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. 2013 Aug;162(4):2140-50.
doi: 10.1104/pp.113.220178. Epub 2013 Jun 10.

Elucidating rice cell metabolism under flooding and drought stresses using flux-based modeling and analysis

Meiyappan Lakshmanan  1 , Zhaoyang Zhang, Bijayalaxmi Mohanty, Jun-Young Kwon, Hong-Yeol Choi, Hyung-Jin Nam, Dong-Il Kim, Dong-Yup Lee
Affiliations

Elucidating rice cell metabolism under flooding and drought stresses using flux-based modeling and analysis

Meiyappan Lakshmanan et al. Plant Physiol. 2013 Aug.

Abstract

Rice (Oryza sativa) is one of the major food crops in world agriculture, especially in Asia. However, the possibility of subsequent occurrence of flood and drought is a major constraint to its production. Thus, the unique behavior of rice toward flooding and drought stresses has required special attention to understand its metabolic adaptations. However, despite several decades of research investigations, the cellular metabolism of rice remains largely unclear. In this study, in order to elucidate the physiological characteristics in response to such abiotic stresses, we reconstructed what is to our knowledge the first metabolic/regulatory network model of rice, representing two tissue types: germinating seeds and photorespiring leaves. The phenotypic behavior and metabolic states simulated by the model are highly consistent with our suspension culture experiments as well as previous reports. The in silico simulation results of seed-derived rice cells indicated (1) the characteristic metabolic utilization of glycolysis and ethanolic fermentation based on oxygen availability and (2) the efficient sucrose breakdown through sucrose synthase instead of invertase. Similarly, flux analysis on photorespiring leaf cells elucidated the crucial role of plastid-cytosol and mitochondrion-cytosol malate transporters in recycling the ammonia liberated during photorespiration and in exporting the excess redox cofactors, respectively. The model simulations also unraveled the essential role of mitochondrial respiration during drought stress. In the future, the combination of experimental and in silico analyses can serve as a promising approach to understand the complex metabolism of rice and potentially help in identifying engineering targets for improving its productivity as well as enabling stress tolerance.

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Figures

Figure 1.
Figure 1.
Profiles of cell biomass and residual concentrations of the carbon nutrient components in batch cultures of aerobic Suc (A), anaerobic Suc (B), aerobic Glc (C), and anaerobic Glc (D). Highlighted regions correspond to exponential growth phases of the cultures. DCW, Dry cell weight.
Figure 2.
Figure 2.
Experimental and simulated growth rates during the exponential phase on different batch cultures.
Figure 3.
Figure 3.
In silico flux maps of seed-derived suspension culture rice cells grown on Suc under aerobic (A) and anaerobic (B) conditions. The color intensity of the lines in the central carbon metabolic network corresponds to the normalized flux values with respect to the Suc uptake rates in each condition. DCW, Dry cell weight. Metabolite abbreviations not defined in the text are as follows: 1,3-PGA, 1,3-diphosphoglycerate; 2-PGA, 2-phosphoglycerate; AA, amino acids; Acald, acetaldehyde; Ac-CoA, acetyl-CoA; E-4-P, erythrose-4-phosphate; F-6-P, Fru-6-P; F-1,6-bP, Fru-1,6-bisP; G-1-P, Glc-1-P; G3P, glyceraldehyde-3-phosphate; G-6-P, Glc-6-P; PEP, phosphoenolpyruvate; PRPP, phosphoribosyl pyrophosphate; Q, ubiquinone; QH2, ubiquinol; R-5-P, Rib-5-P; Ru-5-P, ribulose-5-phosphate; SSA, succinic semialdehyde; UDP-G, UDP-Glc, X-5-P, d-xylulose-5-phosphate. Enzyme abbreviations not defined in the text are as follows: ACO, aconitase; ADH, alcohol dehydrogenase; ALAAT, Ala aminotransferase; ALD, aldolase; APS, Glc-1-P adenylyltransferase; ASP1, Asp aminotransferase; ASPG, asparaginase; COX, cytochrome c oxidase; CSY, citrate synthase; FK, fructokinase; FUM, fumarase; GABA-TP, γ-aminobutyrate aminotransferase; GAD, Glu decarboxylase; GAPDH, glyceraldehyde phosphate dehydrogenase; IDP, isocitrate dehydrogenase (NADP dependent); MDH, malate dehydrogenase; NAD9, NADH dehydrogenase; PDC, pyruvate decarboxylase; PDH, pyruvate dehydrogenase; PEPE, phosphoenolpyruvate enolase; PFK, 6-phosphofructokinase; PFP, PPi-dependent phosphofructokinase; PGI, phosphoglucoisomerase; PGK, phosphoglycerate kinase; PGLYCM, phosphoglycerate mutase; PGM, phosphoglucomutase; PPC, phosphoenolpyruvate carboxylase; PPDK, pyruvate orthophosphate dikinase; PRS, Rib phosphate diphosphokinase; PYK, pyruvate kinase; RPE, Rib-5-P epimerase; SDH, succinate dehydrogenase; SSADH, succinic semialdehyde dehydrogenase; SSI, starch synthase; SUCLG, succinyl-CoA ligase; TKT, transketolase; TPI, triose phosphate isomerase; UGPP, UDP-Glc pyrophosphorylase. [See online article for color version of this figure.]
Figure 4.
Figure 4.
A, Effect of VC/VO of Rubisco on leaf cellular growth and CO2 uptake while absorbing equal amounts of photon. B, Flux map of the central metabolism in photorespiring leaves under normal conditions (VC/VO = 3). C, Variation in fluxes through key enzymes upon varying levels of VC/VO. The color intensity of the lines in the central carbon metabolic network (B) corresponds to the flux values obtained from simulations. C was drawn by normalizing the flux values with respect to VC/VO = 3. DCW, Dry cell weight. Metabolite abbreviations not defined in the text are as follows: 1,3-PGA, 1,3-diphosphoglycerate; 2-PGA, 2-phosphoglycerate; Ac-CoA, acetyl-CoA; ADP-G, ADP-Glc; E-4-P, d-erythrose-4-phosphate; F-1,6-bP, Fru-1,6-bisP; F-6-P, Fru-6-P; G-1-P, Glc-1-P; G3P, glyceraldehyde-3-phosphate; G-6-P, Glc-6-P; HP, hydroxypyruvate; PEP, phosphoenolpyruvate; PRPP, phosphoribosyl pyrophosphate; Q, ubiquinone; QH2, ubiquinol; S-6-P, Suc-6-P; R-5-P, Rib-5-P; Ru-1,5-bP, ribulose-1,5-bisphosphate; Ru-5-P, ribulose-5-phosphate; S-1,7-bP, sedoheptulose-1,7-bisphosphate; S-7-P, sedoheptulose-7-phosphate; Xu-5-P, xylulose-5-phosphate; UDP-G, UDP-Glc. Enzyme abbreviations not defined in the text are as follows: ACO, aconitase; ALAAT, Ala aminotransferase; ALD, aldolase; APS, Glc-1-P adenylyltransferase; ASP1, Asp aminotransferase; COX, cytochrome c oxidase; CSY, citrate synthase; FBP, Fru-bisphosphatase; FK, fructokinase; FUM, fumarase; GABA-TK, γ-aminobutyrate aminotransferase; GAD, Glu decarboxylase; GAPDH, glyceraldehyde phosphate dehydrogenase; GDC, Gly decarboxylase; GGAT, Gly aminotransferase; GLYK, glycerate kinase; GLN1, Glu ammonia ligase; GOX, glycolate oxidase; GS, Glu synthase (ferredoxin dependent); HPR, hydroxypyruvate reductase; MDH, malate dehydrogenase; NAD9, NADH dehydrogenase; PEPE, phosphoenolpyruvate enolase; PFK, phosphofructokinase; PGI, Glc-6-P isomerase; PGK, phosphoglycerate kinase; PGLYCM, phosphoglycerate mutase; PGM, phosphoglucomutase; PGP, phosphoglycolate phosphatase; PPC, phosphoenolpyruvate carboxylase; PPDK, pyruvate orthophosphate dikinase; PPS, pyruvate-water dikinase; PRK, phosphoribulokinase; PSLR, photosynthetic light reaction; PYK, pyruvate kinase; RBCS-C, ribulose-1,5-bisphosphate carboxylase; RBCS-O, ribulose-1,5-bisphosphate oxygenase; RPE, Rib-5-phosphate epimerase; SBP, sedoheptulose-bisphosphatase; SBPGL, sedoheptulose 1,7-bisphosphate d-glyceraldehyde-3-phosphate lyase; SDH, succinate dehydrogenase; SGAT, Ser glyoxylate aminotransferase; SHM, Ser hydroxymethyltransferase; SPP, Suc phosphatase; SPS, Suc phosphate synthase; SSADH, succinic semialdehyde dehydrogenase; SSI, starch synthase; TKT, transketolase; TPI, triose phosphate isomerase; UGPP, UDP-Glc pyrophosphorylase. [See online article for color version of this figure.]
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