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Crassulacean acid metabolism

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The pineapple is an example of a CAM plant.

Crassulacean acid metabolism, also known as CAM photosynthesis, is a carbon fixation pathway that evolved in some plants as an adaptation to arid conditions[1] that allows a plant to photosynthesize during the day, but only exchange gases at night. In a plant using full CAM, the stomata in the leaves remain shut during the day to reduce evapotranspiration, but they open at night to collect carbon dioxide (CO2) and allow it to diffuse into the mesophyll cells. The CO2 is stored as four-carbon malic acid in vacuoles at night, and then in the daytime, the malate is transported to chloroplasts where it is converted back to CO2, which is then used during photosynthesis. The pre-collected CO2 is concentrated around the enzyme RuBisCO, increasing photosynthetic efficiency. This mechanism of acid metabolism was first discovered in plants of the family Crassulaceae.

Historical background

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Observations relating to CAM were first made by de Saussure in 1804 in his Recherches Chimiques sur la Végétation.[2] Benjamin Heyne in 1812 noted that Bryophyllum leaves in India were acidic in the morning and tasteless by afternoon.[3] These observations were studied further and refined by Aubert, E. in 1892 in his Recherches physiologiques sur les plantes grasses and expounded upon by Richards, H. M. 1915 in Acidity and Gas Interchange in Cacti, Carnegie Institution. The term CAM may have been coined by Ranson and Thomas in 1940, but they were not the first to discover this cycle. It was observed by the botanists Ranson and Thomas, in the succulent family Crassulaceae (which includes jade plants and Sedum).[4] The name "Crassulacean acid metabolism" refers to acid metabolism in Crassulaceae, and not the metabolism of "crassulacean acid"; there is no chemical by that name.

Overview: a two-part cycle

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Overview of CAM

CAM is an adaptation for increased efficiency in the use of water, and so is typically found in plants growing in arid conditions.[5] (CAM is found in over 99% of the known 1700 species of Cactaceae and in nearly all of the cacti producing edible fruits.)[6]

During the night

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During the night, a plant employing CAM has its stomata open, allowing 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.[7]

Overnight graph of CO2 absorbed by a CAM plant

During the day

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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.[8]

Benefits

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The most important benefit of CAM to the plant is the ability to leave most leaf stomata closed during the day.[9] 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.[10][What percentage is lost in CAM plants?]

Comparison with C4 metabolism

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CAM is named after the family Crassulaceae, to which the jade plant belongs.

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.[11] 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.[12]

Biochemistry

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Biochemistry of CAM

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

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Cross section of a CAM (Crassulacean acid metabolism) plant, specifically of an agave leaf. Vascular bundles shown. Drawing based on microscopic images courtesy of Cambridge University Plant Sciences Department.

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.[5]

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.[5]

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[13]) 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.[14]

Aquatic CAM

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CAM photosynthesis is also found in aquatic species in at least 4 genera, including: Isoetes, Crassula, Littorella, Sagittaria, and possibly Vallisneria,[15] 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.[16] However, the reason for CAM in aquatic plants is not due to a lack of available water, but a limited supply of CO2.[15] 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.[16] 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.[17]

Ecological and taxonomic distribution of CAM-using plants

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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);[18] 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;[19] 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.[20] 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,[21] and Portulaca oleracea, better known as Purslane, which normally uses C4 fixation but is also able to switch to CAM when drought-stressed.[22]

CAM has evolved convergently many times.[23] It occurs in 16,000 species (about 7% of plants), belonging to over 300 genera and around 40 families, but this is thought to be a considerable underestimate.[24] The great majority of plants using CAM are angiosperms (flowering plants) but it is found in ferns, Gnetopsida and in quillworts (relatives of club mosses). Interpretation of the first quillwort genome in 2021 (I. taiwanensis) suggested that its use of CAM was another example of convergent evolution.[25] In Tillandsia CAM evolution has been associated with gene family expansion.[26]

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

Division Class/Angiosperm group Order Family Plant Type Clade involved
Lycopodiophyta Isoetopsida Isoetales Isoetaceae hydrophyte Isoetes[27] (the sole genus of class Isoetopsida) - I. howellii (seasonally submerged), I. macrospora, I. bolanderi, I. engelmannii, I. lacustris, I. sinensis, I. storkii, I. kirkii, I. taiwanensis.
Pteridophyta Polypodiopsida Polypodiales Polypodiaceae epiphyte, lithophyte CAM is recorded from Microsorum, Platycerium and Polypodium,[28] Pyrrosia and Drymoglossum[29] and Microgramma
Pteridopsida Polypodiales Pteridaceae[30] epiphyte Vittaria[31]

Anetium citrifolium[32]

Cycadophyta Cycadopsida Cycadales Zamiaceae Dioon edule[33]
Gnetophyta Gnetopsida Welwitschiales Welwitschiaceae xerophyte Welwitschia mirabilis[34] (the sole species of the order Welwitschiales)
Magnoliophyta magnoliids Magnoliales Piperaceae epiphyte Peperomia camptotricha[35]
eudicots Caryophyllales Aizoaceae xerophyte widespread in the family; Mesembryanthemum crystallinum is a rare instance of an halophyte that displays CAM[36]
Cactaceae xerophyte Almost all cacti have obligate Crassulacean Acid Metabolism in their stems; the few cacti with leaves may have C3 Metabolism in those leaves;[37] seedlings have C3 Metabolism.[38]
Portulacaceae xerophyte recorded in approximately half of the genera (note: Portulacaceae is paraphyletic with respect to Cactaceae and Didiereaceae)[39]
Didiereaceae xerophyte
Saxifragales Crassulaceae hydrophyte, xerophyte, lithophyte Crassulacean acid metabolism is widespread among the (eponymous) Crassulaceae.
eudicots (rosids) Vitales Vitaceae[40] Cissus,[41] Cyphostemma
Malpighiales Clusiaceae hemiepiphyte Clusia[41][42]
Euphorbiaceae[40] CAM is found is some species of Euphorbia[41][43] including some formerly placed in the sunk genera Monadenium,[41] Pedilanthus[43] and Synadenium. C4 photosynthesis is also found in Euphorbia (subgenus Chamaesyce).
Passifloraceae[30] xerophyte Adenia[44]
Geraniales Geraniaceae CAM is found in some succulent species of Pelargonium,[45] and is also reported from Geranium pratense[46]
Cucurbitales Cucurbitaceae Xerosicyos danguyi,[47] Dendrosicyos socotrana,[48] Momordica[49]
Celastrales Celastraceae[50]
Oxalidales Oxalidaceae[51] Oxalis carnosa var. hirta[51]
Brassicales Moringaceae Moringa[52]
Salvadoraceae[51] CAM is found in Salvadora persica.[51] Salvadoraceae were previously placed in order Celastrales, but are now placed in Brassicales.
Sapindales Sapindaceae Dodonaea viscosa
Fabales Fabaceae[51] CAM is found in Prosopis juliflora (listed under the family Salvadoraceae in Sayed's (2001) table,[51]) but is currently in the family Fabaceae (Leguminosae) according to The Plant List[53]).
Zygophyllaceae Zygophyllum[52]
eudicots (asterids) Ericales Ebenaceae
Solanales Convolvulaceae Ipomoea[citation needed] (Some species of Ipomoea are C3[41][54] - a citation is needed here.)
Gentianales Rubiaceae epiphyte Hydnophytum and Myrmecodia
Apocynaceae CAM is found in subfamily Asclepidioideae (Hoya,[41] Dischidia, Ceropegia, Stapelia,[43] Caralluma negevensis, Frerea indica,[55] Adenium, Huernia), and also in Carissa[56] and Acokanthera[57]
Lamiales Gesneriaceae epiphyte CAM was found Codonanthe crassifolia, but not in 3 other genera[58]
Lamiaceae Plectranthus marrubioides, Coleus[citation needed]
Plantaginaceae hydrophyte Littorella uniflora[27]
Apiales Apiaceae hydrophyte Lilaeopsis lacustris
Asterales Asteraceae[40] some species of Senecio[59]
monocots Alismatales Hydrocharitaceae hydrophyte Hydrilla,[40] Vallisneria
Alismataceae hydrophyte Sagittaria
Araceae Zamioculcas zamiifolia is the only CAM plant in Araceae, and the only non-aquatic CAM plant in Alismatales[60]
Poales Bromeliaceae epiphyte Bromelioideae (91%), Puya (24%), Dyckia and related genera (all), Hechtia (all), Tillandsia (many)[61]
Cyperaceae hydrophyte Scirpus,[40] Eleocharis
Asparagales Orchidaceae epiphyte Orchidaceae has more CAM species than any other family (CAM Orchids)
Agavaceae[42] xerophyte Agave,[41] Hesperaloe, Yucca and Polianthes[44]
Asphodelaceae[40] xerophyte Aloe,[41] Gasteria,[41] and Haworthia
Ruscaceae[40] Sansevieria[41][51] (This genus is listed under the family Dracaenaceae in Sayed's (2001) table, but currently in the family Asparagaceae according to The Plant List), Dracaena[62]
Commelinales Commelinaceae Callisia,[41] Tradescantia, Tripogandra

See also

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References

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