The Penalty of a Long, Hot Summer. Photosynthetic Acclimation to High CO2 and Continuous Light in “Living Fossil” Conifers

Deciduous forests covered the ice-free polar regions 280 to 40 million years ago under warm “greenhouse” climates and high atmospheric pCO2. Their deciduous habit is frequently interpreted as an adaptation for minimizing carbon losses during winter, but experiments with “living fossils” in a simulated warm polar environment refute this explanation. Measured carbon losses through leaf abscission of deciduous trees are significantly greater than losses through winter respiration in evergreens, yet annual rates of primary productivity are similar in all species. Here, we investigate mechanisms underlying this apparent paradox by measuring the seasonal patterns of leaf photosynthesis (A) under pCO2 enrichment in the same trees. During spring, A increased significantly in coastal redwood (Sequoia sempervirens), dawn redwood (Metasequoia glyptostroboides), and swamp cypress (Taxodium distichum) at an elevated pCO2 of 80 Pa compared with controls at 40 Pa. However, strong acclimation in Rubisco carboxylation capacity (Vc,max) completely offset the CO2 response of A in all species by the end of 6 weeks of continuous illumination in the simulated polar summer. Further measurements demonstrated the temporary nature of acclimation, with increases in Vc,max during autumn restoring the CO2 sensitivity of A. Contrary to expectations, the acclimation of Vc,max was not always accompanied by accumulation of leaf carbohydrates, but was associated with a decline in leaf nitrogen in summer, suggesting an alteration of the balance in plant sources and sinks for carbon and nitrogen. Preliminary calculations using A indicated that winter carbon losses through deciduous leaf abscission and respiration were recovered by 10 to 25 d of canopy carbon fixation during summer, thereby explaining the productivity paradox

Carbon loss by deciduous trees in a CO2-rich ancient polar environment

Fossils demonstrate that deciduous forests covered the polar regions for much of the past 250 million years 1 when the climate was warm and atmospheric CO2 high 2. But the evolutionary significance of their deciduous character has remained a matter of conjecture for almost a century 3. The leading hypothesis 1,4-7 argues that it was an adaptation to photoperiod, allowing the avoidance of carbon losses by respiration from a canopy of leaves unable to photosynthesize in the darkness of warm polar winters 8-11. Here we test this proposal with experiments using 'living fossil' tree species grown in a simulated polar climate with and without CO2 enrichment. We show that the quantity of carbon lost annually by shedding a deciduous canopy is significantly greater than that lost by evergreen trees through wintertime respiration and leaf litter production, irrespective of growth CO2 concentration. Scaling up our experimental observations indicates that the greater expense of being deciduous persists in mature forests, even up to latitudes of 83 [degrees]N, where the duration of the polar winter exceeds five months. We therefore reject the carbon-loss hypothesis as an explanation for the deciduous nature of polar forests

A dynamic hydro-mechanical and biochemical model of stomatal conductance for C4 photosynthesis

C4 plants are major grain (maize, sorghum), sugar (sugarcane) and biofuel (Miscanthus) producers, and contribute ~20% to global productivity. Plants lose water through stomatal pores in order to acquire CO2 (assimilation, A), and control their carbon-for-water balance by regulating stomatal conductance (gS). The ability to mechanistically predict gS and A in response to atmospheric CO2, water availability and time is critical for simulating stomatal control of plant-atmospheric carbon and water exchange under current, past or future environmental conditions. Yet, dynamic mechanistic models for gS are lacking, especially for C4 photosynthesis. We developed and coupled a hydro-mechanical model of stomatal behaviour with a biochemical model of C4 photosynthesis, calibrated using gas exchange measurements in maize, and extended the coupled model with time- explicit functions to predict dynamic responses. We demonstrated the wider applicability of the model with three additional C4 grass species in which interspecific differences in stomatal behaviour could be accounted for by fitting a single parameter. The model accurately predicted steady-state responses of gS to light, atmospheric CO2 and O2, soil drying and evaporative demand, as well as dynamic responses to light intensity. Further analyses suggest the effect of variable leaf hydraulic conductance is negligible. Based on the model, we derived a set of equations suitable for incorporation in land surface models. Our model illuminates the processes underpinning stomatal control in C4 plants and suggests the hydraulic benefits associated with fast stomatal responses of C4 grasses may have supported the evolution of C4 photosynthesis

An Excel tool for deriving key photosynthetic parameters from combined gas exchange and chlorophyll fluorescence: theory and practice.

Combined photosynthetic gas exchange and modulated fluorometres are widely used to evaluate physiological characteristics associated with phenotypic and genotypic variation, whether in response to genetic manipulation or resource limitation in natural vegetation or crops. After describing relatively simple experimental procedures, we present the theoretical background to the derivation of photosynthetic parameters, and provide a freely available Excel-based fitting tool (EFT) that will be of use to specialists and non-specialists alike. We use data acquired in concurrent variable fluorescence-gas exchange experiments, where A/Ci and light-response curves have been measured under ambient and low oxygen. From these data, the EFT derives light respiration, initial PSII (photosystem II) photochemical yield, initial quantum yield for CO2 fixation, fraction of incident light harvested by PSII, initial quantum yield for electron transport, electron transport rate, rate of photorespiration, stomatal limitation, Rubisco (ribulose 1·5-bisphosphate carboxylase/oxygenase) rate of carboxylation and oxygenation, Rubisco specificity factor, mesophyll conductance to CO2 diffusion, light and CO2 compensation point, Rubisco apparent Michaelis-Menten constant, and Rubisco CO2 -saturated carboxylation rate. As an example, a complete analysis of gas exchange data on tobacco plants is provided. We also discuss potential measurement problems and pitfalls, and suggest how such empirical data could subsequently be used to parameterize predictive photosynthetic models

Phylogenomics indicates the “living fossil” Isoetes diversified in the Cenozoic

The fossil record provides an invaluable insight into the temporal origins of extant lineages of organisms. However, establishing the relationships between fossils and extant lineages can be difficult in groups with low rates of morphological change over time. Molecular dating can potentially circumvent this issue by allowing distant fossils to act as calibration points, but rate variation across large evolutionary scales can bias such analyses. In this study, we apply multiple dating methods to genome-wide datasets to infer the origin of extant species of Isoetes, a group of mostly aquatic and semi-aquatic isoetalean lycopsids, which closely resemble fossil forms dating back to the Triassic. Rate variation observed in chloroplast genomes hampers accurate dating, but genome-wide nuclear markers place the origin of extant diversity within this group in the mid-Paleogene, 45–60 million years ago. Our genomic analyses coupled with a careful evaluation of the fossil record indicate that despite resembling forms from the Triassic, extant Isoetes species do not represent the remnants of an ancient and widespread group, but instead have spread around the globe in the relatively recent past

Constraining the role of early land plants in Palaeozoic weathering and global cooling

How the colonization of terrestrial environments by early land plants over 400 Ma influenced rock weathering, the biogeochemical cycling of carbon and phosphorus, and climate in the Palaeozoic is uncertain. Here we show experimentally that mineral weathering by liverworts—an extant lineage of early land plants—partnering arbuscular mycorrhizal (AM) fungi, like those in 410 Ma-old early land plant fossils, amplified calcium weathering from basalt grains threefold to sevenfold, relative to plant-free controls. Phosphate weathering by mycorrhizal liverworts was amplified 9–13-fold over plant-free controls, compared with fivefold to sevenfold amplification by liverworts lacking fungal symbionts. Etching and trenching of phyllosilicate minerals increased with AM fungal network size and atmospheric CO2 concentration. Integration of grain-scale weathering rates over the depths of liverwort rhizoids and mycelia (0.1 m), or tree roots and mycelia (0.75 m), indicate early land plants with shallow anchorage systems were probably at least 10-fold less effective at enhancing the total weathering flux than later-evolving trees. This work challenges the suggestion that early land plants significantly enhanced total weathering and land-to-ocean fluxes of calcium and phosphorus, which have been proposed as a trigger for transient dramatic atmospheric CO2 sequestration and glaciations in the Ordovician

Phosphate availability and ectomycorrhizal symbiosis with Pinus sylvestris have independent effects on the Paxillus involutus transcriptome

Many plant species form symbioses with ectomycorrhizal fungi, which help them forage for limiting nutrients in the soil such as inorganic phosphate (Pi). The transcriptional responses to symbiosis and nutrient-limiting conditions in ectomycorrhizal fungal hyphae, however, are largely unknown. An artificial system was developed to study ectomycorrhizal basidiomycete Paxillus involutus growth in symbiosis with its host tree Pinus sylvestris at different Pi concentrations. RNA-seq analysis was performed on P. involutus hyphae growing under Pi-limiting conditions, either in symbiosis or alone. We show that Pi starvation and ectomycorrhizal symbiosis have an independent effect on the P. involutus transcriptome. Notably, low Pi availability induces expression of newly identified putative high-affinity Pi transporter genes, while reducing the expression of putative organic acid transporters. Additionally, low Pi availability induces a close transcriptional interplay between P and N metabolism. GTP-related signalling was found to have a positive effect in the maintenance of ectomycorrhizal symbiosis, whereas multiple putative cytochrome P450 genes were found to be downregulated, unlike arbuscular mycorrhizal fungi. We provide the first evidence of global transcriptional changes induced by low Pi availability and ectomycorrhizal symbiosis in the hyphae of P. involutus, revealing both similarities and differences with better-characterized arbuscular mycorrhizal fungi

C4 savanna grasses fail to maintain assimilation in drying soil under low CO2 compared with C3 trees despite lower leaf water demand

1.C4 photosynthesis evolved when grasses migrated out of contracting forests under a declining atmospheric CO2 concentration ([CO2]a) and drying climate around 30 million years ago. C4 grasses are hypothesised to benefit from improved plant–water relations in open habitats like savannas, giving advantages over C3 plants under low [CO2]a. But experimental evidence in a low CO2 environment is limited and comparisons with C3 trees are needed to understand savanna vegetation patterns. 2.To test whether stomatal conductance (gS) and CO2 assimilation (A) are maintained in drier soil for C4 grasses than C3 trees, particularly under low [CO2]a, we investigated photosynthesis and plant–water relations of three C3 tree and three C4 grass species grown at 800, 400 or 200 ppm [CO2]a over moderate wetting–drying cycles. 3.C4 grasses had a lower soil–to–leaf water potential gradient than C3 trees, especially at 200 ppm [CO2]a, indicating reduced leaf water demand relative to supply. Yet the dependence of gS and A on predawn leaf water potential (a measure of soil water availability) was greater for the C4 grasses than trees, particularly under low [CO2]a. 4.Our findings establish that gS and A are not maintained in drier soil for C4 grasses compared with C3 trees, suggesting that this mechanism was not prevailing in the expansion of C4–dominated grasslands under low [CO2]a. This inherent susceptibility to sudden decreases in soil water availability justifies why C4 grasses have not evolved a resistant xylem allowing operation under drought, but instead shut down below a water potential threshold and rapidly recover. We point to this capacity to respond to transient water availability as a key overlooked driver of C4 grass success under low [CO2]a

Impact of negative and positive CO2 emissions on global warming metrics using an ensemble of Earth system model simulations

The benefits of implementing negative emission technologies in the global warming response to cumulative carbon emissions until the year 2420 are assessed following the shared socioeconomic pathway (SSP) 1-2.6, the sustainable development scenario, with a comprehensive set of intermediate-complexity Earth system model integrations. Model integrations include 86 different model realisations covering a wide range of plausible climate states. The global warming response is assessed in terms of two key climate metrics: the effective transient climate response to cumulative CO2 emissions (eTCRE), measuring the surface warming response to cumulative carbon emissions and associated non-CO2 forcing, and the effective zero emissions commitment (eZEC), measuring the extent of any continued warming after net-zero CO2 emissions are reached. The transient climate response to cumulative CO2 emissions (TCRE) is estimated as 2.2 K EgC−1 (median value) with a 10 %–90 % range of 1.75 to 3.13 K EgC−1 in 2100, approximated from the eTCRE by removing the contribution of non-CO2 forcing. During the positive emission phase, the eTCRE decreases from 2.71 (2.0 to 3.65) to 2.61 (1.91 to 3.62) K EgC−1 due to a weakening in the dependence of radiative forcing on atmospheric carbon, which is partly opposed by an increasing fraction of the radiative forcing warming the surface as the ocean stratifies. During the net negative and zero emission phases, a progressive reduction in the eTCRE to 2.0 (1.39 to 2.96) K EgC−1 is driven by the reducing airborne fraction as atmospheric CO2 is drawn down mainly by the ocean. The model uncertainty in the slopes of warming versus cumulative CO2 emissions varies from being controlled by the radiative feedback parameter during positive emissions to being affected by carbon-cycle parameters during net negative emissions, consistent with the drivers of uncertainty diagnosed from the coefficient of variation of the contributions in the eTCRE framework. The continued warming after CO2 emissions cease and remain at zero gives a model mean eZEC of −0.03 K after 25 years, which decreases in time to −0.21 K at 90 years after emissions cease. However, there is a spread in the ensemble with a temperature overshoot occurring in 20 % of the ensemble members at 25 years after cessation of emissions. If net negative emissions are included, there is a reduction in atmospheric CO2 and there is a decrease in temperature overshoot so that the eZEC is positive in only 5 % of the ensemble members. Hence, incorporating negative emissions enhances the ability to meet climate targets and avoid risk of continued warming after net zero is reached