Carbon balance,productivity, and water use of cold-winter desert shrub communities dominated by C3 and C4 species

Summary Common generalizations concerning the ecologic significance of C₄ photosynthesis were tested in a study of plant gas exchange, productivity, carbon balance, and water use in monospecific communities of C₃ and C₄ salt desert shrubs. Contrary to expectations, few of the hypotheses concerning the performance of C₄ species were supported. Like the C₃ species, Ceratoides lanata, the C₄ shrub, Atriplex confertifolia, initiated growth and photosynthetic activity in the cool spring months and also exhibited maximum photosynthetic rates at this time of year. To compete successfully with C₃ species, Atriplex may have been forced to evolve the capacity for photosynthesis at low temperatures prevalent during the spring when moisture is most abundant. Maximum photosynthetic rates of Atriplex were lower than those of the C₃ species. This was compensated by a prolonged period of low photosynthetic activity in the dry late summer months while Ceratoides became largely inactive. However, the annual photosynthetic carbon fixation per ground area was about the same in these two communities composed of C₃ and C₄ shrubs. The C₄ species did not exhibit greater leaf diffusion resistance than the C₃ species. The photosynthesis/transpiration ratios of the two species were about the same during the period of maximum photosynthetic rates in the spring. During the warm summer months the C₄ species did have superior photosynthesis/transpiration ratios. Yet, since Ceratoides completed a somewhat greater proportion of its annual carbon fixation earlier in the season, the ratio of annual carbon fixation/transpiratory water loss in the two communities was about the same. Atriplex did incorporate a greater percentage of the annual carbon fixation into biomass production than did Ceratoides. However, this is considered to be a reflection of properties apart from the C₄ photosynthetic pathway. Both species displayed a heavy commitment of carbon to the belowground system, and only about half of the annual moisture resource was utilized in both communities.     

Effect of varying environments on photosynthetic parameters of C3, C3-C4 and C4 species of Panicum

Summary CO₂ exchange characteristics and the activity of the carboxylating enzymes phosphoenolpyruvate carboxylase (PEP-C, E.C. 4.1.1.31) and ribulose 1,5-bisphosphate carboxylase (RuBP-C, E.C. 4.1.1.39) during one year in the greenhouse and at two levels of light and temperature in growth chambers were determined in the C₃-C₄ intermediate species P. milioides Nees ex. Trin. These results were compared with those of P. bisulcatum Thumb. (C₃) and P. maximum Jacq. (C₄). Under all tested conditions, and even when the influence of leaf surface temperature on photosynthetic rates and CO₂ compensation points were measured, the biochemical and physiological behaviour of the C₃-C₄ intermediate was more similar to that of the C₃ plant than the C₄ species. The C₄ plant P. maximum, however, responded positively, mainly in terms of PEP-C activity and photosynthetic rate, to the regime of high light and temperature. The results presented indicate that in the C₃-C₄ Panicum grown in high light and temperature no direct relationships between a low CO₂ compesation point and superior growth are evident. It has still to be clarified why in nature a photosynthetic-photorespiratory pathway leading to an intermediate CO₂ compensation value has evolved in P. milioides.     

Modelling C3 and C4 photosynthesis under water-stressed conditions

Despite the observed impact of water stress on photosynthesis, some of the most used models of CO₂ assimilation in C₃ and C₄ functional types do not directly account for it. We discuss an extension of these models, which explicitly includes the metabolic and diffusive limitations due to water stress on photosynthesis. Functional relationships describing the photosynthetic processes and CO₂ diffusion inside leaves are modified to account for leaf water status on the basis of experimental results available in the literature. Extensive comparison with data shows that the model is suitable to describe the reduction in CO₂ assimilation rate with decreasing leaf water potentials in various species. A simultaneous analysis of photosynthesis, transpiration and soil moisture dynamics is then carried out to explore the actual impact of drought on different photosynthesis processes and on the overall plant activity. The model well reproduces measured CO₂ assimilation rate as a function of soil moisture and could be useful to formulate hypotheses for detailed experiments as well as to simulate in detail transpiration and photosynthesis dynamics under water stress.     

Long-term photosynthetic response in single leaves of A C3 and C4 salt marsh species grown at elevated atmospheric CO2 in situ

Summary Mono-specific communities of the C₃ sedge, Scirpus olneyi and the C₄ grass, Spartina patens, were exposed to normal ambient or elevated CO₂, (ca. 680 l l^–1) throughout the 1987 and 1988 growing seasons in open-top field chambers located on a tidal marsh. Single stems of C₃ plants grown in ambient or elevated CO₂ showed an increased photosynthetic rate when tested at elevated CO₂ for both seasons. This increase in photosynthetic response in the C₃ species was maintained throughout the 1987 and 1988 growing season. The stimulation of photosynthesis with elevated CO₂ appeared to increase as temperature increased and decreased as photosynthetic photon flux (PPF) increased. Analysis of the photosynthetic response of the C₃ species during the 1988 season indicated that significant differences in light-saturated photosynthetic rate between ambient and elevated CO₂ conditions continued until October. In contrast to the C₃ sedge, the C₄ grass showed no significant photosynthetic increase to elevated CO₂ except at the beginning of the 1988 season.     

Insect herbivory on C3 and C4 grasses

Summary This study tested the hypothesis that grasses with the C₄ photosynthetic pathway are avoided as a food source by insect herbivores in natural communities. Insects were sampled from ten pairs of C₃–C₄ grasses and their distributions analyzed by paired comparisons tests. Results showed no statistically significant differences in herbivore utilization of C₃–C₄ species. However, there was a trend towards heavier utilization of C₃ species when means for both plant groups were compared. In particular, Homoptera and Diptera showed heavier usage of C₃ plants. Significant correlations between insect abundances and plant protein levels suggest that herbivores respond to the higher protein content of C₃ grasses. ¹³C values for six of the most common grasshopper species in the study area indicated that three species fed on C₃ plants, two species fed on C₄ plants, and one species consumed a mixture of C₃ and C₄ tissue.Welder Wildlife Refuge Contribution Number 213     

Photorespiratory properties of protoplasts from C3-C4 intermediate species of moricandia

Protoplasts were isolated from leaves of the C₃-C₄ intermediate species, Moricandia arvensis (L.) DC. and Moricandia spinosa Pomel. Analysis by light and transmission electron microscopy indicated that these purified preparations contained both mesophyll protoplasts (MP) and bundle-sheath protoplasts (BSP). Conventional density gradient centrifugation procedures failed to yield separations of pure protoplasts from each cell-type. With these heterogeneous suspensions of MP and BSP, values measured for (i) the percentage inhibition of photosynthetic CO₂ fixation by O₂, (ii) the apparent K_m(CO)2 of photosynthesis, and (iii) dark/light ratios of the rate of ¹⁴CO₂ evolution during decarboxylation of exogenous [1-¹⁴C] glycine were not significantly different from those determined for protoplast preparations from related or representative C₃ plants, including M. foetida, Nicotiana tabacum, and Triticum aestivum. In contrast, previous comparisons with C₃ species, using intact leaf tissue from M. arvensis, have shown a reduced sensitivity of net photosynthesis to inhibition by O₂ [Holaday et al., Plant Sci. Lett., 27 (1982) 181] and an enhanced capacity for the photosynthetic refixation of CO₂ evolved during decarboxylation of exogenous photorespiratory substrates [Holbrook et al., Plant Physiol., 77 (1985) 578]. We conclude that these photosynthetic properties, associated with reduced photorespiration by M. arvensis and M. spinosa, are dependent upon the integrity of the anatomical and ultrastructural arrangement of bundle-sheath and mesophyll cells in these C₃-C₄ intermediate species.     

Photosynthetic Enzyme Activities and Localization in Mollugo verticillata Populations Differing in the Levels of C(3) and C(4) Cycle Operation

Ecotypic differences in the photosynthetic carbon metabolism of Mollugo verticillata were studied. Variations in C₃ and C₄ cycle activity are apparently due to differences in the activities of enzymes associated with each pathway. Compared to C₄ plants, the activities of C₄ pathway enzymes were generally lower in M. verticillata, with the exception of the decarboxylase enzyme, NAD malic enzyme. The combined total carboxylase enzyme activity of M. verticillata was greater than that of C₃ plants, possibly accounting for the high photosynthetic rates of this species. Unlike either C₃ or C₄ plants, ribulose bisphosphate carboxylase was present in both mesophyll and bundle sheath cell chloroplasts in M. verticillata. The localization of this enzyme in both cells in this plant, in conjunction with an efficient C₄ acid decarboxylation mechanism most likely localized in bundle sheath cell mitochondria, may account for intermediate photorespiration levels previously observed in this species.     

Photosynthetic,hydraulic and biomass properties in closely related C3 and C4 species

In plants, most water is absorbed by roots and transported through vascular conduits of xylem which evaporate from leaves during photosynthesis. As photosynthesis and transport processes are interconnected, it was hypothesized that any variation in water transport demand influencing water use efficiency (WUE), such as the evolution of C₄ photosynthesis, should affect xylem structure and function. Several studies have provided evidence for this hypothesis, but none has comprehensively compared photosynthetic, hydraulic and biomass allocation properties between C₃ and C₄ species. In this study, photosynthetic, hydraulic and biomass properties in a closely related C₃ Tarenaya hassleriana and a C₄ Cleome gynandra are compared. Light response curves, measured at 30°C, showed that the C₄ C. gynandra had almost twice greater net assimilation rates than the C₃ T. hassleriana under each increasing irradiation level. On the contrary, transpiration rates and stomatal conductance were around twice as high in the C₃, leading to approximately 3.5 times higher WUE in the C₄ compared with the C₃ species. The C₃ showed about 3.3 times higher hydraulic conductivity, 4.3 times greater specific conductivity and 2.6 times higher leaf‐specific conductivity than the C₄ species. The C₃ produced more vessels per xylem area and larger vessels. All of these differences resulted in different biomass properties, where the C₄ produced more biomass in general and had less root to shoot ratio than the C₃ species. These results are in support of our previous findings that WUE, and any changes that affect WUE, contribute to xylem evolution in plants.     

Soil salinity determines the relative abundance of C3/C4 species in Argentinean grasslands

Aim The C₄ and crassulacean acid metabolism (CAM) pathways are adaptations to compensate for high rates of photorespiration and water and carbon deficiency. This is the first attempt to compare the relative abundance of C₃ vs. C₄ + CAM species in temperate and subtropical grasslands across a latitudinal gradient in central Argentina. We predict that under the same rainfall regime, C₄ + CAM plants will have larger soil coverage in highly saline soils than in neighbouring non‐saline ones. Location Data were taken from three phytogeographical provinces in the Santa Fe province of Argentina: Chaquenian, Pampean and Espinal. Methods The salinity of the soil was estimated through aqueous solution conductivity. The proportions of species belonging to C₃/C₄ + CAM photosynthetic pathways were compared among halophyte and non‐halophyte communities with a χ² homogeneity test. The sum of cover percentages corresponding to the C₃ and C₄ + CAM photosynthetic pathways were calculated and compared using analysis of variance (ANOVA). Results The soil conductivity values were higher in the halophyte than in the non‐halophyte communities for the same phytogeographical area. The C₄ + CAM plants had much higher soil coverage values in halophyte than in non‐halophyte communities in the Pampean and Espinal phytogeographical provinces. The differences were not statistically significant in the Chaquenian province. Main conclusions Soil drought provoked by soil salinity results in a much higher soil cover by C₄ + CAM plants in regions with positive to neutral water balance (i.e. Pampean and Espinal). This differential abundance pattern in C₄ + CAM functional group is not observed in areas where a pronounced water deficit exists per se (Chaquenian region), and therefore C₄ + CAM plants predominate in all environments regardless of soil salinity. Our results suggest that one of the main environmental forces driving the upsurge of C₄ species in Argentinean grasslands might have been the strong local soil salinity gradient.     

Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation

Most plants show considerable capacity to adjust their photosynthetic characteristics to their growth temperatures (temperature acclimation). The most typical case is a shift in the optimum temperature for photosynthesis, which can maximize the photosynthetic rate at the growth temperature. These plastic adjustments can allow plants to photosynthesize more efficiently at their new growth temperatures. In this review article, we summarize the basic differences in photosynthetic reactions in C₃, C₄, and CAM plants. We review the current understanding of the temperature responses of C₃, C₄, and CAM photosynthesis, and then discuss the underlying physiological and biochemical mechanisms for temperature acclimation of photosynthesis in each photosynthetic type. Finally, we use the published data to evaluate the extent of photosynthetic temperature acclimation in higher plants, and analyze which plant groups (i.e., photosynthetic types and functional types) have a greater inherent ability for photosynthetic acclimation to temperature than others, since there have been reported interspecific variations in this ability. We found that the inherent ability for temperature acclimation of photosynthesis was different: (1) among C₃, C₄, and CAM species; and (2) among functional types within C₃ plants. C₃ plants generally had a greater ability for temperature acclimation of photosynthesis across a broad temperature range, CAM plants acclimated day and night photosynthetic process differentially to temperature, and C₄ plants was adapted to warm environments. Moreover, within C₃ species, evergreen woody plants and perennial herbaceous plants showed greater temperature homeostasis of photosynthesis (i.e., the photosynthetic rate at high-growth temperature divided by that at low-growth temperature was close to 1.0) than deciduous woody plants and annual herbaceous plants, indicating that photosynthetic acclimation would be particularly important in perennial, long-lived species that would experience a rise in growing season temperatures over their lifespan. Interestingly, across growth temperatures, the extent of temperature homeostasis of photosynthesis was maintained irrespective of the extent of the change in the optimum temperature for photosynthesis (T _opt), indicating that some plants achieve greater photosynthesis at the growth temperature by shifting T _opt, whereas others can also achieve greater photosynthesis at the growth temperature by changing the shape of the photosynthesis–temperature curve without shifting T _opt. It is considered that these differences in the inherent stability of temperature acclimation of photosynthesis would be reflected by differences in the limiting steps of photosynthetic rate.     

Le vie fotosintetiche C3, C4 e CAM nel contesto ecologico

Abstract

Ecological aspects of C₃, C₄ and CAM photosynthetic pathways. - Three different photosynthetic CO₂ fixation pathways are known to occur in higher plants. However all three pathways ultimately depend on the Calvin-Benson cycle for carbon reduction. The oxygenase activity of RuBP carboxilase is responsible for photorespiratory CO₂ release. Both C₄ and CAM pathways behave as a CO₂ concentrating mechanism which prevent photorespiration. The CO₂-concentrating mechanism in C₄ plants is based on intracellular symplastic transport of C₄ dicarboxylic acids from mesophyll-cells to the adjacent bundle-sheath cells. On the contrary in CAM plants the CO₂-concentrating mechanism is based on the intracellular transport of malic acid into and out of the vacuole.

The C₄ photosynthetic pathway as compared to the C₃ pathway permits higher rates of CO₂ fixation in high light and high temperature environments at low costs in terms of water loss, given the stability of the photosynthetic apparatus under such conditions.

CAM is interpreted as an adaptation to arid environments because it enables carbon assimilation to take place at very low water costs during the night when the evaporative demand is low. Nevertheless many aquatic species of Isoetes and some relatives are CAM, suggesting the adaptive role of CAM to environments which become depleted in CO₂.

The photosynthetic carbon fixation pathway certainly contributes to the ecological success of plants in different environments. However the distribution of plants may also reflect their biological history. On the other hand plants with different photosynthetic pathways coexist in many communities and tend to share resources in time. In any case some generalizations are possible: C₄ plants enjoy an ecological advantage in hot, moist, high light regions while the majority of species in desert environments are C₃; CAM plants are more frequent in semiarid regions with seasonal rainfall, coastal fog deserts, and in epiphytic habitats in tropical rain forests.     

Flaveria pringlei (C3) andFlaveria trinervia (C4) under NaCl stress

The C₄ speciesFlaveria trinervia is obviously better adapted to saline environments than the C₃ speciesF. pringlei. Treatment with 100 mM NaCl diminished crop growth rate inF. pringlei by 38% but not inF. trinervia. Under saline conditions, more assimilates were invested in leaf growth inF. trinervia but not inF. pringlei. Electrolyte concentration inF. trinervia in control and salt treated plants is lower than inF. pringlei. Fluorescence data do not indicate a damage of PS 2 charge separation in both species. Whether the C₄ photosynthetic pathway inF. trinervia is responsible for the improved salt tolerance compared toF. pringlei remains an open question.     

Phenology and Productivity of C3 and C4 Grasslands in Hawaii

Grasslands account for a large proportion of global terrestrial productivity and play a critical role in carbon and water cycling. Within grasslands, photosynthetic pathway is an important functional trait yielding different rates of productivity along environmental gradients. Recently, C₃-C₄ sorting along spatial environmental gradients has been reassessed by controlling for confounding traits in phylogenetically structured comparisons. C₃ and C₄ grasses should sort along temporal environmental gradients as well, resulting in differing phenologies and growing season lengths. Here we use 10 years of satellite data (NDVI) to examine the phenology and greenness (as a proxy for productivity) of C₃ and C₄ grass habitats, which reflect differences in both environment and plant physiology. We perform phylogenetically structured comparisons based on 3,595 digitized herbarium collections of 152 grass species across the Hawaiian Islands. Our results show that the clade identity of grasses captures differences in their habitats better than photosynthetic pathway. Growing season length (GSL) and associated productivity (GSP) were not significantly different when considering photosynthetic type alone, but were indeed different when considering photosynthetic type nested within clade. The relationship between GSL and GSP differed most strongly between C₃ clade habitats, and not between C₃-C₄ habitats. Our results suggest that accounting for the interaction between phylogeny and photosynthetic pathway can help improve predictions of productivity, as commonly used C₃-C₄ classifications are very broad and appear to mask important diversity in grassland ecosystem functions.     

Differential responses of plant functional trait to grazing between two contrasting dominant C3 and C4 species in a typical steppe of Inner Mongolia, China

Plant functional traits have been widely used to study the linkage between environmental drivers, trade-offs among different functions within a plant, and ecosystem structure and functioning. Here, the whole-plant traits, leaf morphological and physiological traits of two dominant species, Leymus chinensis (C₃ perennial rhizome grass) and Cleistogenes squarrosa (C₄ perennial bunchgrass), were studied in the Inner Mongolia grassland of China, with a grazing experiment including five stocking rates (0, 3.0, 4.5, 7.5, and 9.0 sheep/ha) in 2008 (wet year) and 2009 (dry year). Our results demonstrated that, for both species, the effects of stocking rate, year, and stocking rate?×?year on whole-plant traits and leaf morphological and physiological traits were highly significant in most cases. The differential responses of plant trait to variation in precipitation were caused by trait trade-offs between the wet and dry years. L. chinensis adopted the high N content and net photosynthetic rate (P_n) in the wet year but both the low N content and P_n in the dry year under grazed conditions. The trait trade-offs of C. squarrosa were characterized by high specific leaf area (SLA) and P_n in the dry year vs. low SLA and P_n in the wet year. Our findings also indicate that C. squarrosa is more resistant to grazing than L. chinensis in terms of avoidance and tolerance traits, particularly under heavy grazing pressure and in the dry year.     

Biochar amendment boosts photosynthesis and biomass in C3 but not C4 plants: A global synthesis

Biochar is a carbon (C)‐rich solid produced from the thermochemical pyrolysis of biomass. Its amendment to soils has been proposed as a promising mean to mitigate greenhouse gas emissions and simultaneously benefit agricultural crops. However, how biochar amendment affects plant photosynthesis and growth remains unclear, especially on a global scale. In this study, we conducted a global synthesis of 74 publications with 347 paired comparisons to acquire an overall tendency of plant photosynthesis and growth following biochar amendment. Overall, we found that biochar amendment significantly increased photosynthetic rate by 27.1%, and improved stomatal conductance, transpiration rate, water use efficiency, and chlorophyll concentration by 19.6%, 26.9%, 26.8%, and 16.1%, respectively. Meanwhile, plant total biomass, shoot biomass, and root biomass increased by 25.4%, 22.1%, and 34.4%, respectively. Interestingly, plant types (C₃ and C₄ plants) showed greater control over plant photosynthesis and biomass than a broad suite of soil and biochar factors. Biochar amendment largely boosted photosynthesis and biomass on C₃ plants, but had a limited effect on C₄ plants. Our results highlight the importance of the differential response of plant types to biochar amendment with respect to plant growth and photosynthesis, providing a scientific foundation for making reasonable strategies towards an extensive application of biochar for agricultural production management.     

The photosynthetic response of C3 and C4 bioenergy grass species to fluctuating light

Bioenergy grass species are a renewable energy source, but their productivity has not been fully realized. Improving photosynthetic efficiency has been proposed as a mechanism to increase the productivity of bioenergy grass species. Fluctuating light, experienced by all field grown crops, is known to reduce photosynthetic efficiency. This experiment aimed to evaluate the photosynthetic performance of both C₃ and C₄ bioenergy grass species under steady state and fluctuating light conditions by examining leaf gas exchange. The fluctuating light regime used here decreased carbon assimilation across all species when compared to expected steady state values. Overall, C₄ species assimilated more carbon than C₃ species during the fluctuating light regime, with both photosynthetic types assimilating about 16% less carbon than expected based on steady state measurements. Little diversity was observed in response to fluctuating light among C₃ species, and photorespiration partially contributed to the rapid decreases in net photosynthetic rates during high to low light transitions. In C₄ species, differences among the four NADP-ME species were apparent. Diversity observed among C₄ species in this experiment provides evidence that photosynthetic efficiency in response to fluctuating light may be targeted to increase C₄ bioenergy grass productivity.     

Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment

Phylogenetic analyses show that C₄ grasses typically occupy drier habitats than their C₃ relatives, but recent experiments comparing the physiology of closely related C₃ and C₄ species have shown that advantages of C₄ photosynthesis can be lost under drought. We tested the generality of these paradoxical findings in grass species representing the known evolutionary diversity of C₄ NADP‐me and C₃ photosynthetic types. Our experiment investigated the effects of drought on leaf photosynthesis, water potential, nitrogen, chlorophyll content and mortality. C₄ grasses in control treatments were characterized by higher CO₂ assimilation rates and water potential, but lower stomatal conductance and nitrogen content. Under drought, stomatal conductance declined more dramatically in C₃ than C₄ species, and photosynthetic water‐use and nitrogen‐use efficiency advantages held by C₄ species under control conditions were each diminished by 40%. Leaf mortality was slightly higher in C₄ than C₃ grasses, but leaf condition under drought otherwise showed no dependence on photosynthetic‐type. This phylogenetically controlled experiment suggested that a drought‐induced reduction in the photosynthetic performance advantages of C₄ NADP‐me relative to C₃ grasses is a general phenomenon.