Acclimation of leaf respiration temperature responses across thermally contrasting biomes.

Short-term temperature response curves of leaf dark respiration (R-T) provide insights into a critical process that influences plant net carbon exchange. This includes how respiratory traits acclimate to sustained changes in the environment. Our study analysed 860 high-resolution R-T (10-70°C range) curves for: (a) 62 evergreen species measured in two contrasting seasons across several field sites/biomes; and (b) 21 species (subset of those sampled in the field) grown in glasshouses at 20°C : 15°C, 25°C : 20°C and 30°C : 25°C, day : night. In the field, across all sites/seasons, variations in R25 (measured at 25°C) and the leaf T where R reached its maximum (Tmax ) were explained by growth T (mean air-T of 30-d before measurement), solar irradiance and vapour pressure deficit, with growth T having the strongest influence. R25 decreased and Tmax increased with rising growth T across all sites and seasons with the single exception of winter at the cool-temperate rainforest site where irradiance was low. The glasshouse study confirmed that R25 and Tmax thermally acclimated. Collectively, the results suggest: (1) thermal acclimation of leaf R is common in most biomes; and (2) the high T threshold of respiration dynamically adjusts upward when plants are challenged with warmer and hotter climates.

Leaf trait variation is similar among genotypes of Eucalyptus camaldulensis from differing climates and arises in plastic responses to the seasons rather than water availability.

We used a widely distributed tree Eucalyptus camaldulensis subsp. camaldulensis to partition intraspecific variation in leaf functional traits to genotypic variation and phenotypic plasticity. We examined if genotypic variation is related to the climate of genotype provenance and whether phenotypic plasticity maintains performance in a changing environment. Ten genotypes from different climates were grown in a common garden under watering treatments reproducing the wettest and driest edges of the subspecies' distribution. We measured functional traits reflecting leaf metabolism and associated with growth (respiration rate, nitrogen and phosphorus concentrations, and leaf mass per area) and performance proxies (aboveground biomass and growth rate) each season over a year. Genotypic variation contributed substantially to the variation in aboveground biomass but much less in growth rate and leaf traits. Phenotypic plasticity was a large source of the variation in leaf traits and performance proxies and was greater among sampling dates than between watering treatments. The variation in leaf traits was weakly correlated to performance proxies, and both were unrelated to the climate of genotype provenance. Intraspecific variation in leaf traits arises similarly among genotypes in response to seasonal environmental variation, instead of long-term water availability or climate of genotype provenance.

The validity of optimal leaf traits modelled on environmental conditions.

The ratio of leaf intercellular to ambient CO2 (χ) is modulated by stomatal conductance (gs ). These quantities link carbon (C) assimilation with transpiration, and along with photosynthetic capacities (Vcmax and Jmax ) are required to model terrestrial C uptake. We use optimization criteria based on the growth environment to generate predicted values of photosynthetic and water-use efficiency traits and test these against a unique dataset. Leaf gas-exchange parameters and carbon isotope discrimination were analysed in relation to local climate across a continental network of study sites. Sun-exposed leaves of 50 species at seven sites were measured in contrasting seasons. Values of χ predicted from growth temperature and vapour pressure deficit were closely correlated to ratios derived from C isotope (δ13 C) measurements. Correlations were stronger in the growing season. Predicted values of photosynthetic traits, including carboxylation capacity (Vcmax ), derived from δ13 C, growth temperature and solar radiation, showed meaningful agreement with inferred values derived from gas-exchange measurements. Between-site differences in water-use efficiency were, however, only weakly linked to the plant's growth environment and did not show seasonal variation. These results support the general hypothesis that many key parameters required by Earth system models are adaptive and predictable from plants' growth environments.

Plasticity of photosynthetic heat tolerance in plants adapted to thermally contrasting biomes.

In many biomes, plants are subject to heatwaves, potentially causing irreversible damage to the photosynthetic apparatus. Field surveys have documented global, temperature-dependent patterns in photosynthetic heat tolerance (PHT ); however, it remains unclear if these patterns reflect acclimation in PHT or inherent differences among species adapted to contrasting habitats. To address these unknowns, we quantified seasonal variations in Tcrit (high temperature where minimal chlorophyll-a fluorescence rises rapidly, reflecting disruption to photosystem II) in 62 species native to 6 sites from 5 thermally contrasting biomes across Australia. Tcrit and leaf fatty acid (FA) composition (important for membrane stability) were quantified in three temperature-controlled glasshouses in 20 of those species. Tcrit was greatest at hot field sites and acclimated seasonally (summer > winter, increasing on average 0.34 °C per °C increase in growth temperature). The glasshouse study showed that Tcrit was inherently higher in species from warmer habitats (increasing 0.16 °C per °C increase in origin annual mean maximum temperature) and acclimated to increasing growth temperature (0.24 °C °C-1 ). Variations in Tcrit were positively correlated with the relative abundance of saturated FAs, with FAs accounting for 40% of Tcrit variation. These results highlight the importance of both plastic adjustments and inherent differences determining contemporary continent-wide patterns in PHT .

Macromolecular rate theory (MMRT) provides a thermodynamics rationale to underpin the convergent temperature response in plant leaf respiration.

Temperature is a crucial factor in determining the rates of ecosystem processes, for example, leaf respiration (R) - the flux of plant respired CO2 from leaves to the atmosphere. Generally, R increases exponentially with temperature and formulations such as the Arrhenius equation are widely used in earth system models. However, experimental observations have shown a consequential and consistent departure from an exponential increase in R. What are the principles that underlie these observed patterns? Here, we demonstrate that macromolecular rate theory (MMRT), based on transition state theory (TST) for enzyme-catalyzed kinetics, provides a thermodynamic explanation for the observed departure and the convergent temperature response of R using a global database. Three meaningful parameters emerge from MMRT analysis: the temperature at which the rate of respiration would theoretically reach a maximum (the optimum temperature, Topt ), the temperature at which the respiration rate is most sensitive to changes in temperature (the inflection temperature, Tinf ) and the overall curvature of the log(rate) versus temperature plot (the change in heat capacity for the system, ΔCP‡). On average, the highest potential enzyme-catalyzed rates of respiratory enzymes for R are predicted to occur at 67.0 ± 1.2°C and the maximum temperature sensitivity at 41.4 ± 0.7°C from MMRT. The average curvature (average negative ΔCP‡) was -1.2 ± 0.1 kJ mol-1  K-1 . Interestingly, Topt , Tinf and ΔCP‡ appear insignificantly different across biomes and plant functional types, suggesting that thermal response of respiratory enzymes in leaves could be conserved. The derived parameters from MMRT can serve as thermal traits for plant leaves that represent the collective temperature response of metabolic respiratory enzymes and could be useful to understand regulations of R under a warmer climate. MMRT extends the classic TST to enzyme-catalyzed reactions and provides an accurate and mechanistic model for the short-term temperature response of R around the globe.

Thermal limits of leaf metabolism across biomes.

High-temperature tolerance in plants is important in a warming world, with extreme heat waves predicted to increase in frequency and duration, potentially leading to lethal heating of leaves. Global patterns of high-temperature tolerance are documented in animals, but generally not in plants, limiting our ability to assess risks associated with climate warming. To assess whether there are global patterns in high-temperature tolerance of leaf metabolism, we quantified Tcrit (high temperature where minimal chlorophyll a fluorescence rises rapidly and thus photosystem II is disrupted) and Tmax (temperature where leaf respiration in darkness is maximal, beyond which respiratory function rapidly declines) in upper canopy leaves of 218 plant species spanning seven biomes. Mean site-based Tcrit values ranged from 41.5 °C in the Alaskan arctic to 50.8 °C in lowland tropical rainforests of Peruvian Amazon. For Tmax , the equivalent values were 51.0 and 60.6 °C in the Arctic and Amazon, respectively. Tcrit and Tmax followed similar biogeographic patterns, increasing linearly (˜8 °C) from polar to equatorial regions. Such increases in high-temperature tolerance are much less than expected based on the 20 °C span in high-temperature extremes across the globe. Moreover, with only modest high-temperature tolerance despite high summer temperature extremes, species in mid-latitude (~20-50°) regions have the narrowest thermal safety margins in upper canopy leaves; these regions are at the greatest risk of damage due to extreme heat-wave events, especially under conditions when leaf temperatures are further elevated by a lack of transpirational cooling. Using predicted heat-wave events for 2050 and accounting for possible thermal acclimation of Tcrit and Tmax , we also found that these safety margins could shrink in a warmer world, as rising temperatures are likely to exceed thermal tolerance limits. Thus, increasing numbers of species in many biomes may be at risk as heat-wave events become more severe with climate change.

Convergence in the temperature response of leaf respiration across biomes and plant functional types.

Plant respiration constitutes a massive carbon flux to the atmosphere, and a major control on the evolution of the global carbon cycle. It therefore has the potential to modulate levels of climate change due to the human burning of fossil fuels. Neither current physiological nor terrestrial biosphere models adequately describe its short-term temperature response, and even minor differences in the shape of the response curve can significantly impact estimates of ecosystem carbon release and/or storage. Given this, it is critical to establish whether there are predictable patterns in the shape of the respiration-temperature response curve, and thus in the intrinsic temperature sensitivity of respiration across the globe. Analyzing measurements in a comprehensive database for 231 species spanning 7 biomes, we demonstrate that temperature-dependent increases in leaf respiration do not follow a commonly used exponential function. Instead, we find a decelerating function as leaves warm, reflecting a declining sensitivity to higher temperatures that is remarkably uniform across all biomes and plant functional types. Such convergence in the temperature sensitivity of leaf respiration suggests that there are universally applicable controls on the temperature response of plant energy metabolism, such that a single new function can predict the temperature dependence of leaf respiration for global vegetation. This simple function enables straightforward description of plant respiration in the land-surface components of coupled earth system models. Our cross-biome analyses shows significant implications for such fluxes in cold climates, generally projecting lower values compared with previous estimates.

Global variability in leaf respiration in relation to climate, plant functional types and leaf traits.

Leaf dark respiration (Rdark ) is an important yet poorly quantified component of the global carbon cycle. Given this, we analyzed a new global database of Rdark and associated leaf traits. Data for 899 species were compiled from 100 sites (from the Arctic to the tropics). Several woody and nonwoody plant functional types (PFTs) were represented. Mixed-effects models were used to disentangle sources of variation in Rdark . Area-based Rdark at the prevailing average daily growth temperature (T) of each site increased only twofold from the Arctic to the tropics, despite a 20°C increase in growing T (8-28°C). By contrast, Rdark at a standard T (25°C, Rdark (25) ) was threefold higher in the Arctic than in the tropics, and twofold higher at arid than at mesic sites. Species and PFTs at cold sites exhibited higher Rdark (25) at a given photosynthetic capacity (Vcmax (25) ) or leaf nitrogen concentration ([N]) than species at warmer sites. Rdark (25) values at any given Vcmax (25) or [N] were higher in herbs than in woody plants. The results highlight variation in Rdark among species and across global gradients in T and aridity. In addition to their ecological significance, the results provide a framework for improving representation of Rdark in terrestrial biosphere models (TBMs) and associated land-surface components of Earth system models (ESMs).

High-resolution temperature responses of leaf respiration in snow gum (Eucalyptus pauciflora) reveal high-temperature limits to respiratory function.

We tested whether snow gum (Eucalyptus pauciflora) trees growing in thermally contrasting environments exhibit generalizable temperature (T) response functions of leaf respiration (R) and fluorescence (Fo). Measurements were made on pot-grown saplings and field-grown trees (growing between 1380 and 2110 m a.s.l.). Using a continuous, high-resolution protocol, we quantified T response curves of R and Fo--these data were used to identify an algorithm for modelling R-T curves at subcritical T's and establish variations in heat tolerance. For the latter, we quantified Tmax [T where R is maximal] and Tcrit [T where Fo rises rapidly]. Tmax ranged from 51 to 57 °C, varying with season (e.g. winter summer). Tcrit ranged from 41 to 49 °C in summer and from 58 to 63 °C in winter. Thus, surprisingly, leaf energy metabolism was more heat-tolerant in trees experiencing ice-encasement in winter than warmer conditions in summer. A polynomial model fitted to log-transformed R data provided the best description of the T-sensitivity of R (between 10 and 45 °C); using these model fits, we found that the negative slope of the Q10 -T relationship was greater in winter than in summer. Collectively, our results (1) highlight high-T limits of energy metabolism in E. pauciflora and (2) provide a framework for improving representation of T-responses of leaf R in predictive models.

Xylem traits mediate a trade-off between resistance to freeze-thaw-induced embolism and photosynthetic capacity in overwintering evergreens.

Hydraulic traits were studied in temperate, woody evergreens in a high-elevation heath community to test for trade-offs between the delivery of water to canopies at rates sufficient to sustain photosynthesis and protection against disruption to vascular transport caused by freeze-thaw-induced embolism. Freeze-thaw-induced loss in hydraulic conductivity was studied in relation to xylem anatomy, leaf- and sapwood-specific hydraulic conductivity and gas exchange characteristics of leaves. We found evidence that a trade-off between xylem transport capacity and safety from freeze-thaw-induced embolism affects photosynthetic activity in overwintering evergreens. The mean hydraulically weighted xylem vessel diameter and sapwood-specific conductivity correlated with susceptibility to freeze-thaw-induced embolism. There was also a strong correlation of hydraulic supply and demand across species; interspecific differences in stomatal conductance and CO(2) assimilation rates were correlated linearly with sapwood- and leaf-specific hydraulic conductivity. Xylem vessel anatomy mediated an apparent trade-off between resistance to freeze-thaw-induced embolism and hydraulic and photosynthetic capacity during the winter. These results point to a new role for xylem functional traits in determining the degree to which species can maintain photosynthetic carbon gain despite freezing events and cold winter temperatures.

Higher daytime leaf temperatures contribute to lower freeze tolerance under elevated CO2.

Elevated atmospheric CO2 adversely affects freezing tolerance in many evergreens, but the underlying mechanism(s) have been elusive. We compared effects of elevated CO2 with those of daytime warming on acclimation of snow gum (Eucalyptus pauciflora) to freezing temperatures under field conditions. Reduction in stomatal conductance g(c) under elevated CO2 was shown to cause leaf temperature to increase by up to 3 degrees C. In this study, this increase in leaf temperature was simulated under ambient CO2 conditions by using a free air temperature increase (FATI) system to warm snow gum leaves during daytime, thereby increasing the diurnal range in temperature without affecting temperature minima. Acclimation to freezing temperatures was assessed using measures of electrolyte leakage and photosynthetic efficiency of leaf discs exposed to different nadir temperatures. Here, we show that both elevated CO2 and daytime warming delayed acclimation to freezing temperatures for 2-3 weeks after which time freeze tolerance of the treated plants in both the FATI and open top chamber (OTC) experiments did not differ from control plants. Our results support the hypothesis that delayed development of freezing tolerance under elevated CO2 is because of higher daytime leaf temperatures under elevated CO2. Thus, potential gains in productivity in response to increasing atmospheric CO2 and prolonging the growing season may be reduced by an increase in freezing stress in frost-prone area.