The CAM lineages of planet Earth

Abstract

Background and scope: The growth of experimental studies of crassulacean acid metabolism (CAM) in diverse plant clades, coupled with recent advances in molecular systematics, presents an opportunity to re-assess the phylogenetic distribution and diversity of species capable of CAM. It has been more than two decades since the last comprehensive lists of CAM taxa were published, and an updated survey of the occurrence and distribution of CAM taxa is needed to facilitate and guide future CAM research. We aimed to survey the phylogenetic distribution of these taxa, their diverse morphology, physiology and ecology, and the likely number of evolutionary origins of CAM based on currently known lineages.

Results and conclusions: We found direct evidence (in the form of experimental or field observations of gas exchange, day-night fluctuations in organic acids, carbon isotope ratios and enzymatic activity) for CAM in 370 genera of vascular plants, representing 38 families. Further assumptions about the frequency of CAM species in CAM clades and the distribution of CAM in the Cactaceae and Crassulaceae bring the currently estimated number of CAM-capable species to nearly 7 % of all vascular plants. The phylogenetic distribution of these taxa suggests a minimum of 66 independent origins of CAM in vascular plants, possibly with dozens more. To achieve further insight into CAM origins, there is a need for more extensive and systematic surveys of previously unstudied lineages, particularly in living material to identify low-level CAM activity, and for denser sampling to increase phylogenetic resolution in CAM-evolving clades. This should allow further progress in understanding the functional significance of this pathway by integration with studies on the evolution and genomics of CAM in its many forms.

Keywords: C3 photosynthesis; C3 + CAM; C4 + CAM; crassulacean acid metabolism; nocturnal acidification; photosynthetic pathway evolution; strong CAM; vascular plants.

Fig. 1.

Simplified overview of biochemistry (A) and four phases of CAM (B); phases in (B) are adapted from Osmond (1978). During phase I of CAM, atmospheric CO₂ is captured in a series of steps involving phosphoenolpyruvate (PEP) carboxylase (PEPC) to form malate, which is stored as malic acid in the vacuole overnight. In phase II, stomata remain open, and both Rubisco and PEPC fix atmospheric CO₂. Stomatal closure marks the beginning of phase III, in which malate is released from the vacuole and decarboxylated by malic enzyme (NADP- or NAD-ME) as shown (or PEP carboxykinase, not shown), releasing CO₂ to be re-fixed by Rubisco. Finally, if phase IV occurs, stomata reopen, and atmospheric CO₂ is fixed predominantly by Rubisco. If phase IV does not occur, stomatal opening is delayed until phase I begins again. Abbreviations: 3PGA, 3-phosphoglycerate; BCA, β-carbonic anhydrase; CBB, Calvin–Benson–Bassham cycle; MDH, malate dehydrogenase; OAA, oxaloacetate.

Fig. 2.

The distribution of crassulacean acid metabolism among vascular plant genera and families. The topology is adapted from Hinchliff and Smith (2014), with an updated topology of some lineages in the core Caryophyllales following Moore et al. (2018); the core Caryophyllales (blue star) are expanded below, with the Cactaceae collapsed because all genera are assumed to be CAM. Only families with CAM genera are labelled, and bars above each tip indicate genera known to have one or more species capable of CAM, regardless of CAM phenotype. Branches are not to scale and have been adjusted for visualization.

Fig. 3.

Mean diel ΔH⁺ in control (well-watered) and stress (drought or drought + salt stress) conditions of 45 Aizoaceae species (circles) (Winter, 2019) and 22 Montiaceae species (triangles) (Hancock et al., 2019). Purple points represent species with no significant ΔH⁺ in any conditions. Green points represent species with significant ΔH⁺ only in stress conditions. Yellow points represent species with significant ΔH⁺ in both control and stress conditions. The inset shows the maximum ΔH⁺ and mean δ¹³C values (Hancock et al., 2019) of the same Montiaceae species in the main plot. Note that ΔH⁺ for Aizoaceae species was calculated by multiplying changes in tissue malate concentrations given by Winter (2019) by a factor of two, assuming that 1 mol malate corresponds to 2 mol H⁺. Points with ΔH⁺ < 0.1 were plotted at 0.1 for visualization. Five individual species discussed in the main text are labelled.

Fig. 4.

Estimated CAM species diversity in vascular plants by family. The proportional (A) and absolute (B) species diversity capable of CAM is shown in each family with known CAM lineages. Orange, green and blue bars and pie charts show lower bounds, expected and upper bounds of CAM species diversity, respectively, as defined in the main text. CAM species diversity was calculated using the list of CAM genera and assumptions about the phylogenetic placement of CAM origins (Table 1), extent of CAM surveys, and links between CAM and other plant traits. Numbers of species in each genus were taken from POWO (2023), which lists 349 036 accepted names for non-hybrid vascular plant species.