Mountain grasslands have recently been exposed to substantial changes in land use and climate and in the near future will likely face an increased frequency of extreme droughts. To date, how the drought responses of carbon (C) allocation, a key process in the C cycle, are affected by land‐use changes in mountain grassland is not known.We performed an experimental summer drought on an abandoned grassland and a traditionally managed hay meadow and traced the fate of recent assimilates through the plant–soil continuum. We applied two 13 CO 2 pulses, at peak drought and in the recovery phase shortly after rewetting.Drought decreased total C uptake in both grassland types and led to a loss of above‐ground carbohydrate storage pools. The below‐ground C allocation to root sucrose was enhanced by drought, especially in the meadow, which also held larger root carbohydrate storage pools.The microbial community of the abandoned grassland comprised more saprotrophic fungal and Gram(+) bacterial markers compared to the meadow. Drought increased the newly introduced AM and saprotrophic (A+S) fungi:bacteria ratio in both grassland types. At peak drought, the 13C transfer into AM and saprotrophic fungi, and Gram(−) bacteria was more strongly reduced in the meadow than in the abandoned grassland, which contrasted the patterns of the root carbohydrate pools.In both grassland types, the C allocation largely recovered after rewetting. Slowest recovery was found for AM fungi and their 13C uptake. In contrast, all bacterial markers quickly recovered C uptake. In the meadow, where plant nitrate uptake was enhanced after drought, C uptake was even higher than in control plots. Synthesis. Our results suggest that resistance and resilience (i.e. recovery) of plant C dynamics and plant‐microbial interactions are negatively related, that is, high resistance is followed by slow recovery and vice versa. The abandoned grassland was more resistant to drought than the meadow and possibly had a stronger link to AM fungi that could have provided better access to water through the hyphal network. In contrast, meadow communities strongly reduced C allocation to storage and C transfer to the microbial community in the drought phase, but in the recovery phase invested C resources in the bacterial communities to gain more nutrients for regrowth. We conclude that the management of mountain grasslands increases their resilience to drought.
Extreme climatic events (ECEs) such as droughts and heat waves are predicted to increase in intensity and frequency and impact the terrestrial carbon balance. However, we lack direct experimental evidence of how the net carbon uptake of ecosystems is affected by ECEs under future elevated atmospheric CO 2 concentrations (eCO 2 ). Taking advantage of an advanced controlled environment facility for ecosystem research (Ecotron), we simulated eCO 2 and extreme cooccurring heat and drought events as projected for the 2050s and analyzed their effects on the ecosystem-level carbon and water fluxes in a C3 grassland. Our results indicate that eCO 2 not only slows down the decline of ecosystem carbon uptake during the ECE but also enhances its recovery after the ECE, as mediated by increases of root growth and plant nitrogen uptake induced by the ECE. These findings indicate that, in the predicted near future climate, eCO 2 could mitigate the effects of extreme droughts and heat waves on ecosystem net carbon uptake.climate change | extreme events | elevated CO 2 | carbon fluxes | grassland ecosystem I ncreased aridity and heat waves are projected to increase in the 21st century for most of Africa, southern and central Europe, the Middle East, and parts of the Americas, Australia, and southeast Asia (1-3). These regions have a large fraction of their land covered by grasslands and rangelands, a biome covering approximately one-quarter of the Earth's land area and contributing to the livelihoods of more than 800 million people (4). There is mounting evidence that extreme climatic events (ECEs) may significantly affect the regional and global carbon (C) fluxes (3, 5-9) and potentially feed back on atmospheric CO 2 concentrations and the climate system (7). However, our knowledge concerning the outcome of the interaction between future ECEs and elevated atmospheric CO 2 concentrations (eCO 2 ) for ecosystem C stocks is equivocal (10-12). Studies focusing on plant physiological responses have shown that eCO 2 has the potential to mitigate future drought-related stress on plant growth by reducing stomatal conductance, thereby increasing water use efficiency (WUE) (13-15) and preserving soil moisture (16)(17)(18). However, to date, little is known on whether and how eCO 2 alters the consequences of ECEs for ecosystem net C uptake. Because the capacity of ecosystems to act as a C sink depends on the relative effects of eCO 2 , ECE, and their potential interaction on both plant and soil processes, an integrated assessment of all C fluxes during and after the ECEs is important if we are to estimate the overall C balance.Using the Montpellier CNRS Ecotron facility (www.ecotron. cnrs.fr), we tested with 12 large controlled environment units (macrocosms, SI Appendix, Fig. S1) whether (i) an ECE (severe drought and heat wave) predicted for the 2050s reduces ecosystem net C uptake by reducing ecosystem photosynthesis relative to ecosystem respiration (R eco ), (ii) eCO 2 buffers the negative effects of the ECE on ecosystem CO 2 fluxes ...
Terrestrial vegetation currently absorbs approximately a third of anthropogenic CO 2 emissions, mitigating the rise of atmospheric CO 2 . However, terrestrial net primary production is highly sensitive to atmospheric CO 2 levels and associated climatic changes. In C 3 plants, which dominate terrestrial vegetation, net photosynthesis depends on the ratio between photorespiration and gross photosynthesis. This metabolic flux ratio depends strongly on CO 2 levels, but changes in this ratio over the past CO 2 rise have not been analyzed experimentally. Combining CO 2 manipulation experiments and deuterium NMR, we first establish that the intramolecular deuterium distribution (deuterium isotopomers) of photosynthetic C 3 glucose contains a signal of the photorespiration/photosynthesis ratio. By tracing this isotopomer signal in herbarium samples of natural C 3 vascular plant species, crops, and a Sphagnum moss species, we detect a consistent reduction in the photorespiration/photosynthesis ratio in response to the ∼100-ppm CO 2 increase between ∼1900 and 2013. No difference was detected in the isotopomer trends between beet sugar samples covering the 20th century and CO 2 manipulation experiments, suggesting that photosynthetic metabolism in sugar beet has not acclimated to increasing CO 2 over >100 y. This provides observational evidence that the reduction of the photorespiration/photosynthesis ratio was ca. 25%. The Sphagnum results are consistent with the observed positive correlations between peat accumulation rates and photosynthetic rates over the Northern Hemisphere. Our results establish that isotopomers of plant archives contain metabolic information covering centuries. Our data provide direct quantitative information on the "CO 2 fertilization" effect over decades, thus addressing a major uncertainty in Earth system models.A tmospheric CO 2 levels have increased from ∼200 ppm during the last ice age to currently 400 ppm, and they may, according to pessimistic scenarios, exceed 1,000 ppm in the year 2100 (1). Understanding plant responses to increasing CO 2 is currently hampered by two fundamental limitations: First, it is unknown how well manipulation experiments represent responses to the gradual CO 2 increase over decades and centuries. In Free-Air CO 2 Enrichment (FACE) experiments, which most closely mimic natural conditions, increases in [CO 2 ] generally increase plant growth, but this "CO 2 fertilization" effect often declines after a few years of enrichment (2). Such transient responses may be related to the step increases in [CO 2 ] used in the experiments, their limited duration (2), or factors other than CO 2 becoming limiting (3). Second, in response to the [CO 2 ] increase since industrialization, genetic (4) and phenotypic plant responses (5-7) have been observed. Although century-scale changes have been detected in carbon isotopes (δ 13 C) and attributed to [CO 2 ], these responses are tied to differences in intercellular substrate concentrations that reflect several metabolic fluxes and dif...
Climate extremes and land-use changes can have major impacts on the carbon cycle of ecosystems. Their combined effects have rarely been tested. We studied whether and how the abandonment of traditionally managed mountain grassland changes the resilience of carbon dynamics to drought. In an in situ common garden experiment located in a subalpine meadow in the Austrian Central Alps, we exposed intact ecosystem monoliths from a managed and an abandoned mountain grassland to an experimental early-summer drought and measured the responses of gross primary productivity, ecosystem respiration, phytomass and its components, and of leaf area index during the drought and the subsequent recovery period. Across all these parameters, the managed grassland was more strongly affected by drought and recovered faster than the abandoned grassland. A bivariate representation of resilience confirmed an inverse relationship of resistance and recovery; thus, low resistance was related to high recovery from drought and vice versa. In consequence, the overall perturbation of the carbon cycle caused by drought was larger in the managed than the abandoned grassland. The faster recovery of carbon dynamics from drought in the managed grassland was associated with a significantly higher uptake of nitrogen from soil. Furthermore, in both grasslands leaf nitrogen concentrations were enhanced after drought and likely reflected drought-induced increases in nitrogen availability. Our study shows that ongoing and future land-use changes have the potential to profoundly alter the impacts of climate extremes on grassland carbon dynamics.Electronic supplementary materialThe online version of this article (doi:10.1007/s10021-017-0178-0) contains supplementary material, which is available to authorized users.
Droughts strongly affect carbon and nitrogen cycling in grasslands, with consequences for ecosystem productivity. Therefore, we investigated how experimental grassland communities interact with groups of soil microorganisms. In particular, we explored the mechanisms of the drought-induced decoupling of plant photosynthesis and microbial carbon cycling and its recovery after rewetting. Our aim was to better understand how root exudation during drought is linked to pulses of soil microbial activity and changes in plant nitrogen uptake after rewetting. We set up a mesocosm experiment on a meadow site and used shelters to simulate drought. We performed two 13C-CO2 pulse labelings, the first at peak drought and the second in the recovery phase, and traced the flow of assimilates into the carbohydrates of plants and the water extractable organic carbon and microorganisms from the soil. Total microbial tracer uptake in the main metabolism was estimated by chloroform fumigation extraction, whereas the lipid biomarkers were used to assess differences between the microbial groups. Drought led to a reduction of aboveground versus belowground plant growth and to an increase of 13C tracer contents in the carbohydrates, particularly in the roots. Newly assimilated 13C tracer unexpectedly accumulated in the water-extractable soil organic carbon, indicating that root exudation continued during the drought. In contrast, drought strongly reduced the amount of 13C tracer assimilated into the soil microorganisms. This reduction was more severe in the growth-related lipid biomarkers than in the metabolic compounds, suggesting a slowdown of microbial processes at peak drought. Shortly after rewetting, the tracer accumulation in the belowground plant carbohydrates and in the water-extractable soil organic carbon disappeared. Interestingly, this disappearance was paralleled by a quick recovery of the carbon uptake into metabolic and growth-related compounds from the rhizospheric microorganisms, which was probably related to the higher nitrogen supply to the plant shoots. We conclude that the decoupling of plant photosynthesis and soil microbial carbon cycling during drought is due to reduced carbon uptake and metabolic turnover of rhizospheric soil microorganisms. Moreover, our study suggests that the maintenance of root exudation during drought is connected to a fast reinitiation of soil microbial activity after rewetting, supporting plant recovery through increased nitrogen availability.
As the central carbon uptake pathway in photosynthetic cells, the Calvin-Benson cycle is among the most important biochemical cycles for life on Earth. A carbon flux of anaplerotic origin (i.e. through the chloroplast-localized oxidative branch of the pentose phosphate pathway) into the Calvin-Benson cycle was proposed recently.Here, we measured intramolecular deuterium abundances in leaf starch of Helianthus annuus grown at varying ambient CO 2 concentrations, C a . Additionally, we modelled deuterium fractionations expected for the anaplerotic pathway and compared modelled with measured fractionations.We report deuterium fractionation signals at H 1 and H 2 of starch glucose. Below a C a change point, these signals increase with decreasing C a consistent with modelled fractionations by anaplerotic flux. Under standard conditions (C a = 450 ppm corresponding to intercellular CO 2 concentrations, C i , of 328 ppm), we estimate negligible anaplerotic flux. At C a = 180 ppm (C i = 140 ppm), more than 10% of the glucose-6-phosphate entering the starch biosynthesis pathway is diverted into the anaplerotic pathway.In conclusion, we report evidence consistent with anaplerotic carbon flux into the Calvin-Benson cycle in vivo. We propose the flux may help to: maintain high levels of ribulose 1,5bisphosphate under source-limited growth conditions to facilitate photorespiratory nitrogen assimilation required to build-up source strength; and counteract oxidative stress.
As the central carbon uptake pathway in photosynthetic cells, the Calvin-Benson cycle is among the most important biochemical cycles for life on Earth. Recently, anaplerotic carbon flux (through the chloroplast-localised oxidative branch of the pentose phosphate pathway) into this cycle was proposed. Here, we measured intramolecular deuterium abundances in leaf starch of Helianthus annuus grown at varying ambient CO2 concentrations, Ca. Additionally, we modelled deuterium fractionations expected for the anaplerotic pathway and compared modelled with measured fractionations. We report deuterium fractionation signals at starch glucose H1 and H2. Below a response change point, these signals increase with decreasing Ca consistent with modelled fractionations by anaplerotic flux. Under normal growth conditions (Ca≥450 ppm corresponding to intercellular CO2 concentrations, Ci, ≥328 ppm), we estimate negligible anaplerotic flux. At Ca=180 ppm (Ci=140 ppm), we estimate that of the glucose 6-phosphate entering the starch biosynthesis pathway more than 11.5% is diverted into the anaplerotic pathway. In conclusion, we report evidence consistent with anaplerotic carbon flux into the Calvin-Benson cycle in vivo. We propose the flux may help to (i) maintain high levels of ribulose 1,5-bisphosphate under source-limited growth conditions to facilitate photorespiratory nitrogen assimilation required to build-up source strength and (ii) counteract oxidative stress.
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