Crassulacean acid metabolism

Overview: a two-part cycle

CAM is an adaptation that enables more efficient use of water, and so is typically found in plants growing in arid conditions. (CAM is found in over 99% of the known 1700 species of Cactaceae and in nearly all of the cacti producing edible fruits.)

During the night

During the night, a plant employing CAM has its stomata open, which allows CO₂ to enter and be fixed as organic acids by a PEP reaction similar to the C₄ pathway. The resulting organic acids are stored in vacuoles for later use, as the Calvin cycle cannot operate without ATP and NADPH, products of light-dependent reactions that do not take place at night.

During the day

During the day, the stomata close to conserve water, and the CO₂-storing organic acids are released from the vacuoles of the mesophyll cells. An enzyme in the stroma of chloroplasts releases the CO₂, which enters into the Calvin cycle so that photosynthesis may take place.

Benefits

The most important benefit of CAM to the plant is the ability to leave most leaf stomata closed during the day. Plants employing CAM are most common in arid environments, where water is scarce. Being able to keep stomata closed during the hottest and driest part of the day reduces the loss of water through evapotranspiration, allowing such plants to grow in environments that would otherwise be far too dry. Plants using only C₃ carbon fixation, for example, lose 97% of the water they take up through the roots to transpiration - a high cost avoided by plants able to employ CAM.

Comparison with C4 metabolism

The C₄ pathway bears resemblance to CAM; both act to concentrate CO₂ around RuBisCO, thereby increasing its efficiency. CAM concentrates it temporally, providing CO₂ during the day, and not at night, when respiration is the dominant reaction. C₄ plants, in contrast, concentrate CO₂ spatially, with a RuBisCO reaction centre in a "bundle sheath cell" being inundated with CO₂. Due to the inactivity required by the CAM mechanism, C₄ carbon fixation has a greater efficiency in terms of PGA synthesis.

There are some C₄/CAM intermediate species, such as Peperomia camptotricha, Portulaca oleracea, and Portulaca grandiflora. It was previously thought that the two pathways of photosynthesis in such plants could occur in the same leaves but not in the same cells, and that the two pathways could not couple but only occur side by side. It is now known, however, that in at least some species such as Portulaca oleracea, C₄ and CAM photosynthesis are fully integrated within the same cells, and that CAM-generated metabolites are incorporated directly into the C₄ cycle.

Biochemistry

Plants with CAM must control storage of CO₂ and its reduction to branched carbohydrates in space and time.

At low temperatures (frequently at night), plants using CAM open their stomata, CO₂ molecules diffuse into the spongy mesophyll's intracellular spaces and then into the cytoplasm. Here, they can meet phosphoenolpyruvate (PEP), which is a phosphorylated triose. During this time, the plants are synthesizing a protein called PEP carboxylase kinase (PEP-C kinase), whose expression can be inhibited by high temperatures (frequently at daylight) and the presence of malate. PEP-C kinase phosphorylates its target enzyme PEP carboxylase (PEP-C). Phosphorylation dramatically enhances the enzyme's capability to catalyze the formation of oxaloacetate, which can be subsequently transformed into malate by NAD⁺ malate dehydrogenase. Malate is then transported via malate shuttles into the vacuole, where it is converted into the storage form malic acid. In contrast to PEP-C kinase, PEP-C is synthesized all the time but almost inhibited at daylight either by dephosphorylation via PEP-C phosphatase or directly by binding malate. The latter is not possible at low temperatures, since malate is efficiently transported into the vacuole, whereas PEP-C kinase readily inverts dephosphorylation.

In daylight, plants using CAM close their guard cells and discharge malate that is subsequently transported into chloroplasts. There, depending on plant species, it is cleaved into pyruvate and CO₂ either by malic enzyme or by PEP carboxykinase. CO₂ is then introduced into the Calvin cycle, a coupled and self-recovering enzyme system, which is used to build branched carbohydrates. The by-product pyruvate can be further degraded in the mitochondrial citric acid cycle, thereby providing additional CO₂ molecules for the Calvin Cycle. Pyruvate can also be used to recover PEP via pyruvate phosphate dikinase, a high-energy step, which requires ATP and an additional phosphate. During the following cool night, PEP is finally exported into the cytoplasm, where it is involved in fixing carbon dioxide via malate.

Use by plants

Plants use CAM to different degrees. Some are "obligate CAM plants", i.e. they use only CAM in photosynthesis, although they vary in the amount of CO₂ they are able to store as organic acids; they are sometimes divided into "strong CAM" and "weak CAM" plants on this basis. Other plants show "inducible CAM", in which they are able to switch between using either the C₃ or C₄ mechanism and CAM depending on environmental conditions. Another group of plants employ "CAM-cycling", in which their stomata do not open at night; the plants instead recycle CO₂ produced by respiration as well as storing some CO₂ during the day.

Plants showing inducible CAM and CAM-cycling are typically found in conditions where periods of water shortage alternate with periods when water is freely available. Periodic drought – a feature of semi-arid regions – is one cause of water shortage. Plants which grow on trees or rocks (as epiphytes or lithophytes) also experience variations in water availability. Salinity, high light levels and nutrient availability are other factors which have been shown to induce CAM.

Since CAM is an adaptation to arid conditions, plants using CAM often display other xerophytic characters, such as thick, reduced leaves with a low surface-area-to-volume ratio; thick cuticle; and stomata sunken into pits. Some shed their leaves during the dry season; others (the succulents) store water in vacuoles. CAM also causes taste differences: plants may have an increasingly sour taste during the night yet become sweeter-tasting during the day. This is due to malic acid being stored in the vacuoles of the plants' cells during the night and then being used up during the day.

Aquatic CAM

CAM photosynthesis is also found in aquatic species in at least 4 genera, including: Isoetes, Crassula, Littorella, Sagittaria, and possibly Vallisneria, being found in a variety of species e.g. Isoetes howellii, Crassula aquatica.

These plants follow the same nocturnal acid accumulation and daytime deacidification as terrestrial CAM species. However, the reason for CAM in aquatic plants is not due to a lack of available water, but a limited supply of CO₂. CO₂ is limited due to slow diffusion in water, 10000x slower than in air. The problem is especially acute under acid pH, where the only inorganic carbon species present is CO₂, with no available bicarbonate or carbonate supply.

Aquatic CAM plants capture carbon at night when it is abundant due to a lack of competition from other photosynthetic organisms. This also results in lowered photorespiration due to less photosynthetically generated oxygen.

Aquatic CAM is most marked in the summer months when there is increased competition for CO₂, compared to the winter months. However, in the winter months CAM still has a significant role.

Ecological and taxonomic distribution of CAM-using plants

CAM has evolved convergently many times across vascular plants and does not represent a single evolutionary lineage. Comparative studies indicate that CAM evolution generally involves modifications to existing photosynthetic pathways rather than the evolution of entirely new enzymes, with many of the enzymes required for CAM already present in C₃ plants. Repeated origins of CAM are commonly associated with changes in when and where these enzymes are expressed, including shifts in daily circadian patterns of gene activity and differences in expression between tissues. Genomic studies in some CAM lineages show that expansion of gene families involved in carbon fixation and organic acid metabolism can accompany the evolution of CAM, suggesting that gene duplication may facilitate repeated evolutionary transitions to this pathway. The evolution of CAM is also strongly associated with plant lineages that possess traits such as succulence and large vacuoles, which enable the storage of organic acids produced during nocturnal carbon fixation.

The majority of plants possessing CAM are either epiphytes (e.g., orchids, bromeliads) or succulent xerophytes (e.g., cacti, cactoid Euphorbias), but CAM is also found in hemiepiphytes (e.g., Clusia); lithophytes (e.g., Sedum, Sempervivum); terrestrial bromeliads; wetland plants (e.g., Isoetes, Crassula (Tillaea), Lobelia); and in one halophyte, Mesembryanthemum crystallinum; one non-succulent terrestrial plant, (Dodonaea viscosa) and one mangrove associate (Sesuvium portulacastrum).

The only trees that can do CAM are in the genus Clusia; species of which are found across Central America, South America and the Caribbean. In Clusia, CAM is found in species that inhabit hotter, drier ecological niches, whereas species living in cooler montane forests tend to be C₃. In addition, some species of Clusia can temporarily switch their photosynthetic physiology from C₃ to CAM, a process known as facultative CAM. This allows these trees to benefit from the elevated growth rates of C₃ photosynthesis, when water is plentiful, and the drought tolerant nature of CAM, when the dry season occurs.

Plants which are able to switch between different methods of carbon fixation include Portulacaria afra, better known as Dwarf Jade Plant, which normally uses C₃ fixation but can use CAM if it is drought-stressed, and Portulaca oleracea, better known as Purslane, which normally uses C₄ fixation but is also able to switch to CAM when drought-stressed.

CAM occurs in approximately 16,000 species across more than 300 genera and around 40 families, although this number is likely an underestimate due to the presence of weak or facultative CAM in many species. Most CAM plants are flowering plants, but CAM has also evolved independently in some ferns, Gnetopsida, and quillworts, including Isoetes taiwanensis, whose genome provides evidence for an independent origin of CAM outside angiosperms.

The following list summarizes the taxonomic distribution of plants with CAM: