The quantum yield for CO2 uptake in C3 and C4 grasses

The quantum yield for CO₂ uptake was measured in C₃ and C₄ monocot species from several different grassland habitats. When the quantum yield was measured in the presence of 21% O₂ and 340 cm³ m^-3 CO₂, values were very similar in C₃ monocots, C₃ dicots, and C₄ monocots (0.045–0.056 mole CO₂ · mole^-1 quanta absorbed). In the presence of 2% O₂ and 800 cm³ m^-3 CO₂, enhancements of the quantum yield values occurred for the C₃ plants (both monocots and dicots), but not for C₄ monocots. A dependence of the quantum yield on leaf temperature was observed in the C₃ grass, Agropyron smithii, but not in the C₄ grass, Bouteloua gracilis, in 21% O₂ and 340 cm³ m^-3 CO₂. At leaf temperatures between 22–25°C the quantum yield values were approximately equal in the two species.     

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     

Implications of interveinal distance for quantum yield in C<Subscript>4</Subscript> grasses: a modeling and meta-analysis

The distance between veins has the potential to affect photosynthesis in C₄ grasses because photon capture and photosynthetic carbon reduction are primarily restricted to vascular bundle sheath cells (BSC). For example, BSC density should increase as interveinal distance (IVD) decreases, and thus IVD may influence photon capture and photosynthesis in C₄ grasses. The objective of this study is to evaluate the potential importance of IVD to the function of C₄ grasses, and a literature survey is conducted to test the hypothesis that quantum yield of photosynthesis () increases with decreasing IVD. First, a meta-analysis of and IVD values obtained for 12 C₄ grass species supports this hypothesis as and IVD are significantly negatively correlated (r=–0.61). Second, a regression of carbon isotope discrimination () versus IVD was conducted and the regression equation was used in a simple biochemical model that relates to and leakage of CO₂ from the BSC. The modeling analysis also supports the hypothesis that decreases with increasing IVD in C₄ grasses. C₄ grasses are virtually absent from shaded habitats, and the biochemical model is employed to examine the implications of IVD for shade-tolerance in C₄ grasses. The model predicts that only those species with uncommonly small IVD values are able to tolerate prolonged shade.     

Improving our understanding of environmental controls on the distribution of C3 and C4 grasses

A number of studies have demonstrated the ecological sorting of C₃ and C₄ grasses along temperature and moisture gradients. However, previous studies of C₃ and C₄ grass biogeography have often inadvertently compared species in different and relatively unrelated lineages, which are associated with different environmental settings and distinct adaptive traits. Such confounded comparisons of C₃ and C₄ grasses may bias our understanding of ecological sorting imposed strictly by photosynthetic pathway. Here, we used MaxEnt species distribution modeling in combination with satellite data to understand the functional diversity of C₃ and C₄ grasses by comparing both large clades and closely related sister taxa. Similar to previous work, we found that C₄ grasses showed a preference for regions with higher temperatures and lower precipitation compared with grasses using the C₃ pathway. However, air temperature differences were smaller (2 °C vs. 4 °C) and precipitation and % tree cover differences were larger (1783 mm vs. 755 mm, 21.3% vs. 7.7%, respectively) when comparing C₃ and C₄ grasses within the same clade vs. comparing all C₄ and all C₃ grasses (i.e., ignoring phylogenetic structure). These results were due to important differences in the environmental preferences of C₃ BEP and PACMAD clades (the two main grass clades). Winter precipitation was found to be more important for understanding the distribution and environmental niche of C₃ PACMADs in comparison with both C₃ BEPs and C₄ taxa, for which temperature was much more important. Results comparing closely related C₃–C₄ sister taxa supported the patterns derived from our modeling of the larger clade groupings. Our findings, which are novel in comparing the distribution and niches of clades, demonstrate that the evolutionary history of taxa is important for understanding the functional diversity of C₃ and C₄ grasses, and should have implications for how grasslands will respond to global change.     

The ecological distribution of C4 and C3 grasses in the Hawaiian Islands

Summary Isoenzyme analyses were carried out on the hypotetraploid Stellaria media and the diploid Stellaria pallida occurring on abandoned sandy fields in the coastal dunes of the Netherlands. Amylase isoenzymes in germinating seeds of Stellaria media showed a striking intrapopulational variability, which is in accordance with the germination behaviour of the different subpopulations. In contrast to these findings no intrapopulational variation nor developmental change in isoenzyme pattern could be detected on basis of 14 other analysed leaf enzymes. For five enzymes there was a difference in isoenzyme pattern between the species Stellaria media and Stellaria pallida. Of these five enzymes two showed an interpopulational variation in Stellaria media. The fact that there was almost no variability of the isoenzyme pattern in Stellaria pallida could be explained by the permanent autogamous (cleistogamous) state of the species. Effects of polyploidy on the isoenzyme pattern and its activity could not be demonstrated. Consequences of the extreme difference between the monomorphic pattern of the leaf enzymes as opposed to the polymorphism of the amylase are discussed in view of the difference in germination ecology and lifecycle strategy of Stellaria media subpopulations.     

The small scale spatial pattern of C3 and C4 grasses depends on shrub distribution

At micro‐site scale, the spatial pattern of a plant species depends on several factors including interactions with neighbours. It has been seen that unfavourable effects generate a negative association between plants, while beneficial effects generate a positive association. In grasslands, the presence of shrubby species promotes a particular microenvironment beneath their canopy that could affect differently the spatial distribution of plants with different tolerance to abiotic conditions. We measured photosynthetic active radiation, air temperature and wind speed under shrub canopies and in adjacent open sites and analysed the spatial distribution of four grass species (two C₃ and two C₄) in relation to shrub canopy in a grazed sub‐humid natural grassland in southern Uruguay. Radiation, air temperature and wind speed were lower under shrubs than in adjacent open sites. The spatial distribution of grasses relative to the shrub canopy varied depending on the photosynthetic metabolism of grasses. C₄ grasses showed a negative association or no correlation with the shrubs, whereas C₃ grasses showed a positive association. Our results highlight the importance of the photosynthetic metabolism of the grasses in the final outcome of interactions between grasses and shrubs. Micro‐environmental conditions generated underneath shrubs create a more suitable site for the establishment of C₃ than for C₄ grasses. These results show that facilitation could be more important than previously thought in sub‐humid grasslands.     

Leaf cold acclimation and freezing injury in C3 and C4 grasses of the Mongolian Plateau

The scarcity of C4 plants in cool climates is usually attributed to their lower photosynthetic efficiency than C3 species at low temperatures. However, a lower freezing resistance may also decrease the competitive advantage of C4 plants by reducing canopy duration, especially in continental steppe grasslands, where a short, hot growing season is bracketed by frost events. This paper reports an experimental test of the hypothesis that cold acclimation is negligible in C4 grasses, leading to greater frost damage than in C3 species. The experiments exposed six C3 and three C4 Mongolian steppe grasses to 20 d chilling or control pre-treatments, followed by a high-light freezing event. Leaf resistance to freezing injury was independent of photosynthetic type. Three C3 species showed constitutive freezing resistance characterized by <20% leaf mortality, associated with high photosynthetic carbon fixation and electron transport rates and low leaf osmotic potential. One freezing-sensitive C4 species showed the expected pattern of chilling-induced damage to photosynthesis and >95% leaf mortality after the freezing event. However, three C3 and two C4 species displayed a cold acclimation response, showing significant decreases in osmotic potential and photosynthesis after exposure to chilling, and a 30-72% reduction of leaf freezing injury. This result suggested that down-regulation of osmotic potential may be involved in the cold acclimation process, and demonstrated that there is no inherent barrier to the development of cold acclimation in C4 species from this ecosystem. Cold acclimation via osmoregulation represents a previously undescribed mechanism to explain the persistence of C4 plants in cool climates.     

Influence of contrasting availabilities of water and nutrients on the radiation use efficiency in C3 and C4 grasses

The radiation use efficiency (RUE) model is one of the most used tools to generate large spatial and temporal scale net primary productivity (NPP) estimations by remote sensing. It involves two key issues to make accurate estimations of NPP: the estimation of the fraction of photosynthetically active radiation (PAR) intercepted by vegetation (fPAR) and the estimation of the plant RUE. The objectives of this work were to quantify the above‐ground RUE under optimal water and nutrient conditions in two C₃ and one C₄ grass species and to analyse the effect of restrictions in these factors upon RUE by comparing both metabolic pathways. Grasses were cultivated from seeds and four treatments combining contrasting availabilities of water and nutrients were applied. RUE values were calculated from measurements of the incoming PAR, fPAR and productivity. In each of the species, plants with sufficient water and nutrients showed the highest RUE (2.61–3.52 g MJ^?1), whereas those with deficiencies in both resources presented the lowest RUE (1.15–2.39 g MJ^?1). Cynodon dactylon (C₄) was the species with higher value of RUE and no significant differences were detected between treatments. However, no significant differences were detected between C. dactylon and D. glomerata under no stress treatment (N1W1) and between C. dactylon and L. perenne under water stress treatment (N1W0). RUE values of Dactylis glomerata (C₃) diminished if only one of the two stress factors was presented, while Lolium perenne (C₃) only when both stress factors were present. The decreases under stress treatments were between 35% and 60% compared with the no stress treatment. When regional NPP is estimated it is therefore important to take into account the decrease in the RUE, especially in areas under severe stress.     

Habitat‐specific differences in plasticity of foliar δ13C in temperate steppe grasses

A decrease in foliar δ¹³C with increasing precipitation is a common tendency in steppe plants. However, the rate of decrease has been reported to differ between different species or populations. We here hypothesized that plant populations in the same habitat of temperate steppes may not differ in foliar δ¹³C response patterns to precipitation, but could differ in the levels of plasticity of foliar δ¹³C across different habitats. In order to test this hypothesis, we conducted controlled watering experiments in northeast China at five sites along a west–east transect at latitude 44°N, which show substantial interannual fluctuations and intra‐annual changes in precipitation among them. In 2001, watering treatment (six levels, three replicates) was assigned to 18 plots at each site. The responses of foliar δ¹³C to precipitation (i.e., the sum of watering and rainfall) were determined in populations of several grass species that were common across all sites. Although similar linear regression slopes were observed for populations of different species growing at the same site, significantly different slopes were obtained for populations of the same species growing at different sites. Further, the slope of the line progressively decreased from Site I to Site V for all species in this study. These results suggest habitat‐specific differences in plasticity of foliar δ¹³C in temperate steppe grasses. This indicates that species' δ¹³C response to precipitation is conservative at the same site due to their long‐term acclimation, but the mechanism responsible behind this needs further investigations.     

Mycorrhizal symbiosis induces plant carbon reallocation differently in C3 and C4 Panicum grasses

Plant and Soil - Although arbuscular mycorrhizal symbiosis is common in many plants with either C3 or C4 photosynthesis, it remains poorly understood whether photosynthesis type has any significant...     

Comparative analysis of thylakoid protein complexes in the mesophyll and bundle sheath cells from C3, C4 and C3–C4 Paniceae grasses

To better understand the coordination between dark and light reactions during the transition from C₃ to C₄ photosynthesis, we optimized a method for separating thylakoids from mesophyll (MC) and bundle sheath cells (BSCs) across different plant species. We grew six Paniceae grasses including representatives from the C₃, C₃–C₄ and C₄ photosynthetic types and all three C₄ biochemical subtypes [nicotinamide adenine dinucleotide phosphate‐dependent malic enzyme (NADP‐ME), nicotinamide adenine dinucleotide‐dependent malic enzyme (NAD‐ME) and phosphoenolpyruvate carboxykinase (PEPCK)] in addition to Zea mays under control conditions (1000 μmol quanta m^?2 s^?1 and 400 ppm of CO₂). Proteomics analysis of thylakoids under native conditions, using blue native polyacrylamide gel electrophoresis followed by liquid chromatography‐mass spectrometry (LC‐MS), demonstrated the presence of subunits of all light‐reaction‐related complexes in all species and cell types. C₄ NADP‐ME species showed a higher photosystems I/II ratio and a clear accumulation of the NADH dehydrogenase‐like complexes in BSCs, while Cytb₆f was more abundant in BSCs of C₄ NAD‐ME species. The C₄ PEPCK species showed no clear differences between cell types. Our study presents, for the first time, a good separation between BSC and MC for a C₃–C₄ intermediate grass which did not show noticeable differences in the distribution of the thylakoid complexes. For the NADP‐ME species Panicum antidotale, growth at glacial CO₂ (180 ppm of CO₂) had no effect on the distribution of the light‐reaction complexes, while growth at low light (200 μmol quanta m^?2 s^?1) promoted the accumulation of light‐harvesting proteins in both cell types. These results add to our understanding of thylakoid distribution across photosynthetic types and subtypes, and introduce thylakoid distribution between the MC and BSC of a C₃–C₄ intermediate species.     

Phylogenetic niche conservatism in C4 grasses

Photosynthetic pathway is used widely to discriminate plant functional types in studies of global change. However, independent evolutionary lineages of C₄ grasses with different variants of C₄ photosynthesis show different biogeographical relationships with mean annual precipitation, suggesting phylogenetic niche conservatism (PNC). To investigate how phylogeny and photosynthetic type differentiate C₄ grasses, we compiled a dataset of morphological and habitat information of 185 genera belonging to two monophyletic subfamilies, Chloridoideae and Panicoideae, which together account for 90 % of the world’s C₄ grass species. We evaluated evolutionary variance and covariance of morphological and habitat traits. Strong phylogenetic signals were found in both morphological and habitat traits, arising mainly from the divergence of the two subfamilies. Genera in Chloridoideae had significantly smaller culm heights, leaf widths, 1,000-seed weights and stomata; they also appeared more in dry, open or saline habitats than those of Panicoideae. Controlling for phylogenetic structure showed significant covariation among morphological traits, supporting the hypothesis of phylogenetically independent scaling effects. However, associations between morphological and habitat traits showed limited phylogenetic covariance. Subfamily was a better explanation than photosynthetic type for the variance in most morphological traits. Morphology, habitat water availability, shading, and productivity are therefore all involved in the PNC of C₄ grass lineages. This study emphasized the importance of phylogenetic history in the ecology and biogeography of C₄ grasses, suggesting that divergent lineages need to be considered to fully understand the impacts of global change on plant distributions.     

Field analysis of photoprotection in co‐occurring cool climate C3 and C4 grasses

C₄ photosynthesis is particularly successful at high light intensities and high temperatures, but is relatively rare when the average growing season temperature is less than about 15°C. We tested the hypothesis that rapidly reversible photoprotection enables some C₄ species to tolerate cool climates, by focusing on two questions: (1) Do chlorophyll fluorescence responses differ seasonally between co‐occurring C₃ and C₄ grasses in the field? (2) Does xanthophyll‐mediated photoprotection differ between the two pathways? Spartina pectinata (C₄) and Calamogrostis canadensis (C₃) were sampled in a herbaceous fresh‐water meadow in New Brunswick, Canada (45°N 66°W). Non‐photochemical thermal energy dissipation (Φ_NPQ) and the epoxidation state of the xanthophyll cycle (EPS) were used as indicators of photoprotection. We observed no differential susceptibility to chronic photoinhibition (i.e. photodamage) between the C₃ and C₄ species, except potentially during spring emergence. On average, C. canadensis showed higher levels of protective dynamic photoinhibition throughout the growing season, but S. pectinata had greater Φ_NPQ and lower EPS during seasonal and daily temperature minima. The low Rubisco capacity of C₄ species is a potential limiting factor to C₄ success at high latitudes, but our findings suggest that it is unlikely via a photoinhibitory feedback mechanism.     

Differential herbivory on C3 versus C4 grasses by the grasshopper Ageneotettix deorum (Orthoptera: acrididae)

Summary The hypothesis that graminivorous grasshoppers select C₃ grasses over C₄ grasses was tested with experiments in the field. It was found that the generalist, graminivorous grasshopper Ageneotettix deorum typically chooses C₃ as opposed to C₄ grasses when both types are equally available. This preference is attributed to the differences in leaf anatomies of C₃ and C₄ plants since crude protein, water, lignin, fiber, and silicon content or the size of the individual leaves tested do not explain the observed feeding pattern. However, examination of the actual food plant selection of actual field inhabiting grasshoppers indicates that food plant prefernce may only be a minor component of food selection in natural settings.     

Geographical and environmental distribution of C3 and C4 grasses in the Sinai,Negev, and Judean deserts

Summary The relation between photosynthetic pathway and habitat of the grass species recorded in the desert regions of Sinai, Negev, and Judea was investigated. The climatic conditions and micro-environments in the study area vary considerably, and the distribution of the various species is found to conform to specific patterns which reveal the adaptive advantages of the different photosynthetic pathways. There is also a distinct correlation between the phytogeographic origin of the grass species and the photosynthetic pathways that they utilize.The survey shows that the majority of the grass species in the region are of the C₃ type and all except one of these species belong to the Holarctic domain. This is in accordance with the fact that the region forms part of the Mediterranean winter rainfall regime and that C₃ species have an adaptive advantage where minimum temperatures are low during the winter growing season.The occurence of C₄ species increases with decreasing rainfall and they dominate in those districts where temperatures are high throughout the year. These C₄ grasses are of both Holarctic and Palaeotropic origin according to the classification adopted here, but they are essentially all elements of the Saharo-Arabian, Irano-Turanian, Sudanian, or Tropical phytogeographic regions and are not typical of the Mediterranean or Euro-Siberian floras. The plants with multi-regional distributions that occur in Mediterranean communities may well be intrusive.Analysis of the three subtypes of the C₄ species suggests that the malate-forming NADP-me grasses grow where water stress is not a dominating factor, while the aspartateforming NAD-me grasses are more successful under xeric conditions. The PEP-ck species are not abundant and form an intermediate group between the NADP-me and NAD-me subtypes.     

Climate, phylogeny and the ecological distribution of C4 grasses

'C4 photosynthesis' refers to a suite of traits that increase photosynthesis in high light and high temperature environments. Most C4 plants are grasses, which dominate tropical and subtropical grasslands and savannas but are conspicuously absent from cold growing season climates. Physiological attributes of C4 photosynthesis have been invoked to explain C4 grass biogeography; however, the pathway evolved exclusively in grass lineages of tropical origin, suggesting that the prevalence of C4 grasses in warm climates could be due to other traits inherited from their non-C4 ancestors. Here we investigate the relative influences of phylogeny and photosynthetic pathway in determining the ecological distributions of C4 grasses in Hawaii. We find that the restriction of C4 grasses to warmer areas is due largely to their evolutionary history as members of a warm-climate grass clade, but that the pathway does appear to confer a competitive advantage to grasses in more arid environments.     

Distribution of C3 and C4 grasses at different altitudes in a temperate arid region of Argentina

Summary The distribution of native C₃ and C₄ grasses in a temperate arid region of Mendoza, Argentina, was studied in six areas at different altitudes. C₄ species predominate at low elevations in both relative species abundance and plant cover. At high elevations C₃ species are dominant in cover and composition. At medium altitudes (1100–1600 m) grass species composition is balanced but plant cover of C₃ species is greater. Of 31 genera in the whole area, 19 were C₄. Only the genera Stipa (C₃) and Aristida (C₄) were present in all the six areas surveyed. The pattern of grass distribution shows high correlation with evapotranspiration and temperature parameters, but low correlation with rainfall. The relation between grass distribution and different climatic parameters is discussed.