Abstract
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.
Highlights
Crassulacean acid metabolism (CAM) photosynthetic CO2 fixation is an evolutionary descendant of C3 photosynthesis
Using a core plant metabolic model, we were able to model the metabolic behaviors of CAM, CAM cycling, and CAM idling by changing a few simple constraints on gaseous exchange and phloem export
Our modeling results suggest that CAM cycling and CAM idling could potentially be evolutionary intermediates on the path to CAM evolution by establishing an intermediate flux through the starch/sugar-malate cycle
Summary
Crassulacean acid metabolism (CAM) photosynthetic CO2 fixation is an evolutionary descendant of C3 photosynthesis. CAM photosynthesis is known to have evolved independently multiple times in at least 35 plant families comprising about 6% of flowering plant species (Winter and Smith, 1996a; Silvera et al, 2010). CAM is an adaptation of photosynthetic CO2 fixation typically associated to limited water availability (Cushman and Borland, 2002). By closing their stomata during the light period and fixing atmospheric and/or respiratory carbon dioxide (CO2) exclusively in the dark period, CAM allows plants to use water more efficiently while fixing carbon for growth (Figure 1). As a carbon-concentrating mechanism, CAM is thought to be more metabolically expensive than C3
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