Crassulacean acid metabolism

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.

The pineapple is an example of a CAM plant.

Historical background

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

 

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

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

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.^{[citation needed]}

Benefits

The most important benefit of CAM to the plant is the ability to leave most leaf stomata closed during the day.^[8] 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.^{[9][What percentage is lost in CAM plants?]}

Comparison with C₄ metabolism

 

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.^[10] 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.^[11]

Biochemistry

 

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

 

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^[12]) 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.^[13]

Aquatic CAM

CAM photosynthesis is also found in aquatic species in at least 4 genera, including: Isoetes, Crassula, Littorella, Sagittaria, and possibly Vallisneria,^[14] 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.^[15] However, the reason for CAM in aquatic plants is not due to a lack of available water, but a limited supply of CO₂.^[14] 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.^[15] 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.^[16]

Ecological and taxonomic distribution of CAM-using plants

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);^[17] 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.^[18] 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,^[19] and Portulaca oleracea, better known as Purslane, which normally uses C₄ fixation but is also able to switch to CAM when drought-stressed.^[20]

CAM has evolved convergently many times.^[21] 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.^[22] 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.^[23]

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^[24] (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,^[25] Pyrrosia and Drymoglossum^[26] and Microgramma
	Pteridopsida	Polypodiales	Pteridaceae^[27]	epiphyte	Vittaria^[28] Anetium citrifolium^[29]
Cycadophyta	Cycadopsida	Cycadales	Zamiaceae		Dioon edule^[30]
Gnetophyta	Gnetopsida	Welwitschiales	Welwitschiaceae	xerophyte	Welwitschia mirabilis^[31] (the sole species of the order Welwitschiales)
Magnoliophyta	magnoliids	Magnoliales	Piperaceae	epiphyte	Peperomia camptotricha^[32]
	eudicots	Caryophyllales	Aizoaceae	xerophyte	widespread in the family; Mesembryanthemum crystallinum is a rare instance of an halophyte that displays CAM^[33]
			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;^[34] seedlings have C3 Metabolism.^[35]
			Portulacaceae	xerophyte	recorded in approximately half of the genera (note: Portulacaceae is paraphyletic with respect to Cactaceae and Didiereaceae)^[36]
			Didiereaceae	xerophyte
		Saxifragales	Crassulaceae	hydrophyte, xerophyte, lithophyte	Crassulacean acid metabolism is widespread among the (eponymous) Crassulaceae.
	eudicots (rosids)	Vitales	Vitaceae^[37]		Cissus,^[38] Cyphostemma
		Malpighiales	Clusiaceae	hemiepiphyte	Clusia^[38]^[39]
			Euphorbiaceae^[37]		CAM is found is some species of Euphorbia^[38]^[40] including some formerly placed in the sunk genera Monadenium,^[38] Pedilanthus^[40] and Synadenium. C4 photosynthesis is also found in Euphorbia (subgenus Chamaesyce).
			Passifloraceae^[27]	xerophyte	Adenia^[41]
		Geraniales	Geraniaceae		CAM is found in some succulent species of Pelargonium,^[42] and is also reported from Geranium pratense^[43]
		Cucurbitales	Cucurbitaceae		Xerosicyos danguyi,^[44] Dendrosicyos socotrana,^[45] Momordica^[46]
		Celastrales	Celastraceae^[47]
		Oxalidales	Oxalidaceae^[48]		Oxalis carnosa var. hirta^[48]
		Brassicales	Moringaceae		Moringa^[49]
			Salvadoraceae^[48]		CAM is found in Salvadora persica.^[48] Salvadoraceae were previously placed in order Celastrales, but are now placed in Brassicales.
		Sapindales	Sapindaceae		Dodonaea viscosa
		Fabales	Fabaceae^[48]		CAM is found in Prosopis juliflora (listed under the family Salvadoraceae in Sayed's (2001) table,^[48]) but is currently in the family Fabaceae (Leguminosae) according to The Plant List^[50]).
			Zygophyllaceae		Zygophyllum^[49]
	eudicots (asterids)	Ericales	Ebenaceae
		Solanales	Convolvulaceae		Ipomoea^[citation needed] (Some species of Ipomoea are C3^[38]^[51] - a citation is needed here.)
		Gentianales	Rubiaceae	epiphyte	Hydnophytum and Myrmecodia
			Apocynaceae		CAM is found in subfamily Asclepidioideae (Hoya,^[38] Dischidia, Ceropegia, Stapelia,^[40] Caralluma negevensis, Frerea indica,^[52] Adenium, Huernia), and also in Carissa^[53] and Acokanthera^[54]
		Lamiales	Gesneriaceae	epiphyte	CAM was found Codonanthe crassifolia, but not in 3 other genera^[55]
			Lamiaceae		Plectranthus marrubioides, Coleus^[citation needed]
			Plantaginaceae	hydrophyte	Littorella uniflora^[24]
		Apiales	Apiaceae	hydrophyte	Lilaeopsis lacustris
		Asterales	Asteraceae^[37]		some species of Senecio^[56]
	monocots	Alismatales	Hydrocharitaceae	hydrophyte	Hydrilla,^[37] Vallisneria
			Alismataceae	hydrophyte	Sagittaria
			Araceae		Zamioculcas zamiifolia is the only CAM plant in Araceae, and the only non-aquatic CAM plant in Alismatales^[57]
		Poales	Bromeliaceae	epiphyte	Bromelioideae (91%), Puya (24%), Dyckia and related genera (all), Hechtia (all), Tillandsia (many)^[58]
			Cyperaceae	hydrophyte	Scirpus,^[37] Eleocharis
		Asparagales	Orchidaceae	epiphyte	Orchidaceae has more CAM species than any other family ()
			Agavaceae^[39]	xerophyte	Agave,^[38] Hesperaloe, Yucca and Polianthes^[41]
			Asphodelaceae^[37]	xerophyte	Aloe,^[38] Gasteria,^[38] and Haworthia
			Ruscaceae^[37]		Sansevieria^[38]^[48] (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^[59]
		Commelinales	Commelinaceae		Callisia,^[38] Tradescantia, Tripogandra

See also

• C2 photosynthesis
• C3 carbon fixation
• C4 carbon fixation
• RuBisCO

References

1. C. Michael Hogan. 2011. Respiration. Encyclopedia of Earth. Eds. Mark McGinley & C.J.cleveland. National council for Science and the Environment. Washington DC
2. de Saussure T (1804). Recherches chimiques sur la végétation. Paris: Nyon.
3. Bonner W, Bonner J (1948). "The Role of Carbon Dioxide in Acid Formation by Succulent Plants". American Journal of Botany. 35 (2): 113–117. doi:10.2307/2437894. JSTOR 2437894.
4. Ranson SL, Thomas M (1960). "Crassulacean acid metabolism" (PDF). Annual Review of Plant Physiology. 11 (1): 81–110. doi:10.1146/annurev.pp.11.060160.000501. hdl:10150/552219.
5. Herrera A (2008), "Crassulacean acid metabolism and fitness under water deficit stress: if not for carbon gain, what is facultative CAM good for?", Annals of Botany, 103 (4): 645–653, doi:10.1093/aob/mcn145, PMC 2707347, PMID 18708641
6. The Encyclopedia of Fruit & Nuts. CABI. 2008. p. 218.
7. Forseth I (2010). "The Ecology of Photosynthetic Pathways". Knowledge Project. Nature Education. Retrieved 2021-03-06. In this pathway, stomata open at night, which allows CO2 to diffuse into the leaf to be combined with PEP and form malate. This acid is then stored in large central vacuoles until daytime.
8. Ting IP (1985). "Crassulacean Acid Metabolism" (PDF). Annual Review of Plant Physiology. 36 (1): 595–622. doi:10.1146/annurev.pp.36.060185.003115. hdl:10150/552219.
9. Raven JA, Edwards D (March 2001). "Roots: evolutionary origins and biogeochemical significance". Journal of Experimental Botany. 52 (Spec Issue): 381–401. doi:10.1093/jexbot/52.suppl_1.381. PMID 11326045.
10. Lüttge U (June 2004). "Ecophysiology of Crassulacean Acid Metabolism (CAM)". Annals of Botany. 93 (6): 629–652. doi:10.1093/aob/mch087. PMC 4242292. PMID 15150072.
11. Moreno-Villena JJ, Zhou H, Gilman IS, Tausta SL, Cheung CY, Edwards EJ (August 2022). "Spatial resolution of an integrated C₄+CAM photosynthetic metabolism". Science Advances. 8 (31): eabn2349. Bibcode:2022SciA....8N2349M. doi:10.1126/sciadv.abn2349. PMC 9355352. PMID 35930634.
12. Smith SD, Monson RK, Anderson JE, Smith SD, Monson RK, Anderson JE (1997). "CAM Succulents". Physiological Ecology of North American Desert Plants. Adaptations of Desert Organisms. pp. 125–140. doi:10.1007/978-3-642-59212-6_6. ISBN 978-3-642-63900-5.
13. Raven, P & Evert, R & Eichhorn, S, 2005, "Biology of Plants" (seventh edition), p. 135 (Figure 7-26), W.H. Freeman and Company Publishers ISBN 0-7167-1007-2
14. Keeley J (1998). "CAM Photosynthesis in Submerged Aquatic Plants". Botanical Review. 64 (2): 121–175. doi:10.1007/bf02856581. S2CID 5025861.
15. Keeley JE, Busch G (October 1984). "Carbon Assimilation Characteristics of the Aquatic CAM Plant, Isoetes howellii". Plant Physiology. 76 (2): 525–530. doi:10.1104/pp.76.2.525. PMC 1064320. PMID 16663874.
16. Klavsen SK, Madsen TV (September 2012). "Seasonal variation in crassulacean acid metabolism by the aquatic isoetid Littorella uniflora". Photosynthesis Research. 112 (3): 163–173. doi:10.1007/s11120-012-9759-0. PMID 22766959. S2CID 17160398.
17. Keddy PA (2010). Wetland Ecology: Principles and Conservation. Cambridge, UK: Cambridge University Press. p. 26. ISBN 978-0521739672.
18. Leverett A, Hurtado Castaño N, Ferguson K, Winter K, Borland AM (June 2021). "Crassulacean acid metabolism (CAM) supersedes the turgor loss point (TLP) as an important adaptation across a precipitation gradient, in the genus Clusia". Functional Plant Biology. 48 (7): 703–716. doi:10.1071/FP20268. PMID 33663679. S2CID 232121559.
19. Guralnick LJ, Ting IP (October 1987). "Physiological Changes in Portulacaria afra (L.) Jacq. during a Summer Drought and Rewatering". Plant Physiology. 85 (2): 481–486. doi:10.1104/pp.85.2.481. PMC 1054282. PMID 16665724.
20. Koch KE, Kennedy RA (April 1982). "Crassulacean Acid Metabolism in the Succulent C(4) Dicot, Portulaca oleracea L Under Natural Environmental Conditions". Plant Physiology. 69 (4): 757–761. doi:10.1104/pp.69.4.757. PMC 426300. PMID 16662291.
21. Keeley JE, Rundel PW (2003). "Evolution of CAM and C4 Carbon-Concentrating Mechanisms" (PDF). International Journal of Plant Sciences. 164 (S3): S55–S77. doi:10.1086/374192. S2CID 85186850.
22. Dodd AN, Borland AM, Haslam RP, Griffiths H, Maxwell K (April 2002). "Crassulacean acid metabolism: plastic, fantastic". Journal of Experimental Botany. 53 (369): 569–580. doi:10.1093/jexbot/53.369.569. PMID 11886877.
23. Wickell D, Kuo LY, Yang HP, Dhabalia Ashok A, Irisarri I, Dadras A, et al. (November 2021). "Underwater CAM photosynthesis elucidated by Isoetes genome". Nature Communications. 12 (1): 6348. Bibcode:2021NatCo..12.6348W. doi:10.1038/s41467-021-26644-7. PMC 8566536. PMID 34732722.
24. Boston HL, Adams MS (1983). "Evidence of crussulacean acid metabolism in two North American isoetids". Aquatic Botany. 15 (4): 381–386. doi:10.1016/0304-3770(83)90006-2.
25. Holtum JA, Winter K (1999). "Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns". Australian Journal of Plant Physiology. 26 (8): 749. doi:10.1071/PP99001.
26. Wong SC, Hew CS (1976). "Diffusive Resistance, Titratable Acidity, and CO₂ Fixation in Two Tropical Epiphytic Ferns". American Fern Journal. 66 (4): 121–124. doi:10.2307/1546463. JSTOR 1546463.
27. Crassulacean Acid Metabolism 2007-06-09 at the Wayback Machine
28. . Archived from the original on 2009-06-18. Retrieved 2008-02-24.
29. Martin SL, Davis R, Protti P, Lin TC, Lin SH, Martin CE (2005). "The Occurrence of Crassulacean Acid Metabolism in Epiphytic Ferns, with an Emphasis on the Vittariaceae". International Journal of Plant Sciences. 166 (4): 623–630. doi:10.1086/430334. hdl:1808/9895. S2CID 67829900.
30. Vovides AP, Etherington JR, Dresser PQ, Groenhof A, Iglesias C, Ramirez JF (2002). "CAM-cycling in the cycad Dioon edule Lindl. in its natural tropical deciduous forest habitat in central Veracruz, Mexico". Botanical Journal of the Linnean Society. 138 (2): 155–162. doi:10.1046/j.1095-8339.2002.138002155.x.
31. Schulze ED, Ziegler H, Stichler W (December 1976). "Environmental control of crassulacean acid metabolism in Welwitschia mirabilis Hook. Fil. in its range of natural distribution in the Namib desert". Oecologia. 24 (4): 323–334. Bibcode:1976Oecol..24..323S. doi:10.1007/BF00381138. PMID 28309109. S2CID 11439386.
32. Sipes DL, Ting IP (January 1985). "Crassulacean Acid Metabolism and Crassulacean Acid Metabolism Modifications in Peperomia camptotricha". Plant Physiology. 77 (1): 59–63. doi:10.1104/pp.77.1.59. PMC 1064456. PMID 16664028.
33. Chu C, Dai Z, Ku MS, Edwards GE (July 1990). "Induction of Crassulacean Acid Metabolism in the Facultative Halophyte Mesembryanthemum crystallinum by Abscisic Acid". Plant Physiology. 93 (3): 1253–1260. doi:10.1104/pp.93.3.1253. PMC 1062660. PMID 16667587.
34. Nobel PS, Hartsock TL (April 1986). "Leaf and Stem CO(2) Uptake in the Three Subfamilies of the Cactaceae". Plant Physiology. 80 (4): 913–917. doi:10.1104/pp.80.4.913. PMC 1075229. PMID 16664741.
35. Winter K, Garcia M, Holtum JA (July 2011). "Drought-stress-induced up-regulation of CAM in seedlings of a tropical cactus, Opuntia elatior, operating predominantly in the C3 mode". Journal of Experimental Botany. 62 (11): 4037–4042. doi:10.1093/jxb/err106. PMC 3134358. PMID 21504876.
36. Guralnick LJ, Jackson MD (2001). "The Occurrence and Phylogenetics of Crassulacean Acid Metabolism in the Portulacaceae". International Journal of Plant Sciences. 162 (2): 257–262. doi:10.1086/319569. S2CID 84007032.
37. Cockburn W (September 1985). "TANSLEY REVIEW No 1.: VARIATION IN PHOTOSYNTHETIC ACID METABOLISM IN VASCULAR PLANTS: CAM AND RELATED PHENOMENA". The New Phytologist. 101 (1): 3–24. doi:10.1111/j.1469-8137.1985.tb02815.x. PMID 33873823.
38. Nelson EA, Sage TL, Sage RF (July 2005). "Functional leaf anatomy of plants with crassulacean acid metabolism". Functional Plant Biology. 32 (5): 409–419. doi:10.1071/FP04195. PMID 32689143.
39. Lüttge U (June 2004). "Ecophysiology of Crassulacean Acid Metabolism (CAM)". Annals of Botany. 93 (6): 629–652. doi:10.1093/aob/mch087. PMC 4242292. PMID 15150072.
40. Bender MM (November 1973). "C/C ratio changes in crassulacean Acid metabolism plants". Plant Physiology. 52 (5): 427–430. doi:10.1104/pp.52.5.427. PMC 366516. PMID 16658576.
41. Szarek SR (1979). "The occurrence of Crassulacean Acid Metabolism a supplementary list during 1976 to 1979". Photosynthetica. 13 (4): 467–473.
42. Jones CS, Cardon ZG, Czaja AD (January 2003). "A phylogenetic view of low-level CAM in Pelargonium (Geraniaceae)". American Journal of Botany. 90 (1): 135–142. doi:10.3732/ajb.90.1.135. PMID 21659089.
43. Kluge M, Ting IP (2012). Crassulacean Acid Metabolism: Analysis of an Ecological Adaptation. de Ecological Studies. Vol. 30. Springer Science & Business Media. p. 24. ISBN 978-3-642-67038-1.
44. Bastide B, Sipes D, Hann J, Ting IP (December 1993). "Effect of Severe Water Stress on Aspects of Crassulacean Acid Metabolism in Xerosicyos". Plant Physiology. 103 (4): 1089–1096. doi:10.1104/pp.103.4.1089. PMC 159093. PMID 12232003.
45. Gibson AC (2012). Structure-Function Relations of Warm Desert Plants Adaptations of Desert Organisms. Springer Science & Business Media. p. 118. ISBN 9783642609794.
46. "Momordica charantia (bitter melon): 111016801". Kyoto Encyclopedia of Genes and Genomes.
47. Bareja BG (2013). "Plant Types: III. CAM Plants, Examples and Plant Families". Cropsreview.
48. Sayed OH (2001). "Crassulacean Acid Metabolism 1975–2000, a Check List". Photosynthetica. 39 (3): 339–352. doi:10.1023/A:1020292623960. S2CID 1434170.
49. Ogburn RM, Edwards EJ (January 2010). "The Ecological Water-Use Strategies of Succulent Plants" (PDF). Advances in Botanical Research. Vol. 55. Academic Press. pp. 179–225 – via Brown University.
50. "Prosopis juliflora". The Plant List. Retrieved 2015-09-11.
51. Martin CE, Lubbers AE, Teeri JA (1982). "Variability in Crassulacean Acid Metabolism A Survey of North Carolina Succulent Species". Botanical Gazette. 143 (4): 491–497. doi:10.1086/337326. hdl:1808/9891. JSTOR 2474765. S2CID 54906851.
52. Lange OL, Zuber M (1977). "Frerea indica, a stem succulent CAM plant with deciduous C₃ leaves". Oecologia. 31 (1): 67–72. Bibcode:1977Oecol..31...67L. doi:10.1007/BF00348709. PMID 28309150. S2CID 23514785.
53. Rao IM, Swamy PM, Das VS (1979). "Some Characteristics of Crassulacean Acid Metabolism in Five Nonsucculent Scrub Species Under Natural Semiarid Conditions". Zeitschrift für Pflanzenphysiologie. 94 (3): 201–210. doi:10.1016/S0044-328X(79)80159-2.
54. Houérou HN (2008). Bioclimatology and Biogeography of Africa Earth and Environmental Science. Springer Science & Business Media. p. 52. ISBN 9783540851929.
55. Guralnick LJ, Ting IP, Lord EM (1986). "Crassulacean Acid Metabolism in the Gesneriaceae". American Journal of Botany. 73 (3): 336–345. doi:10.1002/j.1537-2197.1986.tb12046.x. JSTOR 2444076. S2CID 59329286.
56. Fioretto A, Alfani A (1988). "Anatomy of Succulence and CAM in 15 Species of Senecio". Botanical Gazette. 149 (2): 142–152. doi:10.1086/337701. JSTOR 2995362. S2CID 84302532.
57. Holtum JA, Winter K, Weeks MA, Sexton TR (October 2007). "Crassulacean acid metabolism in the ZZ plant, Zamioculcas zamiifolia (Araceae)". American Journal of Botany. 94 (10): 1670–1676. doi:10.3732/ajb.94.10.1670. PMID 21636363.
58. Crayn DM, Winter K, Smith JA (March 2004). "Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae". Proceedings of the National Academy of Sciences of the United States of America. 101 (10): 3703–3708. Bibcode:2004PNAS..101.3703C. doi:10.1073/pnas.0400366101. PMC 373526. PMID 14982989.
59. Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC (October 2010). "Evolution along the crassulacean acid metabolism continuum". Functional Plant Biology. 37 (11): 995–1010. doi:10.1071/FP10084 – via Research gate.

External links

 

Wikimedia Commons has media related to CAM cycle.

• Khan Academy, video lecture