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

Abstract

Summary-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.-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.-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.-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.

Optimal coordination and reorganization of photosynthetic properties in C4 grasses

“…Our modelling efforts provide an explanation for the observed variation in J atpmax / V cmax and V pmax / V cmax , and why V pmax / V cmax in C 4 appears to be optimized for the lower bounds of atmospheric CO 2 of the Pleistocene (~200 ppm) (Figure 3, Supporting Information: Figure and ). Our reported values of V pmax / V cmax are comparable with previous studies (Kubien et al, 2003; Pengelly et al, 2010; Pignon & Long, 2020; Yin et al, 2016), and two recent papers also indicated that the coordination between CB and C 4 cycles is more appropriate for low CO 2 conditions (Pignon & Long, 2020; Sundermann et al, 2018). All extant C 4 species have gone through a low CO 2 bottleneck over the last 5 million years (Edwards et al, 2010).…”

“…Figure S5 and S8). Our reported values of V pmax /V cmax are comparable with previous studies (Kubien et al, 2003;Pengelly et al, 2010;Pignon & Long, 2020;Yin et al, 2016), and two recent papers also indicated that the coordination between CB and C 4 cycles is more appropriate for low CO 2 conditions (Pignon & Long, 2020;Sundermann et al, 2018). All extant C 4 species have gone through a low CO 2 bottleneck over the last 5 million years…”

Optimal coordination and reorganization of photosynthetic properties in C4grasses

“…Our modeling efforts provide an explanation for the observed variation in J max / V cmax and V pmax / V cmax , and why V pmax / V cmax appears to be optimized for the lower bounds of atmospheric CO 2 of the Pleistocene. Our reported value of V pmax / V cmax are comparable with previous studies (Kubien et al , 2003; Pengelly et al , 2010; Yin et al ,2011, 2016; Pignon and Long, 2020), and two recent papers also indicated that the coordination between CB and C 4 cycles might represent a legacy of ancient low CO 2 conditions (Sundermann et al, 2018; Pignon and Long, 2020). All extant C 4 species have gone through a low CO 2 bottleneck over the last 5 million years (Edwards et al, 2010).…”