Evolution of Crassulacean Acid Metabolism Photosynthesis

The physiological plasticity of CAM corresponds to its evolutionary diversity. CAM manifestation is strongly influenced by the history of a species and its habitat context (Silvera et al. 2010). CAM is taxonomically more broadly distributed than C₄ photosynthesis and is most likely evolutionary older. The presence of CAM in ancient groups such as the Isoetes (see I. howellii above) suggests a first appearance of CAM already in the Triassic.

Further CAM evolution was then probably driven by selection for increased carbon gain and better water use efficiency after the global reduction in atmospheric CO₂ concentration about 30 million years ago during the Oligocene (see evolution of C₄ photosynthesis, Sect. 6.6.2). CAM has evolved many times independently and to varying degrees. The extent of CAM manifestation shows a positive correlation with the dryness of the site; that is, the stronger the water scarcity of a habitat, the higher the likelihood of full CAM expression in the plants populating it.

Several characteristics of CAM can be distinguished, as described above (Borland et al. 2014). Accordingly, CAM requires a number of evolutionary changes in basal mechanisms that principally are present in all higher plants (Fig. 6.25):

Fig. 6.25. Evolutionary changes required for crassulacean acid metabolism (CAM) photosynthesis. (After Silvera et al. (2010))

- First, a reversal of stomatal regulation enables nocturnal CO₂ uptake. The control of the stomatal aperture by light has to be overridden by other control mechanisms. One factor could be the low internal leaf CO₂ partial pressure at night, due to the activity of PEP carboxylase

- Second, diurnal fluctuations in organic acids and (reciprocally) in storage compounds and soluble sugars, plus respective transport activities, are established (e.g. malate into the vacuole and malic acid out of the vacuole)

- Third, key elements of CAM photosynthesis, e.g. carboanhydrase and PEPC, as well as decarboxylating enzymes—are more strongly expressed. Prerequisites here are the duplication and diversification of genes encoding the respective enzymes. As in plants with C₄ photosynthesis, there are CAM plant-specific isoforms of PEP carboxylase with very high leaf expression

- Fourth, enhanced gluconeogenic and glycolytic activities supply substrates for carboxylation and decarboxylation

- The fifth element is leaf succulence. A clear correlation exists between the degree of leaf succulence and the strength of CAM. Plants with thicker leaves show lower δ¹³C values, which is indicative of stronger CAM (see the range of δ¹³C values in Table 6.3). This is explained not only by the greater storage capacity of larger cells (with vacuoles taking up 90-95% of the volume) but also by the tight packing of cells in succulent tissues, which restricts the intercellular gas space and thereby the gas exchange rates, and consequently limits C3 photosynthesis during phases II and IV

Table 6.3. Water use efficiency, photosynthesis and biomass production of C₃, C₄ and CAM plants. Crassulacean acid metabolism (CAM) plants are superior to other photosynthetic types in their water use efficiency^a, but their photosynthetic rates and growth rates are much lower (Lüttge et al. 1994)

- Finally, the sixth key mechanism is the circadian clock control over CO₂ fixation. Comparative studies with four Clusia species (one C₃ species, two C₃-CAM intermediates and one strong, constitutive CAM species) have revealed an association of the circadian control of PEPCK transcript abundance with CAM strength—that is, with day/ night changes in malate and soluble sugar content

As indicated in Fig. 6.25, all of these mechanisms can vary in their extent along a continuum of CAM manifestations.

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