Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration

Abstract While interest in photosynthetic thermal acclimation has been stimulated by climate warming, comparing results across studies requires consistent terminology. We identify five types of photosynthetic adjustments in warming experiments: photosynthesis as measured at the high growth temperature, the growth temperature, and the thermal optimum; the photosynthetic thermal optimum; and leaf-level photosynthetic capacity. Adjustments of any one of these variables need not mean a concurrent adjustment in others, which may resolve apparently contradictory results in papers using different indicators of photosynthetic acclimation. We argue that photosynthetic thermal acclimation (i.e., that benefits a plant in its new growth environment) should include adjustments of both the photosynthetic thermal optimum (T opt ) and photosynthetic rates at the growth temperature (A growth ), a combination termed constructive adjustment. However, many species show reduced photosynthesis when grown at elevated temperatures, despite adjustment of some photosynthetic variables, a phenomenon we term detractive adjustment. An analysis of 70 studies on 103 species shows that adjustment of T opt and A growth are more common than adjustment of other photosynthetic variables, but only half of the data demonstrate constructive adjustment. No systematic differences in these patterns were found between different plant functional groups. We also discuss the importance of thermal acclimation of respiration for net photosynthesis measurements, as respiratory temperature acclimation can generate apparent acclimation of photosynthetic processes, even if photosynthesis is unaltered. We show that while dark respiration is often used to estimate light respiration, the ratio of light to dark respiration shifts in a non-predictable manner with a change in leaf temperature

Consistent responses of vegetation gas exchange to elevated atmospheric CO2 emerge from heuristic and optimization models

Elevated atmospheric CO2 concentration is expected to increase leaf CO(2)assimilation rates, thus promoting plant growth and increasing leaf area. It also decreases stomatal conductance, allowing water savings, which have been hypothesized to drive large-scale greening, in particular in arid and semiarid climates. However, the increase in leaf area could reduce the benefits of elevated CO2 concentration through soil water depletion. The net effect of elevated CO2 on leaf- and canopy-level gas exchange remains uncertain. To address this question, we compare the outcomes of a heuristic model based on the Partitioning of Equilibrium Transpiration and Assimilation (PETA) hypothesis and three model variants based on stomatal optimization theory. Predicted relative changes in leaf- and canopy-level gas exchange rates are used as a metric of plant responses to changes in atmospheric CO2 concentration. Both model approaches predict reductions in leaf-level transpiration rate due to decreased stomatal conductance under elevated CO2, but negligible (PETA) or no (optimization) changes in canopy-level transpiration due to the compensatory effect of increased leaf area. Leaf- and canopy-level CO2 assimilation is predicted to increase, with an amplification of the CO2 fertilization effect at the canopy level due to the enhanced leaf area. The expected increase in vapour pressure deficit (VPD) under warmer conditions is generally predicted to decrease the sensitivity of gas exchange to atmospheric CO2 concentration in both models. The consistent predictions by different models that canopylevel transpiration varies little under elevated CO2 due to combined stomatal conductance reduction and leaf area increase highlight the coordination of physiological and morphological characteristics in vegetation to maximize resource use (here water) under altered climatic conditions

Contrasting acclimation responses to elevated CO2 and warming between an evergreen and a deciduous boreal conifer

Rising atmospheric carbon dioxide (CO2) concentrations may warm northern latitudes up to 8°C by the end of the century. Boreal forests play a large role in the global carbon cycle, and the responses of northern trees to climate change will thus impact the trajectory of future CO2 increases. We grew two North American boreal tree species at a range of future climate conditions to assess how growth and carbon fluxes were altered by high CO2 and warming. Black spruce (Picea mariana, an evergreen conifer) and tamarack (Larix laricina, a deciduous conifer) were grown under ambient (407 ppm) or elevated CO2 (750 ppm) and either ambient temperatures, a 4°C warming, or an 8°C warming. In both species, the thermal optimum of net photosynthesis (ToptA) increased and maximum photosynthetic rates declined in warm-grown seedlings, but the strength of these changes varied between species. Photosynthetic capacity (maximum rates of Rubisco carboxylation, Vcmax, and of electron transport, Jmax) was reduced in warmgrown seedlings, correlating with reductions in leaf N and chlorophyll concentrations. Warming increased the activation energy for Vcmax and Jmax (EaV and EaJ, respectively) and the thermal optimum for Jmax. In both species, the ToptA was positively correlated with both EaV and EaJ, but negatively correlated with the ratio of Jmax/Vcmax. Respiration acclimated to elevated temperatures, but there were no treatment effects on the Q10 of respiration (the increase in respiration for a 10°C increase in leaf temperature). A warming of 4°C increased biomass in tamarack, while warming reduced biomass in spruce. We show that climate change is likely to negatively affect photosynthesis and growth in black spruce more than in tamarack, and that parameters used to model photosynthesis in dynamic global vegetation models (EaV and EaJ) show no response to elevated CO2.Ontario Early Researcher Award; Canada Foundation for Innovation; Natural Sciences and Engineering Research Council of Canada; Australian National Universit

Mechanisms for minimizing height-related stomatal conductance declines in tall vines

The ability to transport water through tall stems hydraulically limits stomatal conductance (g(s)), thereby constraining photosynthesis and growth. However, some plants are able to minimize this height-related decrease in g(s), regardless of path length. We hypothesized that kudzu (Pueraria lobata) prevents strong declines in g(s) with height through appreciable structural and hydraulic compensative alterations. We observed only a 12% decline in maximum g(s) along 15-m-long stems and were able to model this empirical trend. Increasing resistance with transport distance was not compensated by increasing sapwood-to-leaf-area ratio. Compensating for increasing leaf area by adjusting the driving force would require water potential reaching -1.9 MPa, far below the wilting point (-1.2 MPa). The negative effect of stem length was compensated for by decreasing petiole hydraulic resistance and by increasing stem sapwood area and water storage, with capacitive discharge representing 8-12% of the water flux. In addition, large lateral (petiole, leaves) relative to axial hydraulic resistance helped improve water flow distribution to top leaves. These results indicate that g(s) of distal leaves can be similar to that of basal leaves, provided that resistance is highest in petioles, and sufficient amounts of water storage can be used to subsidize the transpiration stream.Peer reviewe

ENV-639: IMPACT OF VEGETATION TYPE AND CLIMATE ON EVAPOTRANSPIRATION FROM EXTENSIVE GREEN ROOFS

Stormwater management solutions are needed to increase resiliency within urban areas by: (1) maintaining the natural hydrologic cycle, (2) controlling erosion and flooding, and (3) protecting water quality (MOE, 2003). Large impervious areas from urban development results in the loss of vegetated surfaces which leads to an increase in direct runoff (e.g. Paul and Meyer, 2008). Within urban areas, conventional roofs cover 40-50% of the impervious surfaces giving them significant potential to host urban stormwater management solutions (Dunnett and Kingsbury, 2004). Green roofs are able to restore the altered hydrologic cycle closer to its natural state by reducing the volume of runoff from a roof as well as attenuating flowrates. The hydrologic benefits of green roofs are partially attributed due to the vegetated surfaces enhancing evapotranspiration (ET) in urban areas. Predicting ET from green roofs is critical to inform green roof design and for optimization of hydrologic performance. This study focuses on evaluating the influence of green roof design parameters, such as vegetation type and growth media depth, on ET and by extension the hydrologic performance of an extensive green roof. While many studies have now demonstrated the effectiveness of green roofs in attenuating flowrate and reducing the volume of stormwater runoff (e.g., VanWoert et al., 2005a, Fassman-Beck et al., 2013, Berndtsson, 2010), little field research has been completed on directly quantifying ET rates and the hydrologic benefits green roofs in Canada including the influence of different vegetation types. The lack of available data on ET rates from green roofs limits optimal green roof design under the Canadian climate

The effect of carbon and nutrient loading during nursery culture on the growth of black spruce seedlings: a six-year field study

Abstract We tested the effects of exponential nutrient loading and springtime carbon loading during nursery culture on the field performance of black spruce (Picea mariana (Mill.) B.S.P.). Seedlings were grown from seed with a conventional, fixed dose fertilizer (10 mg N seedling À1 ) or an exponential nutrient loading regime (75 mg N seedling À1 ). The following spring, seedlings were exposed for two weeks to either ambient (370 ppm) or elevated levels of CO 2 (800 ppm) and then planted in the field; seedling growth was followed for the next six years. Exponential nutrient loading increased seedling height, stem diameter and leader growth, with the largest increases in height and leader length occurring in the first three years after outplanting. Carbon loading increased seedling height and leader length, but only in seedlings that had been exponentially nutrient loaded. A combination of carbon and nutrient loading increased shoot height 26%, stem diameter 37% and leader length 40% over trees that received neither treatment. These results demonstrate that the growth enhancement seen under exponential nutrient loading is maintained under field conditions for at least six years. Carbon loading just before outplanting was a useful supplement to nutrient loading, but was ineffective in the absence of nutrient loading

Photosynthetic and Respiratory Responses of Two Bog Shrub Species to Whole Ecosystem Warming and Elevated CO2 at the Boreal-Temperate Ecotone

Peatlands within the boreal-temperate ecotone contain the majority of terrestrial carbon in this region, and there is concern over the fate of such carbon stores in the face of global environmental changes. The Spruce and Peatland Response Under Changing Environments (SPRUCE) facility aims to advance the understanding of how such peatlands may respond to such changes, using a combination of whole ecosystem warming (WEW; +0, 2.25, 4.5, 6.75, and 9◦C) and elevated CO2 (eCO2; +500 ppm) treatments in an intact bog ecosystem. We examined photosynthetic and respiration responses in leaves of two ericaceous shrub species–leatherleaf [Chamaedaphne calyculata (L.) Moench] and bog Labrador tea [Rhododendron groenlandicum (Oeder) Kron & Judd]–to the first year of combined eCO2 and WEW treatments at SPRUCE. We surveyed the leaf N content per area (Narea), net photosynthesis (AST ) and respiration (RD25) at 25◦C and 400 ppm CO2 and net photosynthesis at mean growing conditions (AGR) of newly emerged, mature and overwintered leaves. We also measured leaf non-structural carbohydrate content (NSC) in mature leaves. The effects of WEW and eCO2 varied by season and species, highlighting the need to accommodate such variability in modeling this system. In mature leaves, we did not observe a response to either treatment of AST or RD25 in R. groenlandicum, but we did observe a 50% decrease in AST of C. calyculata with eCO2. In mature leaves under eCO2, neither species had increased AGR and both had increases in NSC, indicating acclimation of photosynthesis to eCO2 may be related to source-sink imbalances of carbohydrates. Thus, productivity gains of shrubs under eCO2 may be lower than previously predicted for this site by models not accounting for such acclimation. In newly emerged leaves, AST increased with WEW in R. groenlandicum, but not C. calyculata. Overwintered leaves exhibited a decrease in RD25 for R. groenlandicum and in AST for C. calyculata with increasing WEW, as well as an increase of AGR with eCO2 in both species. Responses in newly emerged and overwintered leaves may reflect physiological acclimation or phenological changes in response to treatments

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

Contribution of Various Carbon Sources Toward Isoprene Biosynthesis in Poplar Leaves Mediated by Altered Atmospheric CO2 Concentrations

Biogenically released isoprene plays important roles in both tropospheric photochemistry and plant metabolism. We performed a 13CO2-labeling study using proton-transfer-reaction mass spectrometry (PTR-MS) to examine the kinetics of recently assimilated photosynthate into isoprene emitted from poplar (Populus × canescens) trees grown and measured at different atmospheric CO2 concentrations. This is the first study to explicitly consider the effects of altered atmospheric CO2 concentration on carbon partitioning to isoprene biosynthesis. We studied changes in the proportion of labeled carbon as a function of time in two mass fragments, M41+, which represents, in part, substrate derived from pyruvate, and M69+, which represents the whole unlabeled isoprene molecule. We observed a trend of slower 13C incorporation into isoprene carbon derived from pyruvate, consistent with the previously hypothesized origin of chloroplastic pyruvate from cytosolic phosphenolpyruvate (PEP). Trees grown under sub-ambient CO2 (190 ppmv) had rates of isoprene emission and rates of labeling of M41+ and M69+ that were nearly twice those observed in trees grown under elevated CO2 (590 ppmv). However, they also demonstrated the lowest proportion of completely labeled isoprene molecules. These results suggest that under reduced atmospheric CO2 availability, more carbon from stored/older carbon sources is involved in isoprene biosynthesis, and this carbon most likely enters the isoprene biosynthesis pathway through the pyruvate substrate. We offer direct evidence that extra-chloroplastic rather than chloroplastic carbon sources are mobilized to increase the availability of pyruvate required to up-regulate the isoprene biosynthesis pathway when trees are grown under sub-ambient CO2