Reconstruction of Oryza sativa indica Genome Scale Metabolic Model and Its Responses to Varying RuBisCO Activity, Light Intensity, and Enzymatic Cost Conditions

Abstract

To combat decrease in rice productivity under different stresses, an understanding of rice metabolism is needed. Though there are different genome scale metabolic models (GSMs) of Oryza sativa japonica, no GSM with gene-protein-reaction association exist for Oryza sativa indica. Here, we report a GSM, OSI1136 of O.s. indica, which includes 3602 genes and 1136 metabolic reactions and transporters distributed across the cytosol, mitochondrion, peroxisome, and chloroplast compartments. Flux balance analysis of the model showed that for varying RuBisCO activity (Vc/Vo) (i) the activity of the chloroplastic malate valve increases to transport reducing equivalents out of the chloroplast under increased photorespiratory conditions and (ii) glyceraldehyde-3-phosphate dehydrogenase and phosphoglycerate kinase can act as source of cytosolic ATP under decreased photorespiration. Under increasing light conditions we observed metabolic flexibility, involving photorespiration, chloroplastic triose phosphate and the dicarboxylate transporters of the chloroplast and mitochondrion for redox and ATP exchanges across the intracellular compartments. Simulations under different enzymatic cost conditions revealed (i) participation of peroxisomal glutathione-ascorbate cycle in photorespiratory H2O2 metabolism (ii) different modes of the chloroplastic triose phosphate transporters and malate valve, and (iii) two possible modes of chloroplastic Glu–Gln transporter which were related with the activity of chloroplastic and cytosolic isoforms of glutamine synthetase. Altogether, our results provide new insights into plant metabolism.

Metabolic Modeling of the C3-CAM Continuum Revealed the Establishment of a Starch/Sugar-Malate Cycle in CAM Evolution

“…A similar analysis on a rice model with varying RuBisCO carboxylase to oxygenase ratio but without a change in light period CO 2 uptake showed that decreasing RuBisCO oxygenase contribution led to a decrease in photon influx ( Chatterjee et al, 2017 ). In our analysis, despite the constrained decrease in RuBisCO oxygenase contribution as light period CO 2 uptake decreased, the amount of energy (in terms of photons) required to sustain the same metabolic demand increased by about 7% from C 3 to CAM ( Figure 3C ) as extra energy is needed to run the starch-malate cycle.…”

Model‐assisted identification of metabolic engineering strategies for Jatropha curcas lipid pathways

“…Here we would like to emphasize that even though the genome from Jatropha was sequenced and that there is also the possibility to apply automated tools to perform a bottom‐up reconstruction, it must be noted that we were interested in lipid metabolism for which there is no complete annotation and thus these approaches will not provide optimal results. We also checked other plant metabolic models of small (Schwender et al ., 2004, 2006; Junker et al ., 2007; Alonso et al ., 2007a,b; Williams et al ., 2008; Allen et al ., 2009; Lonien and Schwender, 2009; Alonso et al ., 2010, 2011; Kruger et al ., 2012; Allen and Young, 2013; Masakapalli et al ., 2013; Colombié et al ., 2015; Schwender et al ., 2015; Rossi et al ., 2017; Cocuron et al ., 2019) and medium size (Grafahrend‐Belau et al ., 2009; Pilalis et al ., 2011; Hay and Schwender, 2011a,b; Schwender and Hay, 2012; Grafahrend‐Belau et al ., 2013; Arnold and Nikoloski, 2014), besides the available genome‐scale models (GEMs) (Poolman et al ., 2009; Radrich et al ., 2010; Dal’Molin et al ., 2010; Saha et al ., 2011; Mintz‐Oron et al ., 2012; Poolman et al ., 2013; Monaco et al ., 2013; Simons et al ., 2014; Seaver et al ., 2015; Lakshmanan et al ., 2015; Yuan et al ., 2016; Bogart and Myers, 2016; Chatterjee et al ., 2017; Botero et al ., 2018; Pfau et al ., 2018; Shaw and Cheung, 2018; Moreira et al ., 2019), and found that most of the metabolic reconstructions of small and medium size have low levels of detail of the lipid network, since the lipid‐related reactions are lumped. The exception is the metabolic reconstruction for rapeseed (Hay and Schwender, 2011a,b), with a total of 572 reactions of which 187 are lipid‐related.…”

“…Therefore, to estimate the NGAM costs we made a literature search to gain an overview about how this parameter was estimated and incorporated in plant models (Poolman et al ., 2009; Grafahrend‐Belau et al ., 2009; Dal’Molin et al ., 2010; Radrich et al ., 2010; Hay and Schwender, 2011b; Pilalis et al ., 2011; Saha et al ., 2011; Mintz‐Oron et al ., 2012; Cheung et al ., 2013; Grafahrend‐Belau et al ., 2013; Monaco et al ., 2013; Poolman et al ., 2013; Arnold and Nikoloski, 2014; Simons et al ., 2014; Lakshmanan et al ., 2015; Seaver et al ., 2015; Bogart and Myers, 2016; Yuan et al ., 2016; Chatterjee et al ., 2017; Botero et al ., 2018; Pfau et al ., 2018; Shaw and Cheung, 2018; Moreira et al ., 2019). In only three of the reviewed models (Poolman et al ., 2009, 2013; Cheung et al ., 2013) the respective calculations of the maintenance costs were made using different approaches and experimental data for the respective biological systems, and in turn the reported NGAM costs were used in other published studies (Hay and Schwender, 2011b; Yuan et al ., 2016; Chatterjee et al ., 2017; Shaw and Cheung, 2018; Moreira et al ., 2019). There were other models whose maintenance costs were entirely taken from the literature (Grafahrend‐Belau et al ., 2009; Pfau et al ., 2018).…”

Environment-coupled models of leaf metabolism

“…Later, Chatterjee et al [ 20 ] used a different rice leaf model to study its responses to different light intensities and varying v C /v O ratios of rubisco, thereby mimicking increased photorespiration under drought stress, normal and suppressed photorespiration. Their comprehensive environment-scan combined with cost-weighted flux-balance analysis revealed different metabolic modes for maintaining redox and ATP balance including flux rearrangements across compartments and shifts in transport reactions.…”

“…Studies that investigated the effect of different CO 2 levels on leaf metabolism and particularly photorespiration include models of rice [ 20 , 28 ], tomato [ 29 ] and generic models of CAM photosynthesis [ 30 ]. Typically, constraints on rubisco's v C /v O ratio were implemented to model the leaf's metabolic response to changing CO 2 levels or temperature (as v C /v O is temperature-dependent, see also section ‘Response to different light intensities’).…”