Format: ORAL

Roberts, H.R., Rumble, G., Worall, D.,Hernandez-Verdeja, T.,Lundgren, M.R.

Lancaster Environment Centre, Lancaster University, Bailrigg, Lancaster LA1 4YQ, UK.

Most plants use only C3 photosynthesis, which endures high rates of metabolically costly photorespiration under elevated temperatures and dry conditions. However, several plant lineages convergently evolved carbon concentrating mechanisms (CCM; e.g., C4) to help avoid these photorespiratory costs and consequently boost photosynthetic efficiency under these stressful environments. During the repeated evolutionary transitions from the ancestral C3 to complex C4 CCM, evolutionary intermediate C3-C4 states arose, many of which use a rare physiology called C2 photosynthesis. The C2 CCM is a natural CO2 recycling mechanism that shuttles the photorespiratory product glycine from mesophyll into bundle sheath cells, where it releases, concentrates, and reassimilates the CO2 released from photorespiration. Engineering the C2 CCM into C3 crops shows promise to increase crop yields, especially under climate change, but achieving this requires a detailed understanding of the complete C2phenotype across scales, from the sub-cellular to whole-plant. To comprehensively characterise the C2 phenotype across diverse plant lineages, we quantified ultrastructure, organelle content, and biochemistry of mesophyll vs bundle sheath cells, leaf structure, relative growth rate, whole plant resource allocation, root characteristics, drought responses, leaf gas exchange in C2plants compared with their close C3 relatives from six plant lineages. C2 species showed several clear benefits compared to their C3 relatives under the experimental conditions, including greater biomass, leaf area, and intrinsic water use efficiency, as well as many other phenotypic differences compared to their C3 counterparts. Our findings clarify the phenotypic changes that accompanied the repeated evolution of C2 phenotypes in diverse plant lineages, providing critical information needed engineering the C2 photosynthetic pathway into C3 crops to achieve food security now and into the future.