Combining Kinetic and Constraint-Based Models to Predict Evolution of a Complex Photosynthetic Trait

Background: Understanding how the complex traits we observe in everyday life evolved is still a major challenge in evolutionary biology. C₄ photosynthesis constitutes a complex add-on to C₃ photosynthesis that involves the interplay of leaf anatomy, differential gene expression and specialized biochemistry. Despite its complexity, C₄ photosynthesis has more than 60 independent evolutionary origins. Phylogenetic analyses indicate that the carbon scavenging mechanism termed C₂ photosynthesis is a prerequisite for C₄ evolution. Although our recent modelling work indicates an important role early in C₄ evolution (1), the mechanism of how C₂ photosynthesis increases the probability of C₄ evolution is still unknown.

Method & Results: In order to understand the role of C₂ photosynthesis during C₄ evolution, we coupled a mechanistic kinetic model of C₂ photosynthesis with a multicellular genome-scale stoichiometric model (2). Flux balance analysis revealed intercellular shuttles of nitrogen that utilize components of the C₄ cycle. Furthermore, when the C₄ cycle is assumed to co-occur with C₂ photosynthesis, the cycles are predicted to overlap. Transcript and protein data from C₂ plants confirm the existence of the proposed shuttles.

Conclusion: We thus conclude that C₂ photosynthesis requires nitrogen shuttles that serve as a pre-adaptation for the C₄ cycle. This provides a novel example of how systems modelling of non-model species metabolism can be applied to better understand the non-intuitive evolution of complex traits.

References

1.         D. Heckmann et al., Predicting C₄ Photosynthesis Evolution: Modular, Individually Adaptive Steps on a Mount Fuji Fitness Landscape. Cell 153, 1579-1588 (2013).

2.         J. Mallmann and D. Heckmann et al., The role of photorespiration during the evolution of C₄ photosynthesis in the genus Flaveria. eLife 10.7554/eLife.02478,  (2014).