title: Three distinct biochemical subtypes of C4 photosynthesis? A modelling analysis.
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.
authors.affiliation: State Key Laboratory for Hybrid Rice, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China.
authors.forename: Yu
authors.initials: Y
authors.lastname: Wang
authors.affiliation: Institute of Plant Biochemistry, Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine University, 40225 Düsseldorf, Germany.
authors.forename: Andrea
authors.initials: A
authors.lastname: Bräutigam
authors.affiliation: Institute of Plant Biochemistry, Cluster of Excellence on Plant Sciences (CEPLAS), Heinrich-Heine University, 40225 Düsseldorf, Germany zhuxinguang@picb.ac.cn andreas.weber@uni-duesseldorf.de.
authors.forename: Andreas P M
authors.initials: AP
authors.lastname: Weber
authors.affiliation: State Key Laboratory for Hybrid Rice, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China Key Laboratory of Computational Biology, CAS-MPG Partner Institute for Computational Biology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China zhuxinguang@picb.ac.cn andreas.weber@uni-duesseldorf.de.
authors.forename: Xin-Guang
authors.initials: XG
authors.lastname: Zhu
mesh_terms: D002244:Carbon / Q000378:metabolism; D002245:Carbon Dioxide / Q000378:metabolism*; D019069:Cell Respiration; D008027:Light; D008291:Malate Dehydrogenase; D058503:Mesophyll Cells; D008962:Models, Theoretical; D009584:Nitrogen / Q000378:metabolism; D019764:Phosphoenolpyruvate Carboxykinase (ATP); D010730:Phosphoenolpyruvate Carboxylase / Q000378:metabolism; D010788:Photosynthesis; D018515:Plant Leaves / Q000378:metabolism / Q000528:radiation effects; D010940:Plant Proteins / Q000378:metabolism*; D010944:Plants / Q000378:metabolism* / Q000528:radiation effects
chemical_list: D010940:Plant Proteins; D002245:Carbon Dioxide; D002244:Carbon; D008291:Malate Dehydrogenase; C046446:malate dehydrogenase-(oxaloacetate-decarboxylating) (NAD+); C031917:malate dehydrogenase (oxaloacetate-decarboxylating) (NADP+); D010730:Phosphoenolpyruvate Carboxylase; D019764:Phosphoenolpyruvate Carboxykinase (ATP); D009584:Nitrogen
keywords: Efficiency; NAD-ME; NADP-ME; PEPCK.; flexibility; mixture