Evolutionary implications of C2 photosynthesis: how complex biochemical trade-offs may limit C4 evolution

The C-2 carbon-concentrating mechanism increases net CO2 assimilation by shuttling photorespiratory CO2 in the form of glycine from mesophyll to bundle sheath cells, where CO2 concentrates and can be re-assimilated. This glycine shuttle also releases NH3 and serine into the bundle sheath, and modelling studies suggest that this influx of NH3 may cause a nitrogen imbalance between the two cell types that selects for the C-4 carbon-concentrating mechanism. Here we provide an alternative hypothesis outlining mechanisms by which bundle sheath NH3 and serine play vital roles to not only influence the status of C-2 plants along the C-3 to C-4 evolutionary trajectory, but to also convey stress tolerance to these unique plants. Our hypothesis explains how an optimized bundle sheath nitrogen hub interacts with sulfur and carbon metabolism to mitigate the effects of high photorespiratory conditions. While C-2 photosynthesis is typically cited for its intermediary role in C-4 photosynthesis evolution, our alternative hypothesis provides a mechanism to explain why some C-2 lineages have not made this transition. We propose that stress resilience, coupled with open flux tricarboxylic acid and photorespiration pathways, conveys an advantage to C-2 plants in fluctuating environments. An alternative theory for bundle sheath ammonia tolerance in C(2)species suggests that C(2)to C(4)evolutionary transitions may depend on bundle sheath nitrogen hub optimization.

Automated summary

The C-2 carbon-concentrating mechanism increases CO2 assimilation by shuttling photorespiratory CO2 from mesophyll to bundle sheath cells. NH3 influx caused by this mechanism may lead to nitrogen imbalance and select for C-4 mechanism. Our alternative hypothesis explains the vital roles of bundle sheath NH3 and serine in C-2 plants and their stress tolerance. Optimized bundle sheath nitrogen hub interacts with sulfur and carbon metabolism to mitigate the effects of high photorespiratory conditions.