Systematic Comparison of C3 and C4 Plants Based on Metabolic Network Analysis

Zhuo Wang,Yixue Li,Longyun Guo,Chuanli Wang

doi:10.1186/1752-0509-6-s2-s9

Abstract

BackgroundThe C4 photosynthetic cycle supercharges photosynthesis by concentrating CO2 around ribulose-1,5-bisphosphate carboxylase and significantly reduces the oxygenation reaction. Therefore engineering C4 feature into C3 plants has been suggested as a feasible way to increase photosynthesis and yield of C3 plants, such as rice, wheat, and potato. To identify the possible transition from C3 to C4 plants, the systematic comparison of C3 and C4 metabolism is necessary.ResultsWe compared C3 and C4 metabolic networks using the improved constraint-based models for Arabidopsis and maize. By graph theory, we found the C3 network exhibit more dense topology structure than C4. The simulation of enzyme knockouts demonstrated that both C3 and C4 networks are very robust, especially when optimizing CO2 fixation. Moreover, C4 plant has better robustness no matter the objective function is biomass synthesis or CO2 fixation. In addition, all the essential reactions in C3 network are also essential for C4, while there are some other reactions specifically essential for C4, which validated that the basic metabolism of C4 plant is similar to C3, but C4 is more complex. We also identified more correlated reaction sets in C4, and demonstrated C4 plants have better modularity with complex mechanism coordinates the reactions and pathways than that of C3 plants. We also found the increase of both biomass production and CO2 fixation with light intensity and CO2 concentration in C4 is faster than that in C3, which reflected more efficient use of light and CO2 in C4 plant. Finally, we explored the contribution of different C4 subtypes to biomass production by setting specific constraints.ConclusionsAll results are consistent with the actual situation, which indicate that Flux Balance Analysis is a powerful method to study plant metabolism at systems level. We demonstrated that in contrast to C3, C4 plants have less dense topology, higher robustness, better modularity, and higher CO2 and radiation use efficiency. In addition, preliminary analysis indicated that the rate of CO2 fixation and biomass production in PCK subtype are superior to NADP-ME and NAD-ME subtypes under enough supply of water and nitrogen.

Highlights

The C4 photosynthetic cycle supercharges photosynthesis by concentrating CO2 around ribulose-1,5bisphosphate carboxylase and significantly reduces the oxygenation reaction
Some important topological parameters such as average degree, betweenness centrality, average clustering coefficient and distance were compared between these two models, as shown in Table 1.The results demonstrated that the AraGEM has a more dense structure than C4GEM, because C3 plant is single-cell, while C4 plant consists of mesophyll cell and bundle sheath cell, the connections between two-cells are not as close as single-cell
To realize the transition from C3 to C4, systems biology will play a critical role in many aspects, including identification of key regulatory elements controlling development of C4 features and viable routine towards C4 using constraint-based modeling approach [47]

Summary

Introduction

The C4 photosynthetic cycle supercharges photosynthesis by concentrating CO2 around ribulose-1,5bisphosphate carboxylase and significantly reduces the oxygenation reaction. Engineering C4 feature into C3 plants has been suggested as a feasible way to increase photosynthesis and yield of C3 plants, such as rice, wheat, and potato. C4 plants such as maize, sorghum, and sugarcane, approximately have 50% higher photosynthesis efficiency than those of C3 plants such as rice, wheat, and potato [1]. The CO2 concentration mechanism suppresses the oxygenation reaction by Rubisco and the subsequent energy-wasteful photorespiratory pathway, resulting in increased photosynthetic yield and more efficient use of water and nitrogen comparing to C3 plants [2]. Genetic manipulations rarely cause the predicted effects, and new rate-limiting steps prevent the accumulation of some desired compounds [6,7]

Methods

Results

Conclusion