Evolutionary implications of C(2) photosynthesis: how complex biochemical trade-offs may limit C(4) evolution

The C(2) carbon-concentrating mechanism increases net CO(2) assimilation by shuttling photorespiratory CO(2) in the form of glycine from mesophyll to bundle sheath cells, where CO(2) concentrates and can be re-assimilated. This glycine shuttle also releases NH(3) and serine into the bundle sheath, and modelling studies suggest that this influx of NH(3) 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 NH(3) 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.