Photorespiratory Bypasses Lead to Increased Growth in Arabidopsis thaliana: Are Predictions Consistent with Experimental Evidence?

Georg Basler, Anika Küken, Alisdair R. Fernie, Zoran Nikoloski

Arguably, the biggest challenge of modern plant systems biology lies in predicting the performance of plant species, and crops in particular, upon different intracellular and external perturbations. Recently, an increased growth of Arabidopsis thaliana plants was achieved by introducing two different photorespiratory bypasses via metabolic engineering. Here, we investigate the extent to which these findings match the predictions from constraint-based modeling. To determine the effect of the employed metabolic network model on the predictions, we perform a comparative analysis involving three state-of-the-art metabolic reconstructions of A. thaliana. In addition, we investigate three scenarios with respect to experimental findings on the ratios of the carboxylation and oxygenation reactions of Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO). We demonstrate that the condition-dependent growth phenotypes of one of the engineered bypasses can be qualitatively reproduced by each reconstruction, particularly upon considering the additional constraints with respect to the ratio of fluxes for the RuBisCO reactions. Moreover, our results lend support for the hypothesis of a reduced photorespiration in the engineered plants, and indicate that specific changes in CO2 exchange as well as in the proxies for co-factor turnover are associated with the predicted growth increase in the engineered plants. We discuss our findings with respect to the structure of the used models, the modeling approaches taken, and the available experimental evidence. Our study sets the ground for investigating other strategies for increase of plant biomass by insertion of synthetic reactions.