Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis.

Yu Wang,Andrea Bräutigam,Xin-Guang Zhu,Andreas P M Weber

doi:10.1093/jxb/eru058

Abstract

C4 photosynthesis has higher light-use, nitrogen-use, and water-use efficiencies than C3 photosynthesis. Historically, most of C4 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 C4 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 C4 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 C4 pathways robustly affords high photosynthetic efficiency under a broad range of light regimes. A pure PEPCK-type C4 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 C4 subtypes should be considered as distinct subtypes, the NADP-ME type and NAD-ME types, which both inherently involve a supplementary PEPCK cycle.

Highlights

Plants using C4 photosynthesis have higher potential energy-conversion efficiency than C3 plants because of a CO2-concentrating mechanism that largely reduces photorespiration (Zhu et al, 2008; Amthor, 2010)
The results indicate that employing mixed C4 pathways, either the NADP-malic enzyme (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
Can the PEPCK pathway exists in isolation: i.e. is there a C4 photosynthetic subtype where no NAD-ME or NADP-ME exists at all? Analysis from this study showed that photosystem II in bundle sheath cells (BSCs) is essential for a pure PEPCK C4 photosynthetic pathway that uses only PEPCK as the decarboxylase and only aspartate as the C4 transfer acid from mesophyll cells (MCs) to BSCs (Fig. 7)

Summary

Introduction

Plants using C4 photosynthesis have higher potential energy-conversion efficiency than C3 plants because of a CO2-concentrating mechanism that largely reduces photorespiration (Zhu et al, 2008; Amthor, 2010). With the exception of single-cell C4 photosynthesis (Edwards et al, 2004), this CO2-concentrating mechanism usually requires compartmentalized photosynthetic reactions into two distinct cell types: bundle sheath cells (BSCs) and mesophyll cells (MCs) (Hatch, 1987). Decarboxylation in BSCs, together with the CO2 diffusion barrier between BSCs and MCs, elevates the CO2 concentration around Rubisco, thereby minimizing photorespiration (von Caemmerer and Furbank, 2003).

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