Respiration in the light (RL) releases CO2 in photosynthesizing leaves and is a phenomenon that occurs independently from photorespiration. Since RL lowers net carbon fixation, understanding RL could help improve plant carbon-use efficiency and models of crop photosynthesis. Although RL was identified more than 75 years ago, its biochemical mechanisms remain unclear. To identify reactions contributing to RL, we mapped metabolic fluxes in photosynthesizing source leaves of the oilseed crop and model plant camelina (Camelina sativa). We performed a flux analysis using isotopic labeling patterns of central metabolites during 13CO2 labeling time course, gas exchange and carbohydrate production rate experiments. To quantify the contributions of multiple potential CO2 sources with statistical and biological confidence, we increased the number of metabolites measured and reduced biological and technical heterogeneity by using single mature source leaves and quickly quenching metabolism by directly injecting liquid N2; we then compared the goodness-of-fit between these data and data from models with alternative metabolic network structures and constraints. Our analysis predicted that RL releases 5.2 μmol CO2 g−1 FW hr−1 of CO2, which is relatively consistent with a value of 9.3 μmol CO2 g−1 FW hr−1 measured by CO2 gas exchange. The results indicated that ≤10% of RL results from TCA cycle reactions, which are widely considered to dominate RL. Further analysis of the results indicated that oxidation of glucose-6-phosphate to pentose phosphate via 6-phosphogluconate (the G6P/OPP shunt) can account for >93% of CO2 released by RL.
Given their ability to harness chemical energy from the sun and generate the organic compounds necessary for life, photosynthetic organisms have the unique capacity to act simultaneously as their own power and manufacturing plant. This dual capacity presents many unique challenges, chiefly that energy supply must be perfectly balanced with energy demand to prevent photodamage and allow for optimal growth. From this perspective, we discuss the energy balancing network using recent studies and a quantitative framework for calculating metabolic ATP and NAD(P)H demand using measured leaf gas exchange and assumptions of metabolic demand. We focus on exploring how the energy balancing network itself is structured to allow safe and flexible energy supply. We discuss when the energy balancing network appears to operate optimally and when it favors high capacity instead. We also present the hypothesis that the energy balancing network itself can adapt over longer time scales to a given metabolic demand and how metabolism itself may participate in this energy balancing.
The metabolic intermediate acetyl-CoA links anabolic and catabolic processes and coordinates metabolism with cellular signaling by influencing protein acetylation. In this study we demonstrate that in Arabidopsis (Arabidopsis thaliana), two distinctly localized acetate-activating enzymes, ACETYL-COA SYNTHETASE (ACS) in plastids and ACETATE NON-UTILIZING1 (ACN1) in peroxisomes, function redundantly to prevent the accumulation of excess acetate. In contrast to the near wild-type morphological and metabolic phenotypes of acs or acn1 mutants, the acs acn1 double mutant is delayed in growth and sterile, which is associated with hyperaccumulation of cellular acetate and decreased accumulation of acetyl-CoA-derived intermediates of central metabolism. Using multiple mutant stocks and stable isotope-assisted metabolic analyses, we demonstrate the twin metabolic origins of acetate from the oxidation of ethanol and the nonoxidative decarboxylation of pyruvate, with acetaldehyde being the common intermediate precursor of acetate. Conversion from pyruvate to acetate is activated under hypoxic conditions, and ACS recovers carbon that would otherwise be lost from the plant as ethanol. Plastid-localized ACS metabolizes cellular acetate and contributes to the de novo biosynthesis of fatty acids and Leu; peroxisome-localized ACN1 enables the incorporation of acetate into organic acids and amino acids. Thus, the activation of acetate in distinct subcellular compartments provides plants with the metabolic flexibility to maintain physiological levels of acetate and a metabolic mechanism for the recovery of carbon that would otherwise be lost as ethanol, for example following hypoxia.
Abiotic stresses rewire plant central metabolism to maintain metabolic and energy homeostasis. Metabolites involved in the plant central metabolic network serve as a hub for regulating carbon and energy metabolism under various stress conditions. In this review, we introduce recent metabolomics techniques used to investigate the dynamics of metabolic responses to abiotic stresses and analyze the trend of publications in this field. We provide an updated overview of the changing patterns in central metabolic pathways related to the metabolic responses to common stresses, including flooding, drought, cold, heat, and salinity. We extensively review the common and unique metabolic changes in central metabolism in response to major abiotic stresses. Finally, we discuss the challenges and some emerging insights in the future application of metabolomics to study plant responses to abiotic stresses.
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