Plant responses to climate warming : physiological adjustments and implications for plant functioning in a future, warmer world

The Earth’s average temperatures have been rising since the start of the Industrial Revolution, in major part driven by rising concentrations of carbon dioxide. Correlated with the rise of atmospheric CO2 from ~280 ppm (before the start of the Industrial Revolution) to the current 410 ppm, the average temperature has warmed by about 1°C since 1880 (Ciais et al., 2013). However, as CO2 concentrations continue to rise, the Earth will experience further warming, although how much warming will also depend on political will and human capacity to reduce carbon emissions in the near future. As such, rising temperatures will create new climate conditions in many places, affecting species’ functioning and their current geographical distributions

Nitrogen Availability Alters Species Photosynthetic Responses to Elevated Atmospheric CO2.

Atmospheric [CO2] and soil N availability are critical resources for plant growth, both of which are increasing due to global climate change. Therefore, we need to understand how additional resources in the form of elevated CO2 and increased N availability impact photosynthesis as the main driver of plant productivity. I conducted studies on pines, grasses and forbs, all grown under Free-Air CO2 Enrichment (FACE) and nitrogen fertilization, to determine how these global change factors affect plant photosynthesis and nitrogen use. Both forbs and pines showed down-regulation of photosynthetic capacity under elevated CO2 as changes in Vcmax of 23% and 17%, respectively. Grasses did not show significant photosynthetic down-regulation under elevated CO2 compared to ambient CO2. Grasses showed the least reduction of Nmass in elevated CO2 (-7%), followed by pines (-12%) and forbs (-18%). When reductions in photosynthetic capacity occurred, as was observed in forbs, a smaller photosynthetic stimulation of 9% occurred under elevated CO2 than when no down-regulation was observed. Compared to forb species, CO2-induced photosynthetic stimulation was 31% to 57% for pines and grasses, respectively. A reduction in foliar N concurrent with down-regulation of photosynthetic capacity in elevated CO2 could indicate plant N redistribution where N is allocated away from photosynthetic components. This N redistribution in response to elevated CO2 may be a key response in adjusting plant growth to long-term elevated CO2. At the canopy scale, increased leaf area index (LAI) under elevated CO2 due to photosynthetic enhancement could compensate for the effects of physiological down-regulation on canopy photosynthesis. Grasses had higher canopy photosynthesis than forbs under elevated CO2 due to large LAI increases in combination with no photosynthetic down-regulation. Both LAI and photosynthetic down-regulation are important in determining plant canopy productivity in elevated CO2. Given that few models include CO2-induced photosynthetic adjustments such as decreased foliar N or reduced photosynthetic capacity, I conclude that much of previous experimental work on CO2 enrichment has greatly overestimated photosynthetic enhancement in native ecosystems. Interacting effects of long-term elevated CO2 and N fertilization may ultimately determine the magnitude of C uptake from the atmosphere and overall plant productivity.Ph.D.Natural Resources and EnvironmentUniversity of Michigan, Horace H. Rackham School of Graduate Studieshttp://deepblue.lib.umich.edu/bitstream/2027.42/61580/1/kcrous_1.pd

Temperature responses of photosynthesis and respiration in evergreen trees from boreal to tropical latitudes

Evergreen species are widespread across the globe, representing two major plant functional forms in terrestrial models. We reviewed and analysed the responses of photosynthesis and respiration to warming in 101 evergreen species from boreal to tropical biomes. Summertime temperatures affected both latitudinal gas exchange rates and the degree of responsiveness to experimental warming. The decrease in net photosynthesis at 25 degrees C (A(net25)) was larger with warming in tropical climates than cooler ones. Respiration at 25 degrees C (R-25) was reduced by 14% in response to warming across species and biomes. Gymnosperms were more sensitive to greater amounts of warming than broadleaved evergreens, with A(net25) and R-25 reduced c. 30-40% with > 10 degrees C warming. While standardised rates of carboxylation (V-cmax25) and electron transport (J(max25)) adjusted to warming, the magnitude of this adjustment was not related to warming amount (range 0.6-16 degrees C). The temperature optimum of photosynthesis (T-optA) increased on average 0.34 degrees C per degrees C warming. The combination of more constrained acclimation of photosynthesis and increasing respiration rates with warming could possibly result in a reduced carbon sink in future warmer climates. The predictable patterns of thermal acclimation across biomes provide a strong basis to improve modelling predictions of the future terrestrial carbon sink with warming

Water availability affects seasonal CO₂-induced photosynthetic enhancement in herbaceous species in a periodically dry woodland

Elevated atmospheric CO2 (eCO2) is expected to reduce the impacts of drought and increase photosynthetic rates via two key mechanisms: first, through decreased stomatal conductance (gs) and increased soil water content (VSWC) and second, through increased leaf internal CO2 (Ci) and decreased stomatal limitations (Slim>). It is unclear if such findings from temperate grassland studies similarly pertain to warmer ecosystems with periodic water deficits. We tested these mechanisms in three important C3 herbaceous species in a periodically dry Eucalyptus woodland and investigated how eCO2-induced photosynthetic enhancement varied with seasonal water availability, over a 3 year period. Leaf photosynthesis increased by 10%–50% with a 150 μmol mol-1 increase in atmospheric CO2 across seasons. This eCO2-induced increase in photosynthesis was a function of seasonal water availability, given by recent precipitation and mean daily VSWC. The highest photosynthetic enhancement by eCO2 (>30%) was observed during the most water-limited period, for example, with VSWC 2 there was neither a significant decrease in gs in the three herbaceous species, nor increases in VSWC, indicating no “water-savings effect” of eCO2. Periods of low VSWC showed lower gs (less than ≈ 0.12 mol m-2 s-1), higher relative Slim (>30%) and decreased Ci under the ambient CO2 concentration (aCO2), with leaf photosynthesis strongly carboxylation-limited. The alleviation of Slim by eCO2 was facilitated by increasing Ci, thus yielding a larger photosynthetic enhancement during dry periods. We demonstrated that water availability, but not eCO2, controls gs and hence the magnitude of photosynthetic enhancement in the understory herbaceous plants. Thus, eCO2 has the potential to alter vegetation functioning in a periodically dry woodland understory through changes in stomatal limitation to photosynthesis, not by the “water-savings effect” usually invoked in grasslands

Linking photosynthesis and leaf N allocation under future elevated CO2 and climate warming in Eucalyptus globulus

Leaf-level photosynthetic processes and their environmental dependencies are critical for estimating CO2 uptake from the atmosphere. These estimates use biochemical-based models of photosynthesis that require accurate Rubisco kinetics. We investigated the effects of canopy position, elevated atmospheric CO2 [eC; ambient CO2 (aC)+240 ppm] and elevated air temperature (eT; ambient temperature (aT)+3 °C) on Rubisco content and activity together with the relationship between leaf N and Vcmax (maximal Rubisco carboxylation rate) of 7 m tall, soil-grown Eucalyptus globulus trees. The kinetics of E. globulus and tobacco Rubisco at 25 °C were similar. In vitro estimates of Vcmax derived from measures of E. globulus Rubisco content and kinetics were consistent, although slightly lower, than the in vivo rates extrapolated from gas exchange. In E. globulus, the fraction of N invested in Rubisco was substantially lower than for crop species and varied with treatments. Photosynthetic acclimation of E. globulus leaves to eC was underpinned by reduced leaf N and Rubisco contents; the opposite occurred in response to eT coinciding with growth resumption in spring. Our findings highlight the adaptive capacity of this key forest species to allocate leaf N flexibly to Rubisco and other photosynthetic proteins across differing canopy positions in response to future, warmer and elevated [CO2] climates.This is a contribution from the Hawkesbury Forest Experiment. We thank Burhan Amiji and Dr Craig Barton for their assistance in undertaking gas exchange. This research was supported by funding from ARC grant DP160102452, the Forest Industries Climate Change Research Fund from the Australian Department of Agriculture, and the Commonwealth Government through the Education Investment Fund

Nitrogen and Phosphorus Retranslocation of Leaves and Stemwood in a Mature Eucalyptus Forest Exposed to 5 Years of Elevated CO2

Elevated CO2 affects C cycling processes which in turn can influence the nitrogen (N) and phosphorus (P) concentrations of plant tissues. Given differences in how N and P are used by plants, we asked if their stoichiometry in leaves and wood was maintained or altered in a long-term elevated CO2 experiment in a mature Eucalyptus forest on a low P soil (EucFACE). We measured N and P concentrations in green leaves at different ages at the top of mature trees across 6 years including 5 years in elevated CO2. N and P concentrations in green and senesced leaves and wood were determined to evaluate both spatial and temporal variation of leaf N and P concentrations, including the N and P retranslocation in leaves and wood. Leaf P concentrations were 32% lower in old mature leaves compared to newly flushed leaves with no effect of elevated CO2 on leaf P. By contrast, elevated CO2 significantly decreased leaf N concentrations in newly flushed leaves but this effect disappeared as leaves matured. As such, newly flushed leaves had 9% lower N:P ratios in elevated CO2 and N:P ratios were not different in mature green leaves (CO2 by Age effect, P = 0.02). Over time, leaf N and P concentrations in the upper canopy slightly declined in both CO2 treatments compared to before the start of the experiment. P retranslocation in leaves was 50%, almost double that of N retranslocation (29%), indicating that this site was P-limited and that P retranslocation was an important mechanism in this ecosystem to retain P in plants. As P-limited trees tend to store relatively more N than P, we found an increased N:P ratio in sapwood in response to elevated CO2 (P < 0.01), implying N accumulation in live wood. The flexible stoichiometric ratios we observed can have important implications for how plants adjust to variable environmental conditions including climate change. Hence, variable nutrient stoichiometry should be accounted for in large-scale Earth Systems models invoking biogeochemical processes

Drought increases heat tolerance of leaf respiration in Eucalyptus globulus saplings grown under both ambient and elevated atmospheric [CO₂] and temperature

Climate change is resulting in increasing atmospheric [CO₂], rising growth temperature (T), and greater frequency/severity of drought, with each factor having the potential to alter the respiratory metabolism of leaves. Here, the effects of elevated atmospheric [CO₂], sustained warming, and drought on leaf dark respiration (R(dark)), and the short-term T response of R(dark) were examined in Eucalyptus globulus. Comparisons were made using seedlings grown under different [CO₂], T, and drought treatments. Using high resolution T-response curves of R(dark) measured over the 15-65 °C range, it was found that elevated [CO₂], elevated growth T, and drought had little effect on rates of R(dark) measured at T <35 °C and that there was no interactive effect of [CO₂], growth T, and drought on T response of R(dark). However, drought increased R(dark) at high leaf T typical of heatwave events (35-45 °C), and increased the measuring T at which maximal rates of R(dark) occurred (Tmax) by 8 °C (from 52 °C in well-watered plants to 60 °C in drought-treated plants). Leaf starch and soluble sugars decreased under drought and elevated growth T, respectively, but no effect was found under elevated [CO₂]. Elevated [CO₂] increased the Q₁₀ of R(dark) (i.e. proportional rise in R(dark) per 10 °C) over the 15-35 °C range, while drought increased Q₁₀ values between 35 °C and 45 °C. Collectively, the study highlights the dynamic nature of the T dependence of R dark in plants experiencing future climate change scenarios, particularly with respect to drought and elevated [CO₂].This work was funded by the Australian Research Council (ARC FT0991448, DP1093759, and CE140100008, to OKA; and DP0879531, to DTT). This project is supported by funding from the Australian Government Department of Agriculture, Fisheries and Forestry under its Forest Industries Climate Change Research Fund programme. Support for the renovation of the Hawkesbury Forest Experiment tree chambers to improve T and humidity control of the WTC was provided as part of an initiative of the Australian Government through the Education Investment Fund supporting research infrastructure

Predicting resilience through the lens of competing adjustments to vegetation function

There is a pressing need to better understand ecosystem resilience to droughts and heatwaves. Eco-evolutionary optimization approaches have been proposed as means to build this understanding in land surface models and improve their predictive capability, but competing approaches are yet to be tested together. Here, we coupled approaches that optimize canopy gas exchange and leaf nitrogen investment, respectively, extending both approaches to account for hydraulic impairment. We assessed model predictions using observations from a native Eucalyptus woodland that experienced repeated droughts and heatwaves between 2013 and 2020, whilst exposed to an elevated [CO2] treatment. Our combined approaches improved predictions of transpiration and enhanced the simulated magnitude of the CO2 fertilization effect on gross primary productivity. The competing approaches also worked consistently along axes of change in soil moisture, leaf area, and [CO2]. Despite predictions of a significant percentage loss of hydraulic conductivity due to embolism (PLC) in 2013, 2014, 2016, and 2017 (99th percentile PLC > 45%), simulated hydraulic legacy effects were small and short-lived (2 months). Our analysis suggests that leaf shedding and/or suppressed foliage growth formed a strategy to mitigate drought risk. Accounting for foliage responses to water availability has the potential to improve model predictions of ecosystem resilience

Leaf day respiration: Low CO2 flux but high significance for metabolism and carbon balance

It has been 75 yr since leaf respiratory metabolism in the light (day respiration) was identified as a low-flux metabolic pathway that accompanies photosynthesis. In principle, it provides carbon backbones for nitrogen assimilation and evolves CO2 and thus impacts on plant carbon and nitrogen balances. However, for a long time, uncertainties have remained as to whether techniques used to measure day respiratory efflux were valid and whether day respiration responded to environmental gaseous conditions. In the past few years, significant advances have been made using carbon isotopes, ‘omics’ analyses and surveys of respiration rates in mesocosms or ecosystems. There is substantial evidence that day respiration should be viewed as a highly dynamic metabolic pathway that interacts with photosynthesis and photorespiration and responds to atmospheric CO2 mole fraction. The view of leaf day respiration as a constant and/or negligible parameter of net carbon exchange is now outdated and it should now be regarded as a central actor of plant carbon-use efficiency.G.T. also thank the Australian Research Council for its financial support through a Future Fellowship, under contract FT140100645

Carbon-phosphorus cycle models overestimate CO2 enrichment response in a mature Eucalyptus forest.

The importance of phosphorus (P) in regulating ecosystem responses to climate change has fostered P-cycle implementation in land surface models, but their CO2 effects predictions have not been evaluated against measurements. Here, we perform a data-driven model evaluation where simulations of eight widely used P-enabled models were confronted with observations from a long-term free-air CO2 enrichment experiment in a mature, P-limited Eucalyptus forest. We show that most models predicted the correct sign and magnitude of the CO2 effect on ecosystem carbon (C) sequestration, but they generally overestimated the effects on plant C uptake and growth. We identify leaf-to-canopy scaling of photosynthesis, plant tissue stoichiometry, plant belowground C allocation, and the subsequent consequences for plant-microbial interaction as key areas in which models of ecosystem C-P interaction can be improved. Together, this data-model intercomparison reveals data-driven insights into the performance and functionality of P-enabled models and adds to the existing evidence that the global CO2-driven carbon sink is overestimated by models