Evolution of C4 photosynthesis predicted by constraint-based modelling

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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.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. We provide jupyter notebooks as documentation for all the in silico experiments using constraint-based modelling and additional python code for Figure 1, 3, 4, 6, as well as the metabolic network used as source data for Figure 1 which can be accessed and executed from the GitHub repository https://github.com/512 ma-blaetke/CBM_C3_C4_Metabolism

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Mary-Ann Blätke

Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland OT Gatersleben, Germany

For correspondence
blaetke@ipk-gatersleben.de

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-4790-7377
Andrea Bräutigam

Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), Seeland OT Gatersleben, Germany

Competing interests
The authors declare that no competing interests exist.

Funding

The authors declare that there was no funding for this work.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.