Abstract
C4 plants, such as maize, concentrate carbon dioxide in a specialized compartment surrounding the veins of their leaves to improve the efficiency of carbon dioxide assimilation. Nonlinear relationships between carbon dioxide and oxygen levels and reaction rates are key to their physiology but cannot be handled with standard techniques of constraint-based metabolic modeling. We demonstrate that incorporating these relationships as constraints on reaction rates and solving the resulting nonlinear optimization problem yields realistic predictions of the response of C4 systems to environmental and biochemical perturbations. Using a new genome-scale reconstruction of maize metabolism, we build an 18000-reaction, nonlinearly constrained model describing mesophyll and bundle sheath cells in 15 segments of the developing maize leaf, interacting via metabolite exchange, and use RNA-seq and enzyme activity measurements to predict spatial variation in metabolic state by a novel method that optimizes correlation between fluxes and expression data. Though such correlations are known to be weak in general, we suggest that developmental gradients may be particularly suited to the inference of metabolic fluxes from expression data, and we demonstrate that our method predicts fluxes that achieve high correlation with the data, successfully capture the experimentally observed base-to-tip transition between carbon-importing tissue and carbon-exporting tissue, and include a nonzero growth rate, in contrast to prior results from similar methods in other systems.
Highlights
C4 photosynthesis is an anatomical and biochemical system which improves the efficiency of carbon dioxide assimilation in plant leaves by restricting the carbon-fixing enzyme Rubisco to specialized bundle sheath compartments surrounding the veins, where a high-CO2PLOS ONE | DOI:10.1371/journal.pone.0151722 March 18, 2016Multiscale Metabolic Modeling of C4 Plants environment is maintained that favors CO2 over O2 in their competition for Rubisco active sites, suppressing photorespiration [1]
High-level, nonlinear models of photosynthetic physiology [15] relating enzyme activities, light and atmospheric CO2 levels, and the rates of CO2 assimilation by leaves have been widely applied to infer biochemical properties from macroscopic experiments and explore the responses of C4 plants under varying conditions. (We describe these models as ‘high-level’ since they describe in detail only a few of the individual biochemical reactions involved in the physiological processes they model, operating at a higher level of abstraction than more detailed kinetic models or genome-scale metabolic reconstructions.) More recently, detailed kinetic models have been used to explore the optimal allocation of resources to enzymes in an NADP-ME type C4 plant [16] and the relationship between the three decarboxylation types [17]
A high-confidence subset of the model, excluding many reactions not associated with manually curated pathways or lacking computationally predicted gene assignments as well as all reactions which could not achieve nonzero flux in flux balance analysis (FBA) calculations, involves 635 reactions among 603 species, with 469 reactions associated with a total of 2140 genes
Summary
C4 photosynthesis is an anatomical and biochemical system which improves the efficiency of carbon dioxide assimilation in plant leaves by restricting the carbon-fixing enzyme Rubisco to specialized bundle sheath compartments surrounding the veins, where a high-CO2PLOS ONE | DOI:10.1371/journal.pone.0151722 March 18, 2016Multiscale Metabolic Modeling of C4 Plants environment is maintained that favors CO2 over O2 in their competition for Rubisco active sites, suppressing photorespiration [1]. C4 plants are geographically and phylogenetically diverse, and represent the descendants of over 60 independent evolutionary origins of the system [2]. They include major crop plants such as maize, sugarcane and sorghum as well as many weeds and, relative to non-C4 (C3) plants, typically show improved nitrogen and water use efficiencies [3]. The core biochemical pathways are generally understood [4] but many areas of active research remain, including the genetic regulation of the C4 system [5], the importance of particular components of the system to its function (e.g., [6]), the significance of inter-specific variations in C4 biochemistry including alternative pathways for decarboxylation in the bundle sheath [7], details of the process of C4 evolution, [8,9,10,11,12] and the prospect of increasing yields of C3 crops by artificially introducing C4 functionality to those species [13, 14]
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