Hernandez, J. S. | Search bioRxiv

bioRxiv2023

Temperature acclimation of photosynthesis and carbohydrate metabolism are related to the geographical origin of Arabidopsis thaliana

Acclimation is a multigenic trait by which plants adjust photosynthesis and metabolism to cope with a changing environment. Here, natural variation of photosynthetic and metabolic acclimation was analyzed in response to low and elevated temperature. For this, 18 natural accessions of Arabidopsis thaliana, originating from Africa and Europe, were grown at 22{degrees}C before being exposed to 4{degrees}C and 34{degrees}C for cold and heat acclimation, respectively. Amounts of carbohydrates were quantified together with their subcellular distribution across plastids, cytosol and vacuole. Linear electron transport rates (ETRs) were determined together with maximum quantum efficiency of photosystem II (Fv/Fm) for all growth conditions and under temperature fluctuation. Under elevated temperature, residuals of ETR under increasing photosynthetic photon flux densities were found to significantly correlate with the longitudinal gradient of the geographic origin of accessions indicating a naturally occurring east-west gradient of photosynthetic acclimation capacities. Further, in heat acclimated plants, vacuolar fructose amount was found to positively correlate with longitude while plastidial and cytosolic amounts were found to be negatively correlated. Plastidial sucrose concentrations were found to positively correlate with maximal ETRs under fluctuating temperature indicating a stabilizing role within the chloroplast. In summary, our findings revealed specific subcellular carbohydrate distributions which contribute differentially to photosynthetic efficiencies of natural Arabidopsis thaliana accessions across a longitudinal gradient. This sheds light on the relevance of subcellular metabolic regulation for photosynthetic performance in a fluctuating environment and supports the physiological interpretation of naturally occurring genetic variation of temperature tolerance and acclimation.

plant biology↗

bioRxiv2022

The trade-off function of photorespiration in a changing environment

The photorespiratory pathway in plants comprises metabolic reactions distributed across several cellular compartments. It emerges from the dual catalytic function of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) which either carboxylates or oxygenates ribulose-1,5-bisphosphate (RuBP). Carboxylation reactions produce 3-phospho-glycerate (3PGA) molecules which are substrate for central carbohydrate metabolism while oxygenation forms 2-phosphoglycolate (2PG) molecules which are substrate for the multicompartmental recovery process of photorespiration. Further, 2PG is a strong inhibitor of several enzymes involved in the Calvin-Benson-Bassham cycle which challenges the experimental and theoretical study of carbon assimilation, photorespiration and metabolic regulation in vivo. Here, an approach of structural kinetic modeling (SKM) is presented to investigate the extend of stabilization of CBC and carbohydrate metabolism by photorespiration. Further, our approach highlights the importance of feedback regulation by 2-PG for alleviation of environmental perturbation. Our findings indicate that oxygenation of RuBP by Rubisco significantly stabilizes CBC activity and, thus, carbohydrate metabolism. Based on our findings, we suggest a trade-off function of photorespiration which reduces carbon assimilation rates but simultaneously stabilizes metabolism by increasing plasticity of metabolic regulation within the chloroplast. Furthermore, our analysis suggests a stabilizing effect of increasing the partition of newly assimilated carbon going towards sucrose biosynthesis. With this, our analysis sheds light on the role of a multicompartmental metabolic pathway in stabilizing plant metabolism within a changing environment.

plant biology↗