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The Coevolution of RuBisCO, Photorespiration, and Carbon Concentrating Mechanisms in Higher Plants.

ABSTRACT: Ribulose-1,5-bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO) is the carbon-fixing enzyme present in most photosynthetic organisms, converting CO₂ into organic matter. Globally, photosynthetic efficiency in terrestrial plants has become increasingly challenged in recent decades due to a rapid increase in atmospheric CO₂ and associated changes toward warmer and dryer environments. Well adapted for these new climatic conditions, the C₄ photosynthetic pathway utilizes carbon concentrating mechanisms to increase CO₂ concentrations surrounding RuBisCO, suppressing photorespiration from the oxygenase catalyzed reaction with O₂. The energy efficiency of C₃ photosynthesis, from which the C₄ pathway evolved, is thought to rely critically on an uninterrupted supply of chloroplast CO₂. Part of the homeostatic mechanism that maintains this constancy of supply involves the CO₂ produced as a byproduct of photorespiration in a negative feedback loop. Analyzing the database of RuBisCO kinetic parameters, we suggest that in genera (Flaveria and Panicum) for which both C₃ and C₄ examples are available, the C₄ pathway evolved only from C₃ ancestors possessing much lower than the average carboxylase specificity relative to that of the oxygenase reaction (S _C/O=S _C/S _O), and hence, the higher CO₂ levels required for development of the photorespiratory CO₂ pump (C₂ photosynthesis) essential in the initial stages of C₄ evolution, while in the later stage (final optimization phase in the Flaveria model) increased CO₂ turnover may have occurred, which would have been supported by the higher CO₂ levels. Otherwise, C₄ RuBisCO kinetic traits remain little changed from the ancestral C₃ species. At the opposite end of the spectrum, C₃ plants (from Limonium) with higher than average S _C/O, which may be associated with the ability of increased CO₂, relative to O₂, affinity to offset reduced photorespiration and chloroplast CO₂ levels, can tolerate high stress environments. It is suggested that, instead of inherently constrained by its kinetic mechanism, RuBisCO possesses the extensive kinetic plasticity necessary for adaptation to changes in photorespiration that occur in the homeostatic regulation of CO₂ supply under a broad range of abiotic environmental conditions.

SUBMITTER: Cummins PL

PROVIDER: S-EPMC8440988 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Seaweeds that lack carbon-concentrating mechanisms are potentially inorganic carbon-limited under current air equilibrium conditions. To estimate effects of increased atmospheric carbon dioxide concentration and ocean acidification on photosynthetic rates, we modeled rates of photosynthesis in response to pCO2, temperature, and their interaction under limiting and saturating photon flux densities. We synthesized the available data for photosynthetic responses of red seaweeds lacking carbon-concentrating mechanisms to light and temperature. The model was parameterized with published data and known carbonate system dynamics. The model predicts that direction and magnitude of response to pCO2 and temperature, depend on photon flux density. At sub-saturating light intensities, photosynthetic rates are predicted to be low and respond positively to increasing pCO2, and negatively to increasing temperature. Consequently, pCO2 and temperature are predicted to interact antagonistically to influence photosynthetic rates at low PFD. The model predicts that pCO2 will have a much larger effect than temperature at sub-saturating light intensities. However, photosynthetic rates under low light will not increase proportionately as pCO2 in seawater continues to rise. In the range of light saturation (Ik), both CO2 and temperature have positive effects on photosynthetic rate and correspondingly strong predicted synergistic effects. At saturating light intensities, the response of photosynthetic rates to increasing pCO2 approaches linearity, but the model also predicts increased importance of thermal over pCO2 effects, with effects acting additively. Increasing boundary layer thickness decreased the effect of added pCO2 and, for very thick boundary layers, overwhelmed the effect of temperature on photosynthetic rates. The maximum photosynthetic rates of strictly CO2-using algae are low, so even large percentage increases in rates with climate change will not contribute much to changing primary production in the habitats where they commonly live.

Dataset Information

The Coevolution of RuBisCO, Photorespiration, and Carbon Concentrating Mechanisms in Higher Plants.

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