Three distinct biochemical subtypes of C ₄ photosynthesis? A modelling analysis

Summary

Only two distinct C ₄ subtypes exist: the NADP-malic enzyme and NAD-malic enzyme subtypes. Both inherently involve a supplementary phosphoenolpyruvate carboxykinase cycle, which affords increased metabolic flexibility and robustness under diverse environments.

Abstract

C ₄ photosynthesis has higher light-use, nitrogen-use, and water-use efficiencies than C ₃ photosynthesis. Historically, most of C ₄ plants were classified into three subtypes (NADP-malic enzyme (ME), NAD-ME, or phosphoenolpyruvate carboxykinase (PEPCK) subtypes) according to their major decarboxylation enzyme. However, a wealth of historic and recent data indicates that flexibility exists between different decarboxylation pathways in many C ₄ species, and this flexibility might be controlled by developmental and environmental cues. This work used systems modelling to theoretically explore the significance of flexibility in decarboxylation mechanisms and transfer acids utilization. The results indicate that employing mixed C ₄ pathways, either the NADP-ME type with the PEPCK type or the NAD-ME type with the PEPCK type, effectively decreases the need to maintain high concentrations and concentration gradients of transport metabolites. Further, maintaining a mixture of C ₄ pathways robustly affords high photosynthetic efficiency under a broad range of light regimes. A pure PEPCK-type C ₄ photosynthesis is not beneficial because the energy requirements in bundle sheath cells cannot be fulfilled due to them being shaded by mesophyll cells. Therefore, only two C ₄ subtypes should be considered as distinct subtypes, the NADP-ME type and NAD-ME types, which both inherently involve a supplementary PEPCK cycle.