Evolution of C4 photosynthesis predicted by constraint-based modelling.

Mary-Ann Blätke,Andrea Bräutigam

doi:10.7554/elife.49305

Abstract

Constraint-based modelling (CBM) is a powerful tool for the analysis of evolutionary trajectories. Evolution, especially evolution in the distant past, is not easily accessible to laboratory experimentation. Modelling can provide a window into evolutionary processes by allowing the examination of selective pressures which lead to particular optimal solutions in the model. To study the evolution of C4 photosynthesis from a ground state of C3 photosynthesis, we initially construct a C3 model. After duplication into two cells to reflect typical C4 leaf architecture, we allow the model to predict the optimal metabolic solution under various conditions. The model thus identifies resource limitation in conjunction with high photorespiratory flux as a selective pressure relevant to the evolution of C4. It also predicts that light availability and distribution play a role in guiding the evolutionary choice of possible decarboxylation enzymes. The data shows evolutionary CBM in eukaryotes predicts molecular evolution with precision.

Highlights

Identifying specific evolutionary trajectories and modelling the outcome of adaptive strategies at the molecular levels is a major challenge in evolutionary systems biology Papp et al (2011)
We hypothesised that the evolution of the agriculturally important trait of C4 photosynthesis is accessible to constraint-based modelling (CBM)
To analyse evolution towards C4 photosynthesis based on C3 metabolism, a CBM of C3 metabolism is required (Figure 1)

Summary

Introduction

Identifying specific evolutionary trajectories and modelling the outcome of adaptive strategies at the molecular levels is a major challenge in evolutionary systems biology Papp et al (2011). The evolution of novel metabolic pathways from existing parts may be predicted using constraint-based modelling (CBM) Orth et al (2010). In CBM, selective pressures are coded via the objective functions for which the model is optimised. The factors which constrain evolution are integrated into the models via changes in model inputs or outputs and via flux constraints. We hypothesised that the evolution of the agriculturally important trait of C4 photosynthesis is accessible to CBM. The C4 cycle acts as a biochemical pump which enriches the CO2 concentration at the site of Rubisco to overcome a major limitation of carbon fixation Sage (2004).

Methods

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Discussion

Conclusion