Alternative Crassulacean Acid Metabolism Modes Provide Environment-Specific Water-Saving Benefits in a Leaf Metabolic Model

Töpfer, Nadine; Braam, Thomas; Shameer, Sanu; Ratcliffe, R. G.; Sweetlove, Lee J.

doi:10.1105/tpc.20.00132

Cited by 53 publications

(66 citation statements)

References 66 publications

(70 reference statements)

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“…By varying the CO 2 exchange in the light period, as a proxy for stomatal conductance, our model predicted a C 3 -CAM continuum with gradual metabolic changes along the continuum ( Figure 3 ). A recent modeling study demonstrated that CAM could be a result of a trade-off between water saving and leaf productivity ( Töpfer et al, 2020 ), which is in line with our results that CAM could emerge under an evolutionary pressure for reduced light period stomatal conductance such as water saving. The key metabolic changes along the C 3 -CAM continuum included the processes in the starch/sugar-malate cycle, the TCA cycle at night, and the chloroplastic and mitochondrial ETCs, which are consistent with what we know about metabolic fluxes in CAM ( Silvera et al, 2010 ).…”

Section: Discussionsupporting

confidence: 92%

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

2021

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The evolution of Crassulacean acid metabolism (CAM) is thought to be along a C3-CAM continuum including multiple variations of CAM such as CAM cycling and CAM idling. Here, we applied large-scale constraint-based modeling to investigate the metabolism and energetics of plants operating in C3, CAM, CAM cycling, and CAM idling. Our modeling results suggested that CAM cycling and CAM idling could be potential evolutionary intermediates in CAM evolution by establishing a starch/sugar-malate cycle. Our model analysis showed that by varying CO2 exchange during the light period, as a proxy of stomatal conductance, there exists a C3-CAM continuum with gradual metabolic changes, supporting the notion that evolution of CAM from C3 could occur solely through incremental changes in metabolic fluxes. Along the C3-CAM continuum, our model predicted changes in metabolic fluxes not only through the starch/sugar-malate cycle that is involved in CAM photosynthetic CO2 fixation but also other metabolic processes including the mitochondrial electron transport chain and the tricarboxylate acid cycle at night. These predictions could guide engineering efforts in introducing CAM into C3 crops for improved water use efficiency.

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Section: Discussionsupporting

confidence: 92%

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

2021

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“…In our recent work, we focussed on studying the tradeoff between water-saving and leaf productivity and the analysis of alternative CAM-like flux modes in a C3 metabolic network [ 36 ]. In contrast with C4 photosynthesis, in CAM photosynthesis initial and re-fixation of CO 2 are not spatially but temporally separated between day and night.…”

Section: Abiotic Interactionsmentioning

confidence: 99%

“…Environment-coupled flux-balance models of leaf metabolism are a versatile means for multi-omics data integration and interpretation [ 17 , 60 ], they have closed gaps in our understanding of plant metabolism and led to the suggestion of engineering strategies to enhance plant's performance [ 36 ].…”

Section: Perspectivesmentioning

confidence: 99%

Environment-coupled models of leaf metabolism

Töpfer

2021

Biochemical Society Transactions

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The plant leaf is the main site of photosynthesis. This process converts light energy and inorganic nutrients into chemical energy and organic building blocks for the biosynthesis and maintenance of cellular components and to support the growth of the rest of the plant. The leaf is also the site of gas–water exchange and due to its large surface, it is particularly vulnerable to pathogen attacks. Therefore, the leaf's performance and metabolic modes are inherently determined by its interaction with the environment. Mathematical models of plant metabolism have been successfully applied to study various aspects of photosynthesis, carbon and nitrogen assimilation and metabolism, aided suggesting metabolic intervention strategies for optimized leaf performance, and gave us insights into evolutionary drivers of plant metabolism in various environments. With the increasing pressure to improve agricultural performance in current and future climates, these models have become important tools to improve our understanding of plant–environment interactions and to propel plant breeders efforts. This overview article reviews applications of large-scale metabolic models of leaf metabolism to study plant–environment interactions by means of flux-balance analysis. The presented studies are organized in two ways — by the way the environment interactions are modelled — via external constraints or data-integration and by the studied environmental interactions — abiotic or biotic.

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“…As most metabolomics experiments capture data of whole tissues, our knowledge is largely biased toward prevailing cells such as mesophyll cells in leaves [118] and endosperm in seeds [119,120]. However, several works highlight the striking differences in cell-specific metabolism and the impact that less recurrent cell types have in regulating and integrating crucial physiological processes, including transpiration and photosynthesis [121,122]. Moreover, assessing metabolic heterogeneity across cells belonging to a tissue has the potential to unravel unforeseen details masked by averaging such populations of cells, thereby contributing to a deeper understanding of metabolic regulation [6].…”

Section: Conclusion and Future Perspectivesmentioning

confidence: 99%

Plant Single-Cell Metabolomics—Challenges and Perspectives

Souza

Borghi

Fernie

2020

IJMS

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Omics approaches for investigating biological systems were introduced in the mid-1990s and quickly consolidated to become a fundamental pillar of modern biology. The idea of measuring the whole complement of genes, transcripts, proteins, and metabolites has since become widespread and routinely adopted in the pursuit of an infinity of scientific questions. Incremental improvements over technical aspects such as sampling, sensitivity, cost, and throughput pushed even further the boundaries of what these techniques can achieve. In this context, single-cell genomics and transcriptomics quickly became a well-established tool to answer fundamental questions challenging to assess at a whole tissue level. Following a similar trend as the original development of these techniques, proteomics alternatives for single-cell exploration have become more accessible and reliable, whilst metabolomics lag behind the rest. This review summarizes state-of-the-art technologies for spatially resolved metabolomics analysis, as well as the challenges hindering the achievement of sensu stricto metabolome coverage at the single-cell level. Furthermore, we discuss several essential contributions to understanding plant single-cell metabolism, finishing with our opinion on near-future developments and relevant scientific questions that will hopefully be tackled by incorporating these new exciting technologies.

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Alternative Crassulacean Acid Metabolism Modes Provide Environment-Specific Water-Saving Benefits in a Leaf Metabolic Model

Abstract: Stoichiometric modelling of leaf metabolism reveals metabolic and morphological determinants for introducing Crassulacean acid metabolism and alternative watersaving flux modes into a C3 leaf in different environments.

Cited by 53 publications

References 66 publications

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

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

Environment-coupled models of leaf metabolism

Plant Single-Cell Metabolomics—Challenges and Perspectives

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