant data are presented on the CO₂ storage in green plant cells and the oxygen burst which is often observed during the beginning of the light period. After the statement of the necessary precautions for isotope experiments data of former measurements of the oxygen isotope discrimination by photosynthetic and respiratory processes are discussed. The data laid down in the literature together with the results of some experiments with deuterated water are taken as disproof of the hypothesis of water oxidation.     

Regulation of photosynthesis during Arabidopsis leaf development in continuous light

Previous investigations in our laboratory have shown that leaf developmental programming in tobacco is regulated by source strength. One hypothesis to explain how source strength is perceived is that hexokinase acts as a sensor of carbohydrate flux to regulate the expression of photosynthetic genes, possibly as a result of sucrose cycling through acid invertase and hexokinase. We have turned to Arabidopsis as a model system to study leaf development and have examined various photosynthetic parameters during the ontogeny of a single leaf on the Arabidopsis rosette grown in continuous light. We found that photosynthetic rates, photosynthetic gene expression, pigment contents and total protein amounts attain peak levels early in the expansion phase of development, then decline progressively as development proceeds. In contrast, the flux of ¹⁴CO₂ into hexoses increases modestly until full expansion is attained, then falls in the fully expanded leaf. Partitioning of carbon into hexoses versus sucrose increases until full expansion is attained, then falls. The in vitro activities of hexokinase, vacuolar acid invertase, and cell wall acid invertase do not change until the late stages of senescence, when they increase markedly. At this time there are also dramatic increases in hexose pool sizes and in senescence-associated gene (SAG) expression. Taken together, our results suggest that invertase and hexokinase activities do not control the partitioning of label into hexoses during development. We conclude that our data are not readily compatible with a simple model of leaf development, whereby alterations in photosynthetic rates are mediated directly by hexose flux or by hexose pool sizes. Yet, these factors might contribute to the control of gene expression. This revised version was published online in June 2006 with corrections to the Cover Date.     

A Mathematical Analysis of Agonist- and KCl-Induced Ca Oscillations in Mouse Airway Smooth Muscle Cells

Airway hyperresponsiveness is a major characteristic of asthma and is generally ascribed to excessive airway narrowing associated with the contraction of airway smooth muscle cells (ASMCs). ASMC contraction is initiated by a rise in intracellular calcium concentration ([Ca²⁺]_i), observed as oscillatory Ca²⁺ waves that can be induced by either agonist or high extracellular K⁺ (KCl). In this work, we present a model of oscillatory Ca²⁺ waves based on experimental data that incorporate both the inositol trisphosphate receptor and the ryanodine receptor. We then combined this Ca²⁺ model and our modified actin-myosin cross-bridge model to investigate the role and contribution of oscillatory Ca²⁺ waves to contractile force generation in mouse ASMCs. The model predicts that: 1), the difference in behavior of agonist- and KCl-induced Ca²⁺ waves results principally from the fact that the sarcoplasmic reticulum is depleted during agonist-induced oscillations, but is overfilled during KCl-induced oscillations; 2), regardless of the order in which agonist and KCl are added into the cell, the resulting [Ca²⁺]_i oscillations will always be the short-period, agonist-induced-like oscillations; and 3), both the inositol trisphosphate receptor and the ryanodine receptor densities are higher toward one end of the cell. In addition, our results indicate that oscillatory Ca²⁺ waves generate less contraction than whole-cell Ca²⁺ oscillations induced by the same agonist concentration. This is due to the spatial inhomogeneity of the receptor distributions.     

Electron transfer through the acceptor side of photosystem I: Interaction with exogenous acceptors and molecular oxygen

This review considers the state-of-the-art on mechanisms and alternative pathways of electron transfer in photosynthetic electron transport chains of chloroplasts and cyanobacteria. The mechanisms of electron transport control between photosystems (PS) I and II and the Calvin–Benson cycle are considered. The redistribution of electron fluxes between the noncyclic, cyclic, and pseudocyclic pathways plays an important role in the regulation of photosynthesis. Mathematical modeling of light-induced electron transport processes is considered. Particular attention is given to the electron transfer reactions on the acceptor side of PS I and to interactions of PS I with exogenous acceptors, including molecular oxygen. A kinetic model of PS I and its interaction with exogenous electron acceptors has been developed. This model is based on experimental kinetics of charge recombination in isolated PS I. Kinetic and thermodynamic parameters of the electron transfer reactions in PS I are scrutinized. The free energies of electron transfer between quinone acceptors A_1A/A_1B in the symmetric redox cofactor branches of PS I and iron–sulfur clusters F_X, F_A, and F_B have been estimated. The second-order rate constants of electron transfer from PS I to external acceptors have been determined. The data suggest that byproduct formation of superoxide radical in PS I due to the reduction of molecular oxygen in the A1 site (Mehler reaction) can exceed 0.3% of the total electron flux in PS I.