Response of photosynthesis, growth and water relations of a savannah-adapted tree and grass grown across high to low CO2.

BACKGROUND AND AIMS: By the year 2100, atmospheric CO2 concentration ([CO2]a) could reach 800 ppm, having risen from ~200 ppm since the Neogene, beginning ~24 Myr ago. Changing [CO2]a affects plant carbon-water balance, with implications for growth, drought tolerance and vegetation shifts. The evolution of C4 photosynthesis improved plant hydraulic function under low [CO2]a and preluded the establishment of savannahs, characterized by rapid transitions between open C4-dominated grassland with scattered trees and closed forest. Understanding directional vegetation trends in response to environmental change will require modelling. But models are often parameterized with characteristics observed in plants under current climatic conditions, necessitating experimental quantification of the mechanistic underpinnings of plant acclimation to [CO2]a. METHODS: We measured growth, photosynthesis and plant-water relations, within wetting-drying cycles, of a C3 tree (Vachellia karroo, an acacia) and a C4 grass (Eragrostis curvula) grown at 200, 400 or 800 ppm [CO2]a. We investigated the mechanistic linkages between trait responses to [CO2]a under moderate soil drying, and photosynthetic characteristics. KEY RESULTS: For V. karroo, higher [CO2]a increased assimilation, foliar carbon:nitrogen, biomass and leaf starch, but decreased stomatal conductance and root starch. For Eragrostis, higher [CO2]a decreased C:N, did not affect assimilation, biomass or starch, and markedly decreased stomatal conductance. Together, this meant that C4 advantages in efficient water-use over the tree were maintained with rising [CO2]a. CONCLUSIONS: Acacia and Eragrostis acclimated differently to [CO2]a, with implications for their respective responses to water limitation and environmental change. Our findings question the carbon-centric focus on factors limiting assimilation with changing [CO2]a, how they are predicted and their role in determining productivity. We emphasize the continuing importance of water-conserving strategies in the assimilation response of savannah plants to rising [CO2]a.

A Dynamic Hydro-Mechanical and Biochemical Model of Stomatal Conductance for C4 Photosynthesis.

C4 plants are major grain (maize [Zea mays] and sorghum [Sorghum bicolor]), sugar (sugarcane [Saccharum officinarum]), and biofuel (Miscanthus spp.) 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 hydromechanical model of stomatal behavior 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 behavior could be accounted for by fitting a single parameter. The model accurately predicted steady-state responses of gS to light, atmospheric CO2 and oxygen, soil drying, and evaporative demand as well as dynamic responses to light intensity. Further analyses suggest that 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 that the hydraulic benefits associated with fast stomatal responses of C4 grasses may have supported the evolution of C4 photosynthesis.

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 liverworts­an extant lineage of early land plants­partnering 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.

Ectomycorrhizal fungi and past high CO2 atmospheres enhance mineral weathering through increased below-ground carbon-energy fluxes.

Field studies indicate an intensification of mineral weathering with advancement from arbuscular mycorrhizal (AM) to later-evolving ectomycorrhizal (EM) fungal partners of gymnosperm and angiosperm trees. We test the hypothesis that this intensification is driven by increasing photosynthate carbon allocation to mycorrhizal mycelial networks using 14CO2-tracer experiments with representative tree­fungus mycorrhizal partnerships. Trees were grown in either a simulated past CO2 atmosphere (1500 ppm)­under which EM fungi evolved­or near-current CO2 (450 ppm). We report a direct linkage between photosynthate-energy fluxes from trees to EM and AM mycorrhizal mycelium and rates of calcium silicate weathering. Calcium dissolution rates halved for both AM and EM trees as CO2 fell from 1500 to 450 ppm, but silicate weathering by AM trees at high CO2 approached rates for EM trees at near-current CO2. Our findings provide mechanistic insights into the involvement of EM-associating forest trees in strengthening biological feedbacks on the geochemical carbon cycle that regulate atmospheric CO2 over millions of years.

Increased susceptibility to drought-induced mortality in Sequoia sempervirens (Cupressaceae) trees under Cenozoic atmospheric carbon dioxide starvation.

PREMISE OF THE STUDY: Climate-induced forest retreat has profound ecological and biogeochemical impacts, but the physiological mechanisms underlying past tree mortality are poorly understood, limiting prediction of vegetation shifts with climate variation. Climate, drought, fire, and grazing represent agents of tree mortality during the late Cenozoic, but the interaction between drought and declining atmospheric carbon dioxide ([CO2]a) from high to near-starvation levels ∼34 million years (Ma) ago has been overlooked. Here, this interaction frames our investigation of sapling mortality through the interdependence of hydraulic function, carbon limitation, and defense metabolism. • METHODS: We recreated a changing Cenozoic [CO2]a regime by growing Sequoia sempervirens trees within climate-controlled growth chambers at 1500, 500, or 200 ppm [CO2]a, capturing the decline toward minimum concentrations from 34 Ma. After 7 months, we imposed drought conditions and measured key physiological components linking carbon utilization, hydraulics, and defense metabolism as hypothesized interdependent mechanisms of tree mortality. • KEY RESULTS: Catastrophic failure of hydraulic conductivity, carbohydrate starvation, and tree death occurred at 200 ppm, but not 500 or 1500 ppm [CO2]a. Furthermore, declining [CO2]a reduced investment in carbon-rich foliar defense compounds that would diminish resistance to biotic attack, likely exacerbating mortality. • CONCLUSIONS: Low-[CO2]a-driven tree mortality under drought is consistent with Pleistocene pollen records charting repeated Californian Sequoia forest contraction during glacial periods (180-200 ppm [CO2]a) and may even have contributed to forest retreat as grasslands expanded on multiple continents under low [CO2]a over the past 10 Ma. In this way, geologic intervals of low [CO2]a coupled with drought could impose a demographic bottleneck in tree recruitment, driving vegetation shifts through forest mortality.

Evolution of trees and mycorrhizal fungi intensifies silicate mineral weathering.

Forested ecosystems diversified more than 350 Ma to become major engines of continental silicate weathering, regulating the Earth's atmospheric carbon dioxide concentration by driving calcium export into ocean carbonates. Our field experiments with mature trees demonstrate intensification of this weathering engine as tree lineages diversified in concert with their symbiotic mycorrhizal fungi. Preferential hyphal colonization of the calcium silicate-bearing rock, basalt, progressively increased with advancement from arbuscular mycorrhizal (AM) to later, independently evolved ectomycorrhizal (EM) fungi, and from gymnosperm to angiosperm hosts with both fungal groups. This led to 'trenching' of silicate mineral surfaces by AM and EM fungi, with EM gymnosperms and angiosperms releasing calcium from basalt at twice the rate of AM gymnosperms. Our findings indicate mycorrhiza-driven weathering may have originated hundreds of millions of years earlier than previously recognized and subsequently intensified with the evolution of trees and mycorrhizas to affect the Earth's long-term CO(2) and climate history.

Physiological responses to low CO2 over prolonged drought as primers for forest-grassland transitions.

Savannahs dominated by grasses with scattered C3 trees expanded between 24 and 9 million years ago in low latitudes at the expense of forests. Fire, herbivory, drought and the susceptibility of trees to declining atmospheric CO2 concentrations ([CO2]a) are proposed as key drivers of this transition. The role of disturbance is well studied, but physiological arguments are mostly derived from models and palaeorecords, without direct experimental evidence. In replicated comparative experimental trials, we examined the physiological effects of [CO2]a and prolonged drought in a broadleaf forest tree, a savannah tree and a savannah C4 grass. We show that the forest tree was more disadvantaged than either the savannah tree or the C4 grass by the low [CO2]a and increasing aridity. Our experiments provide insights into the role of the intrinsic physiological susceptibility of trees in priming the disturbance-driven transition from forest to savannah in the conditions of the early Miocene.

Stomatal and non-stomatal limitations in savanna trees and C4 grasses grown at low, ambient and high atmospheric CO2.

By the end of the century, atmospheric CO2 concentration ([CO2]a) could reach 800 ppm, having risen from ∼200 ppm ∼24 Myr ago. Carbon dioxide enters plant leaves through stomata that limit CO2 diffusion and assimilation, imposing stomatal limitation (LS). Other factors limiting assimilation are collectively called non-stomatal limitations (LNS). C4 photosynthesis concentrates CO2 around Rubisco, typically reducing LS. C4-dominated savanna grasslands expanded under low [CO2]a and are metastable ecosystems where the response of trees and C4 grasses to rising [CO2]a will determine shifting vegetation patterns. How LS and LNS differ between savanna trees and C4 grasses under different [CO2]a will govern the responses of CO2 fixation and plant cover to [CO2]a - but quantitative comparisons are lacking. We measured assimilation, within soil wetting-drying cycles, of three C3 trees and three C4 grasses grown at 200, 400 or 800 ppm [CO2]a. Using assimilation-response curves, we resolved LS and LNS and show that rising [CO2]a alleviated LS, particularly for the C3 trees, but LNS was unaffected and remained substantially higher for the grasses across all [CO2]a treatments. Because LNS incurs higher metabolic costs and recovery compared with LS, our findings indicate that C4 grasses will be comparatively disadvantaged as [CO2]a rises.

A multi-species synthesis of physiological mechanisms in drought-induced tree mortality.

Widespread tree mortality associated with drought has been observed on all forested continents and global change is expected to exacerbate vegetation vulnerability. Forest mortality has implications for future biosphere-atmosphere interactions of carbon, water and energy balance, and is poorly represented in dynamic vegetation models. Reducing uncertainty requires improved mortality projections founded on robust physiological processes. However, the proposed mechanisms of drought-induced mortality, including hydraulic failure and carbon starvation, are unresolved. A growing number of empirical studies have investigated these mechanisms, but data have not been consistently analysed across species and biomes using a standardized physiological framework. Here, we show that xylem hydraulic failure was ubiquitous across multiple tree taxa at drought-induced mortality. All species assessed had 60% or higher loss of xylem hydraulic conductivity, consistent with proposed theoretical and modelled survival thresholds. We found diverse responses in non-structural carbohydrate reserves at mortality, indicating that evidence supporting carbon starvation was not universal. Reduced non-structural carbohydrates were more common for gymnosperms than angiosperms, associated with xylem hydraulic vulnerability, and may have a role in reducing hydraulic function. Our finding that hydraulic failure at drought-induced mortality was persistent across species indicates that substantial improvement in vegetation modelling can be achieved using thresholds in hydraulic function.