skip to main content


The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, May 23 until 2:00 AM ET on Friday, May 24 due to maintenance. We apologize for the inconvenience.

This content will become publicly available on December 1, 2024

Title: Increased activity of core photorespiratory enzymes and CO2 transfer conductances are associated with higher and more optimal photosynthetic rates under elevated temperatures in the extremophile Rhazya stricta

Increase photorespiration and optimising intrinsic water use efficiency are unique challenges to photosynthetic carbon fixation at elevated temperatures. To determine how plants can adapt to facilitate high rates of photorespiration at elevated temperatures while also maintaining water‐use efficiency, we performed in‐depth gas exchange and biochemical assays of the C3extremophile,Rhazya stricta. These results demonstrate thatR. strictasupports higher rates of photorespiration under elevated temperatures and that these higher rates of photorespiration correlate with increased activity of key photorespiratory enzymes; phosphoglycolate phosphatase and catalase. The increased photorespiratory enzyme activities may increase the overall capacity of photorespiration by reducing enzymatic bottlenecks and allowing minimal inhibitor accumulation under high photorespiratory rates. Additionally, we found the CO2transfer conductances (stomatal and mesophyll) are re‐allocated to increase the water‐use efficiency inR. strictabut not necessarily the photosynthetic response to temperature. These results suggest important adaptive strategies inR. strictathat maintain photosynthetic rates under elevated temperatures with optimal water loss. The strategies found in R. stricta may inform breeding and engineering efforts in other C3species to improve photosynthetic efficiency at high temperatures.

more » « less
Award ID(s):
Author(s) / Creator(s):
; ;
Publisher / Repository:
Plant, Cell & Environment
Date Published:
Journal Name:
Plant, Cell & Environment
Page Range / eLocation ID:
3704 to 3720
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Photorespiration can limit gross primary productivity in terrestrial plants. The rate of photorespiration relative to carbon fixation increases with temperature and decreases with atmospheric [CO2]. However, the extent to which this rate varies in the environment is unclear. Here, we introduce a proxy for relative photorespiration rate based on the clumped isotopic composition of methoxyl groups (R–O–CH3) in wood. Most methoxyl C–H bonds are formed either during photorespiration or the Calvin cycle and thus their isotopic composition may be sensitive to the mixing ratio of these pathways. In water-replete growing conditions, we find that the abundance of the clumped isotopologue13CH2D correlates with temperature (18–28 °C) and atmospheric [CO2] (280–1000 ppm), consistent with a common dependence on relative photorespiration rate. When applied to a global dataset of wood, we observe global trends of isotopic clumping with climate and water availability. Clumped isotopic compositions are similar across environments with temperatures below ~18 °C. Above ~18 °C, clumped isotopic compositions in water-limited and water-replete trees increasingly diverge. We propose that trees from hotter climates photorespire substantially more than trees from cooler climates. How increased photorespiration is managed depends on water availability: water-replete trees export more photorespiratory metabolites to lignin whereas water-limited trees either export fewer overall or direct more to other sinks that mitigate water stress. These disparate trends indicate contrasting responses of photorespiration rate (and thus gross primary productivity) to a future high-[CO2] world. This work enables reconstructing photorespiration rates in the geologic past using fossil wood.

    more » « less
  2. Summary

    Steady‐state photosyntheticCO2responses (A/Cicurves) are used to assess environmental responses of photosynthetic traits and to predict future vegetative carbon uptake through modeling. The recent development of rapidA/Cicurves (RACiRs) permits faster assessment of these traits by continuously changing [CO2] around the leaf, and may reveal additional photosynthetic properties beyond what is practical or possible with steady‐state methods.

    Gas exchange necessarily incorporates photosynthesis and (photo)respiration. Each process was expected to respond on different timescales due to differences in metabolite compartmentation, biochemistry and diffusive pathways. We hypothesized that metabolic lags in photorespiration relative to photosynthesis/respiration andCO2diffusional limitations can be detected by varying the rate of change in [CO2] duringRACiR assays. We tested these hypotheses through modeling and experiments at ambient and 2% oxygen.

    Our data show that photorespiratory delays cause offsets in predictedCO2compensation points that are dependent on the rate of change in [CO2]. Diffusional limitations may reduce the rate of change in chloroplastic [CO2], causing a reduction in apparentRACiR slopes under highCO2ramp rates.

    MultirateRACiRs may prove useful in assessing diffusional limitations to gas exchange and photorespiratory rates.

    more » « less
  3. Abstract

    Photorespiration recovers carbon that would be otherwise lost following the oxygenation reaction of rubisco and production of glycolate. Photorespiration is essential in plants and recycles glycolate into usable metabolic products through reactions spanning the chloroplast, mitochondrion, and peroxisome. Catalase in peroxisomes plays an important role in this process by disproportionating H2O2resulting from glycolate oxidation into O2and water. We hypothesize that catalase in the peroxisome also protects against nonenzymatic decarboxylations between hydrogen peroxide and photorespiratory intermediates (glyoxylate and/or hydroxypyruvate). We test this hypothesis by detailed gas exchange and biochemical analysis ofArabidopsis thalianamutants lacking peroxisomal catalase. Our results strongly support this hypothesis, with catalase mutants showing gas exchange evidence for an increased stoichiometry of CO2release from photorespiration, specifically an increase in the CO2compensation point, a photorespiratory‐dependent decrease in the quantum efficiency of CO2assimilation, increase in the12CO2released in a13CO2background, and an increase in the postillumination CO2burst. Further metabolic evidence suggests this excess CO2release occurred via the nonenzymatic decarboxylation of hydroxypyruvate. Specifically, the catalase mutant showed an accumulation of photorespiratory intermediates during a transient increase in rubisco oxygenation consistent with this hypothesis. Additionally, end products of alternative hypotheses explaining this excess release were similar between wild type and catalase mutants. Furthermore, the calculated rate of hydroxypyruvate decarboxylation in catalase mutant is much higher than that of glyoxylate decarboxylation. This work provides evidence that these nonenzymatic decarboxylation reactions, predominately hydroxypyruvate decarboxylation, can occur in vivo when photorespiratory metabolism is genetically disrupted.

    more » « less
  4. Abstract

    Uncertainty about long‐term leaf‐level responses to atmospheric CO2rise is a major knowledge gap that exists because of limited empirical data. Thus, it remains unclear how responses of leaf gas exchange to elevated CO2(eCO2) vary among plant species and functional groups, or across different levels of nutrient supply, and whether they persist over time for long‐lived perennials. Here, we report the effects of eCO2on rates of net photosynthesis and stomatal conductance in 14 perennial grassland species from four functional groups over two decades in a Minnesota Free‐Air CO2Enrichment experiment, BioCON. Monocultures of species belonging to C3grasses, C4grasses, forbs, and legumes were exposed to two levels of CO2and nitrogen supply in factorial combinations over 21 years. eCO2increased photosynthesis by 12.9% on average in C3species, substantially less than model predictions of instantaneous responses based on physiological theory and results of other studies, even those spanning multiple years. Acclimation of photosynthesis to eCO2was observed beginning in the first year and did not strengthen through time. Yet, contrary to expectations, the response of photosynthesis to eCO2was not enhanced by increased nitrogen supply. Differences in responses among herbaceous plant functional groups were modest, with legumes responding the most and C4grasses the least as expected, but did not further diverge over time. Leaf‐level water‐use efficiency increased by 50% under eCO2primarily because of reduced stomatal conductance. Our results imply that enhanced nitrogen supply will not necessarily diminish photosynthetic acclimation to eCO2in nitrogen‐limited systems, and that significant and consistent declines in stomatal conductance and increases in water‐use efficiency under eCO2may allow plants to better withstand drought.

    more » « less
  5. Abstract

    Bioenergy with carbon capture and storage (BECCS) has been proposed as a potential climate mitigation strategy raising concerns over trade‐offs with existing ecosystem services. We evaluate the feasibility of BECCS in the Upper Missouri River Basin (UMRB), a landscape with diverse land use, ownership, and bioenergy potential. We develop land‐use change scenarios and a switchgrass (Panicum virgatumL.) crop functional type to use in a land‐surface model to simulate second‐generation bioenergy production. By the end of this century, average annual switchgrass production over the UMRB ranges from 60 to 210 Tg dry mass/year and is dependent on the Representative Concentration Pathway for greenhouse gas emissions and on land‐use change assumptions. Under our simple phase‐in assumptions this results in a cumulative total production of 2,000–6,000 Tg C over the study period with the upper estimates only possible in the absence of climate change. Switchgrass yields decreased as average CO2concentrations and temperatures increased, suggesting the effect of elevated atmospheric CO2was small because of its C4 photosynthetic pathway. By the end of the 21st century, the potential energy stored annually in harvested switchgrass averaged between 1 and 4 EJ/year assuming perfect conversion efficiency, or an annual electrical generation capacity of 7,000–28,000 MW assuming current bioenergy efficiency rates. Trade‐offs between bioenergy and ecosystem services were identified, including cumulative direct losses of 1,000–2,600 Tg C stored in natural ecosystems from land‐use change by 2090. Total cumulative losses of ecosystem carbon stocks were higher than the potential ~300 Tg C in fossil fuel emissions from the single largest power plant in the region over the same time period, and equivalent to potential carbon removal from the atmosphere from using biofuels grown in the same region. Numerous trade‐offs from BECCS expansion in the UMRB must be balanced against the potential benefits of a carbon‐negative energy system.

    more » « less