Modeling Cellular Resource Allocation Reveals Low Phenotypic Plasticity of C4 Plants and Infers Environments of C4 Photosynthesis Evolution

Abstract

- The regulation of resource allocation in biological systems observed today is the cumulative result of natural selection in ancestral and recent environments. To what extent are observed resource allocation patterns in different photosynthetic types optimally adapted to current conditions, and to what extend do they reflect ancestral environments? Here, we explore these questions for C3, C4, and C3-C4 intermediate plants of the model genus Flaveria.\n- We developed a detailed mathematical model of carbon fixation, which accounts for various environmental parameters and for energy and nitrogen partitioning across photosynthetic components. This allows us to assess environment-dependent plant physiology and performance as a function of resource allocation patterns.\n- To achieve maximal CO2 fixation rates under growth conditions differing from those experienced during their evolution, C4 species need to re-allocate significantly more nitrogen between photosynthetic components than their C3 relatives. As this is linked to a limited phenotypic plasticity, observed resource distributions in C4 plants still reflect optimality in ancestral environments, allowing their quantitative inference.\n- Our work allows us to quantify environmental effects on resource allocation and performance of photosynthetic organisms. This understanding paves the way for interpreting present photosynthetic physiology in the light of evolutionary history.