The evolution of grasses using C4 photosynthesis and their sudden rise to ecological dominance 3 to 8 million years ago is among the most dramatic examples of biome assembly in the geological record. A growing body of work suggests that the patterns and drivers of C4 grassland expansion were considerably more complex than originally assumed. Previous research has benefited substantially from dialog between geologists and ecologists, but current research must now integrate fully with phylogenetics. A synthesis of grass evolutionary biology with grassland ecosystem science will further our knowledge of the evolution of traits that promote dominance in grassland systems and will provide a new context in which to evaluate the relative importance of C4 photosynthesis in transforming ecosystems across large regions of Earth.
The concentration of carbon dioxide in Earth's atmosphere may double by the end of the 21st century. The response of higher plants to a carbon dioxide doubling often includes a decline in their nitrogen status, but the reasons for this decline have been uncertain. We used five independent methods with wheat and Arabidopsis to show that atmospheric carbon dioxide enrichment inhibited the assimilation of nitrate into organic nitrogen compounds. This inhibition may be largely responsible for carbon dioxide acclimation, the decrease in photosynthesis and growth of plants conducting C(3) carbon fixation after long exposures (days to years) to carbon dioxide enrichment. These results suggest that the relative availability of soil ammonium and nitrate to most plants will become increasingly important in determining their productivity as well as their quality as food.
Biochemical models are used to predict and understand the response of photosynthesis to rising temperatures and CO2 partial pressures. These models require the temperature dependency of ribulose-1,5-bisphosphate carboxylase/ oxygenase (Rubisco) kinetics and mesophyll conductance to CO2 (gm). However, it is not known how the temperature response of Rubisco kinetics differs between species, and comprehensive in vivo Rubisco kinetics that include gm have only been determined in the warm-adapted Nicotiana tabacum. Here, we measured the temperature response of Rubisco kinetics and gm in N. tabacum and the cold-adapted Arabidopsis thaliana using gas exchange and 13 CO2 isotopic discrimination on plants with genetically reduced levels of Rubisco. While the individual Rubisco kinetic parameters in N. tabacum and A. thaliana were similar across temperatures, they collectively resulted in significantly different modelled rates of photosynthesis. Additionally, gm increased with temperature in N. tabacum but not in A. thaliana. These findings highlight the importance of considering speciesdependent differences in Rubisco kinetics and gm when modelling the temperature response of photosynthesis.
Photosynthetic carbon gain in plants using the C3 photosynthetic pathway is substantially inhibited by photorespiration in warm environments, particularly in atmospheres with low CO2 concentrations. Unlike C4 plants, C3 plants are thought to lack any mechanism to compensate for the loss of photosynthetic productivity caused by photorespiration. Here, for the first time, we demonstrate that the C3 plants rice and wheat employ a specific mechanism to trap and reassimilate photorespired CO2. A continuous layer of chloroplasts covering the portion of the mesophyll cell periphery that is exposed to the intercellular air space creates a diffusion barrier for CO2 exiting the cell. This facilitates the capture and reassimilation of photorespired CO2 in the chloroplast stroma. In both species, 24-38% of photorespired and respired CO2 were reassimilated within the cell, thereby boosting photosynthesis by 8-11% at ambient atmospheric CO2 concentration and 17-33% at a CO2 concentration of 200 mmol mol -1 . Widespread use of this mechanism in tropical and subtropical C3 plants could explain why the diversity of the world's C3 flora, and dominance of terrestrial net primary productivity, was maintained during the Pleistocene, when atmospheric CO2 concentrations fell below 200 mmol mol -1 .
Photorespiration, a process that diminishes net photosynthesis by Ϸ25% in most plants, has been viewed as the unfavorable consequence of plants having evolved when the atmosphere contained much higher levels of carbon dioxide than it does today. Here we used two independent methods to show that exposure of Arabidopsis and wheat shoots to conditions that inhibited photorespiration also strongly inhibited nitrate assimilation. Thus, nitrate assimilation in both dicotyledonous and monocotyledonous species depends on photorespiration. This previously undescribed role for photorespiration (i) explains several responses of plants to rising carbon dioxide concentrations, including the inability of many plants to sustain rapid growth under elevated levels of carbon dioxide; and (ii) raises concerns about genetic manipulations to diminish photorespiration in crops.global climate change ͉ CO2 acclimation ͉ Arabidopsis ͉ wheat R ubisco, the most prevalent protein in plants, indeed in the biosphere, catalyzes the reaction of ribulose-1,5-bisphosphate with either CO 2 or O 2 and thereby initiates, respectively, the CO 2 assimilatory (C 3 reductive) or photorespiratory (C 2 oxidative) pathways. The balance between the two reactions depends on the relative concentrations of CO 2 and O 2 at the site of catalysis. At current atmospheric levels of CO 2 (Ϸ360 mol⅐mol Ϫ1 ) and O 2 (Ϸ209,700 mol⅐mol Ϫ1 ), photorespiration in C 3 plants dissipates Ͼ25% of the carbon fixed during CO 2 assimilation (1). Thus, photorespiration has been viewed as a wasteful process, a vestige of the high CO 2 atmospheres under which plants evolved (2). At best, according to current thought, photorespiration may mitigate photoinhibition under high light and drought stress (2, 3) or may generate amino acids such as glycine for other metabolic pathways (4). Genetic modification of Rubisco to minimize photorespiration in crop plants has been the goal of many investigations (5).Atmospheric CO 2 concentrations will rise to somewhere between 600 and 1,000 mol⅐mol Ϫ1 by the end of the 21st century (6). Transferring C 3 plants from ambient (Ϸ360 mol⅐mol Ϫ1 ) to elevated (Ϸ720 mol⅐mol Ϫ1 ) CO 2 concentrations decreases photorespiration and initially stimulates net CO 2 assimilation and growth by Ϸ30% (7). With longer exposures to elevated CO 2 concentrations (days to weeks), however, net CO 2 assimilation and plant growth slow down until they stabilize at rates that average 12% (8) and 8% (9), respectively, above those of plants kept at ambient CO 2 concentrations. This phenomenon, known as CO 2 acclimation, is often associated with diminished activities of Rubisco and other enzymes in the C 3 reductive photosynthetic carbon cycle (10, 11), but the influence of elevated CO 2 may not be specific to these enzymes (12). Rather, CO 2 acclimation follows a 14% decline in overall shoot nitrogen concentrations (13), a change nearly double what would be expected if a given amount of nitrogen were diluted by the additional biomass that accumulates under elevated CO 2 conce...
The genus Oryza, which includes rice (Oryza sativa and Oryza glaberrima) and wild relatives, is a useful genus to study leaf properties in order to identify structural features that control CO 2 access to chloroplasts, photosynthesis, water use efficiency, and drought tolerance. Traits, 26 structural and 17 functional, associated with photosynthesis and transpiration were quantified on 24 accessions (representatives of 17 species and eight genomes). Hypotheses of associations within, and between, structure, photosynthesis, and transpiration were tested. Two main clusters of positively interrelated leaf traits were identified: in the first cluster were structural features, leaf thickness (Thick leaf ), mesophyll (M) cell surface area exposed to intercellular air space per unit of leaf surface area (S mes ), and M cell size; a second group included functional traits, net photosynthetic rate, transpiration rate, M conductance to CO 2 diffusion (g m ), stomatal conductance to gas diffusion (g s ), and the g m /g s ratio. While net photosynthetic rate was positively correlated with g m , neither was significantly linked with any individual structural traits. The results suggest that changes in g m depend on covariations of multiple leaf (S mes ) and M cell (including cell wall thickness) structural traits. There was an inverse relationship between Thick leaf and transpiration rate and a significant positive association between Thick leaf and leaf transpiration efficiency. Interestingly, high g m together with high g m /g s and a low S mes /g m ratio (M resistance to CO 2 diffusion per unit of cell surface area exposed to intercellular air space) appear to be ideal for supporting leaf photosynthesis while preserving water; in addition, thick M cell walls may be beneficial for plant drought tolerance.
ORCID IDs: 0000-0003-4009-7700 (R.A.B.); 0000-0001-7184-5113 (A.G.).The photosynthetic assimilation of CO 2 in C 4 plants is potentially limited by the enzymatic rates of Rubisco, phosphoenolpyruvate carboxylase (PEPc), and carbonic anhydrase (CA). Therefore, the activity and kinetic properties of these enzymes are needed to accurately parameterize C 4 biochemical models of leaf CO 2 exchange in response to changes in CO 2 availability and temperature. There are currently no published temperature responses of both Rubisco carboxylation and oxygenation kinetics from a C 4 plant, nor are there known measurements of the temperature dependency of the PEPc Michaelis-Menten constant for its substrate HCO 3 2 , and there is little information on the temperature response of plant CA activity. Here, we used membrane inlet mass spectrometry to measure the temperature responses of Rubisco carboxylation and oxygenation kinetics, PEPc carboxylation kinetics, and the activity and first-order rate constant for the CA hydration reaction from 10°C to 40°C using crude leaf extracts from the C 4 plant Setaria viridis. The temperature dependencies of Rubisco, PEPc, and CA kinetic parameters are provided. These findings describe a new method for the investigation of PEPc kinetics, suggest an HCO 3 2 limitation imposed by CA, and show similarities between the Rubisco temperature responses of previously measured C 3 species and the C 4 plant S. viridis.
Mesophyll conductance (g ) is an important factor limiting rates of C photosynthesis. However, its role in C photosynthesis is poorly understood because it has been historically difficult to estimate. We use two methods to derive the temperature responses of g in C species. The first (Δ O) combines measurements of gas exchange with models and measurements of O discrimination. The second method (in vitro V ) derives g by retrofitting models of C photosynthesis and C discrimination with gas exchange, kinetic constants and in vitro V measurements. The two methods produced similar g for Setaria viridis and Zea mays. Additionally, we present the first temperature response (10-40°C) of C g in S. viridis, Z. mays and Miscanthus × giganteus. Values for g at 25°C ranged from 2.90 to 7.85 μmol m s Pa . Our study demonstrated that: the two described methods are suitable to calculate g in C species; g values in C are similar to high-end values reported for C species; and g increases with temperature analogous to reports for C species and the response is species specific. These results improve our mechanistic understanding of C photosynthesis.
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