Evolutionary implications of C2photosynthesis: How complex biochemical trade-offs may limit C4evolution

Abstract

The C2carbon-concentrating mechanism increases net CO2assimilation by shuttling photorespiratory CO2in the form of glycine from mesophyll to bundle sheath cells, where CO2concentrates and can be re-Assimilated. This glycine shuttle also releases NH3and serine into the bundle sheath, and modelling studies suggest that this influx of NH3may cause a nitrogen imbalance between the two cell types that selects for the C4carbon-concentrating mechanism. Here we provide an alternative hypothesis outlining mechanisms by which bundle sheath NH3and serine play vital roles to not only influence the status of C2plants along the C3to C4evolutionary 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 C2photosynthesis is typically cited for its intermediary role in C4photosynthesis evolution, our alternative hypothesis provides a mechanism to explain why some C2lineages have not made this transition. We propose that stress resilience, coupled with open flux tricarboxylic acid and photorespiration pathways, conveys an advantage to C2plants in fluctuating environments. © 2022 The Author(s). Published by Oxford University Press on behalf of the Society for Experimental Biology.