Richard S. Criddle

Kinetics of plant growth and metabolism

Abstract Direct measurements of plant growth rates in terms of volume, length, net photosynthate, etc. provide little information concerning the mechanism of adaptation of metabolism to an environment. To derive the mechanism, metabolic properties must be measured as functions of environmental variables. Growth rates may be limited by the availability of nutrients including fixed carbon, by climate, by other environmental factors including toxins, or by the genetically determined properties of the plant. But in all cases, growth rate is equal to a function of respiration rate and efficiency. For a plant to thrive, its respiratory metabolism as well as its photosynthetic metabolism must be closely adapted to the seasonal and daily variations in the environment. Thus, measurement of respiratory properties is necessary for understanding plant adaptation. In terms of readily measurable respiratory variables, the rate law for growth driven by aerobic respiration is R SG =R CO 2 ϵ C 1−ϵ C =rR O 2 ϵ C 1−ϵ C =−R CO 2 Δ H CO 2 η H Δ H B = − Δ H CO 2 R CO 2 −R q Δ H B where RSG is the specific growth rate, RCO2 the specific rate of CO2 evolution, ϵC the fraction of substrate carbon converted into structural biomass or the substrate carbon conversion efficiency, r the respiratory quotient, RO2 the specific rate of O2 uptake, ΔHCO2 the enthalpy change for combustion of substrate per mole of CO2, ηH the fraction of enthalpy produced by oxidation of substrate that is conserved in the biomass synthesized through anabolism (i.e. the enthalpic efficiency), and ΔHB is the enthalpy change for conversion of substrate into structural biomass per C-mole. ΔHCO2 can be obtained from Thornton’s rule, and ΔHB from either heat of combustion or composition data or from growth measurements. Calorespirometric measurements can then be used to obtain values for ϵC and ηH. Measurements of RCO2(or of r and RO2) and the metabolic heat rate, Rq, as functions of environmental variables thus, can be used to rapidly ascertain the growth and metabolic responses of plants to environmental variables. This model and calorespirometric measurements are used to predict the responses of plant growth to differing climates, to predict the global gradient of plant species ranges and diversity, and to predict global treeline temperature conditions. Growth-season temperature and temperature variability are found to be major determinants of growth rates and distributions of plants. These findings may be useful in predicting the response of plants to climate changes.

Fundamental Causes of the Global Patterns of Species Range and Richness1

Global patterns of species range and richness are a consequence of many interacting factors, including environmental conditions, competition, geographical area, and historical/evolutionary development. Two widely studied global patterns of distribution are the latitudinal and elevation gradients of species range and richness. The fundamental mechanisms by which environment and physiology of the plants themselves interact to generate global-scale correlations between increased species range or decreased species richness and latitude/elevation have not previously been established. This paper develops the hypothesis that the primary climatic variables determining global-scale gradients in ectotherm species range and richness are temperature (T) and temperature variability (ΔT), and that the primary physiological variable defining adaptation of ectotherms to temperature is respiratory energy metabolism. This hypothesis is based on a postulate that adaptation of ectotherms to latitudinal/altitudinal gradients of T and ΔT leads to corresponding gradients in properties of energy metabolism. The gradients of metabolic properties give rise to gradients of species range and richness that are observed on a global scale. We demonstrate that natural selection results in ectotherms with metabolic properties matched to their environment and that energy use efficiency and the temperature range allowing growth are inversely related. Thus, opposing selective pressures to increase metabolic energy-use-efficiency or to increase the probability of surviving climate extremes control adaptation of ectotherms to climate. The principles developed in this paper yield fundamental laws of ecology that allow calculation of the contributions of global temperature patterns to the formation of gradients of species range and diversity. Relative values of richness and range are calculated solely from data on abiotic variables. Predictions agree with known patterns of ectotherm distribution.

Cryptogamic crust metabolism in response to temperature, water vapor, and liquid water

Cryptogamic crusts are communities composed of li- chens, cyanobacteria, algae, mosses, and fungi. These integrated soil crusts are susceptible to disturbance, but if intact, appear to play a role in providing nutrients, especially nitrogen, to higher plants. It is not known how or under what conditions desert crusts can grow. Crust samples from localities on the Colorado Plateau and the Great Basin were brought to the laboratory and exposed to atmospheres of different humidity and different levels of liquid water. Both metabolic heat rate (q) and carbon dioxide evolution rate (RCO2) were measured in microcalorimeters at temperatures from 10 to 35 °C. While exposure to water vapor alone had little effect, addition of liquid water caused a marked increase in meta- bolic rate and a switch from anaerobic to aerobic metabolism.

Biological calorimetry and the thermodynamics of the origination and evolution of life

Calorimetric measurements on biological systems from small molecules to whole organisms lead to a new conception of the nature of live matter that has profound consequences for our understanding of biology. The data show that the differences in Gibbs energy (ΔG) and enthalpy (ΔH) are near zero or negative and the difference in entropy (ΔS) is near zero between a random mixture of molecules and live matter of the same composition. A constant input of energy is required to maintain ion gradients, ATP production, and the other functions of living matter, but because cells are organized in a spontaneous process, no energy input is required to maintain the structure or organization of cells. Thus, the origin of life and evolution of complex life forms occurs by thermodynamically spontaneous processes, carbon-based life should be common throughout the universe, and because there is no energy cost, evolution can occur relatively rapidly.

Thermodynamic law for adaptation of plants to environmental temperatures

A thermodynamic law of adaptation of plants to temperature is developed. Plant growth rate is proportional to the product of the metabolic rate and the metabolic efficiency for production of anabolic products. Over much of the growth temperature range, metabolic rate is proportional to mean temperature and efficiency is proportional to the reciprocal of temperature variability. The mean temperature and short-term (hours to weeks) variability of temperature during the growth season at a particular location thus determine the optimum energy and growth strategy for plants. Because they can grow and reproduce most vigorously, plants with a growth rate vs. temperature curve that matches the time-at-temperature vs. temperature curve during the growth season are favored by natural selection. The law of temperature adaptation explains many recent and long-standing observations of plant growth and survival, including latitudinal gradients of plant diversity and species range.

Calorespirometry in Plant Biology

Calorespirometry is a means for understanding how plants adapt and acclimate metabolically to their environment. Analysis of the energetics of respiration shows that measurements of metabolic heat and CO2 rates by calorespirometry, combined with estimates of substrate and biomass composition, are sufficient to calculate substrate carbon-conversion efficiencies, anabolic rates or rates of growth and development, and relative activities of metabolic paths. Calorespirometric measurements can thus be used to rapidly investigate the responses of plant growth and metabolism to varying conditions and to compare the responses of species and genotypes. Calorespirometric and calorimetric methods have been used to determine the temperature dependence of growth rate, temperature limits for growth, the kinetics of both chilling- and high-temperature responses, and the effects of toxins and nutrient deficiencies.

Determination of growth and maintenance coefficients by calorespirometry

This study describes a calorespirometric method for determining the coefficients of the correlation of specific respiration and growth rates. To validate the calorespirometric method, coefficients obtained from calorespirometric data are compared with coefficients obtained from mass and elongation growth rates measured at three temperatures on oat (Avena sativa L.) shoots. Calorespirometric measurements were also made on leaf tissue of varying age from Verbascum thapsus L., Convolvulus arvensis L., and Helianthus tuberosus Nutt. Measurements on A. sativa, C. arvensis and H. tuberosus at several temperatures show maintenance coefficients generally increase with temperature, but, in disagreement with accepted theory, growth coefficients for C. arvensis and A. sativa vary with temperature. A comparison of rates expressed as intensive and extensive quantities showed that the decline in specific respiration and growth rates with age is caused by dilution-by-growth, not down-regulation of respiration rate by reduced demand. The ratio of heat rate to CO2 rate increases with leaf age, and, for fully mature leaves, exceeds the maximum possible value for carbohydrates. This shows that the catabolic substrate may vary with leaf age in immature leaves and cannot be assumed to consist only of carbohydrates in mature leaves. Dilution-by-growth, substrate variation, and inseparability of the variables in the growth-maintenance model all complicate physiological interpretation of the slope and intercept of plots of specific respiration rates v. specific growth rates.

Analysis of respiratory metabolism correlates well with the response of Eucalyptus camaldulensis seedlings to NaCl and high pH

Growth of sand-cultured Eucalyptus camaldulensis Dehnh. (river red gum) seedlings from six wide-ranging provenances was reduced in the presence of 150 mM NaCl, a high pH of 9.5, and combined NaCl and high pH, compared with no applied NaCl and neutral pH. Effects of these stress conditions on respiration rates and substrate carbon conversion efficiencies of rapidly-expanding leaf tissue were measured with calorespirometric techniques. Growth rates were calculated from respiration parameters. Respiration rate, measured as metabolic heat production rate (q), showed no consistent trend with either NaCl or high pH, whereas the rate measured as CO2 production rate (R CO2) was generally lower with both treatments. The ratio of heat lost per mole of CO2 produced [q/(R CO2)] was consistently increased by both stresses. Stress causes a larger fraction of metabolic energy produced by aerobic metabolism to be lost as heat, relative to non-stressed controls. Consequently, a larger fraction of photosynthetic product in stressed seedlings must be metabolized to CO2 per mole of C incorporated into biomass. Our results indicate that 0.42 mol substrate C is converted to CO2 per mole C incorporated into biomass for control plants, compared with 0.96 mol for plants treated with combined NaCl and high pH. Respiratory responses to treatment varied with provenance. Specific growth rates, calculated from repiratory parameters (q and RCO2) of stressed E. camaldulensis seedlings, generally paralleled experimentally-determined reduced growth (dry weight) of these seedlings. Thus, measurements of leaf respiration allow calculation of growth inhibition caused by NaCl and high pH stress. However, we could not discriminate among provenances in this experiment with only one level of NaCl and pH.

Metabolic Rate of Barley Root as a Continuous Function of Temperature

Summary As part of an effort to define the nature of the physical changes in plant cells that trigger temperature stress responses, metabolic rates of root tissues of three barley (Hordeum vulgare L.) cultivars were determined by differential temperature scanning calorimetry. Metabolic rate data were determined as a continuous function of temperature from near freezing to high temperatures that thermally inactivated metabolism. Two abrupt changes in metabolism were found, a largely reversible change resulting in a greatly increased temperature dependence at about 30 °C and an irreversible high temperature inactivation about four degrees higher. The temperatures at which these abrupt deviations from linear Arrhenius kinetics occurred were affected by degree of saturation of the lipids in root tissues, salt concentration in the medium, and the time-temperature program used in raising the samples to elevated temperatures. No physicochemical events were observed calorimetrically in temperature ranges where abrupt changes in metabolic rate were noted. Thus, if such a physicochemical change is the triggering event in high temperature stress responses in this species, it must involve less than about 5% of the total lipids or proteins in a first order event or be a thermodynamically higher order event.

Effects of climate on growth traits of river red gum are determined by respiration parameters

Temperature is the major uncontrollable climate variable in plantation forestry. Matching plants to climate is essential for optimizing growth. Matching is usually done with field trials because of the lack of a predictive relation between laboratory measurements of physiological responses and climatic factors affecting growth. This paper evaluates the potential of using respiration parameters for selection of appropriate drainage or seed sources within a drainage for superior growth in a particular climate. The growth traits measured are tree height, stem diameter and stem volume. The respiratory parameters measured are respiratory heat rate, rate of CO2 production, and temperature dependence of respiratory heat rate. Five open-pollinated families from each of nine seed sources of river red gum (Eucalyptus camaldulensis Dehnh.) were studied following selection from a larger set of seed sources planted at three plantations in California. The three plantations differ in climate, particularly in extreme temperatures, diurnal temperature variability and total rainfall. Within each plantation, growth and respiration parameters show high genetic variation (overall coefficient of variation (CV) = 14-58%, family CV = 11-33%), with at least one of these traits showing significant (P < 0.10) difference due to drainage, or source within drainage, or families within source. The relationship of growth to respiration for each trait differs, depending on test plantation, origin drainage, source or family, suggesting a unique pattern for each trait. Correlation of drainage level averages between growth and respiration were strongly negative and significant (P = 0.10-0.01). Rankings for drainages between paired plantations were strong and significant (P = 0.10-0.05) only for respiration, but not for growth traits.