The Science
Thermotolerance mechanisms that protect photosynthesis during heat stress are not well understood. CO2 fixation and production only provide part of the story. O2 production, electron transport, and lipid synthesis provide important mechanistic information on thermal optima. This study developed a novel method to simultaneously measure net oxygen production (NOP) and isoprene emissions in poplar leaves during photosynthesis under varying environmental conditions.
The Findings
The findings provide a comprehensive view of how light, CO2 and temperature affect the photosynthetic redox budget, revealing key insights into how these variables influence ATP/NADPH utilization and thermotolerance mechanisms in plants including CO2 and O2 recycling and lipid synthesis.
The Impact
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In this study, we present the first coupled observations of leaf net CO2 assimilation (Anet), net oxygen production (NOP), δ18O in O2 and isoprene emissions together with traditional CO2/H2O gas exchange fluxes allowing estimates of ETR and the assimilatory quotient (AQ = Anet/NOP).
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The results confirm a tight connection between water oxidation and ETR and support a model where light-dependent lipid synthesis is primarily driven by photosynthetic ATP/NADPH not consumed by the Calvin-Benson cycle, as an important thermotolerance mechanism linked with high rates of (photo)respiration and CO2/O2 recycling.
Summary
Our study shows that coupling O2 and isoprene exchange to traditional CO2/H2O gas exchange is possible, using cavity ringdown spectroscopy (O2) and proton transfer-reaction mass spectrometery (isoprene). This configuration allows a more complete picture of the photosynthetic redox budget via photosynthetic production of O2, electron transport rate (ETR), and isoprene biosynthesis. This opens avenues for useful measurements during photosynthesis, such as the temperature sensitivity of gross oxygen production (GOP) using 18O-water labeling, and the assimilatory quotient (AQ) which appears to be suppressed at high leaf temperature. Also, our findings may help resolve some confusion in the literature as to whether isoprene emissions and perhaps lipid synthesis in chloroplasts in general, may or may not be directly linked to net photosynthesis. In agreement with numerous previous studies, we found that isoprene emission can be uncoupled from Anet, i.e., at low Ci and high temperature, and thus it is unlikely that lipid biosynthesis in chloroplasts strictly depends on photosynthesis rate or carbon provision by photosynthates. Therefore, our results suggest that (i) isoprene synthesis (and potentially lipid synthesis in general) in chloroplasts is related to electron generation by photolysis and thus probably via excess photosynthetic ATP/NADPH (not consumed by the Calvin cycle, the photorespiratory cycle, and other pathways acting in parallel like the malate/oxaloacetate shuttle), and (ii) is carbon-limited only when gross photosynthesis declines considerably. The results confirm a tight connection between water oxidation and ETR and support a view of light-dependent lipid synthesis primarily driven by photosynthetic ATP/NADPH not consumed by the Calvin-Benson cycle, as an important thermotolerance mechanism linked with high rates of (photo)respiration and CO2/O2 recycling. Simplified metabolic model of primary CO2 and O2 metabolism at elevated leaf temperatures (e.g. 35 ºC) in poplar leaves (accelerated metabolism). Elevated temperature leads to a suppression of stomatal conductance (gs), net oxygen production (NOP), and net atmospheric CO2 uptake (Anet) and a stimulation of photosynthesis, (photo)respiration, and internal CO2/O2 recycling and isoprenoid synthesis consuming ATP/NADPH. Note the activity of the water-water cycle is depicted as the cycling between O2 and H2O2.
Contact
Dr. Kolby Jeremiah Jardine
Climate and Ecosystem Sciences Division
Lawrence Berkeley National Laboratory
Email: kjjardine@lbl.gov
Funding
This research was supported by the U.S. Department of Energy (DOE) Office of Science, Office of Biological and Environmental Research (BER), Biological System Science Division (BSSD), Early Career Research Program under Award number FP00007421. Additional support was provided by the Next Generation Ecosystem Experiments-Tropics (NGEE-Tropics) through contract No. DE-AC02-05CH11231.
Publications
Jardine KJ, Som S, Gallo LB, Demus J, Domingues TF, Wistrom CM, Gu L, Tcherkez G, Niinemets Ü. Concurrent Measurement of O2 Production and Isoprene Emission During Photosynthesis: Pros, Cons and Metabolic Implications of Responses to Light, CO2 and Temperature. Plant, cell & environment. 2024.