Crassulacean Acid Metabolism

Abstract

Crassulacean acid metabolism (CAM) is a carbon dioxide acquisition, transient storage and concentrating mechanism of plants based on organic acid synthesis. Amongst 350 000 species of vascular plants, 21 000 species perform CAM. In this variant of photosynthesis, carbon dioxide can be fixed nocturnally in the dark and is stored in the form of organic acids from which it is remobilised during the day for assimilation in the light. This has arisen polyphyletically during evolution. It is an ecophysiological adaptation that allows carbon dioxide acquisition with exceptionally economic use of water. CAM allows acclimation to a variety of interacting stresses. It is an adaptation for survival and not for high productivity. Nevertheless, performance of CAM species on drought‐prone marginal lands makes them potential alternative crop plants and biofuel plants. CAM is regulated in a natural night/day rhythm, but can also oscillate freely under the control of circadian biological clocks.

Key Concepts

  • Metabolic mechanisms concentrating carbon dioxide internally in plants are important for photosynthesis at the low external carbon dioxide concentration in the present atmosphere.
  • Massive nocturnal CO2 uptake, fixation and storage in the form of organic acids result in inorganic carbon acquisition with high water‐use efficiency (WUE).
  • Rearranged internal management of available metabolic housekeeping functions can generate new metabolic options of adaptive value.
  • Generation of isoforms of housekeeping enzymes can facilitate polyphyletic evolution of new metabolic pathways.
  • Circadian oscillations can be controlled by different biological clocks, which are feedback related to each other and present in many copies.
  • Flexibility in the expression of metabolic pathway variants facilitates adaptation under variable stress situations.
  • Stress adaptation in plants is for survival and mostly not for high productivity.
  • Resistance to drought stress and high water‐use efficiency supports the quest for new crop plants including biofuel crops to be grown on marginal land.

Keywords: circadian rhythmicity; carbon dioxide acquisition; malate; phosphoenolpyruvate carboxylase; vacuolar H+ ATPase

Figure 1. Crassulacean acid metabolism (CAM) – a carbon dioxide acquisition, carbon dioxide transient storage and carbon dioxide‐concentrating mechanism. Simplified metabolic scheme of carbon flow, metabolic pathway and compartmentation. Left part: dark period; right part: light period; C, cytosol; M, mitochondrion; P, plastid (chloroplast); V, vacuole. The following abbreviations are used: AcCoA, acetyl‐coenzyme A; ADPG, adenosine diphosphate glucose; [CH2O] , carbohydrate; Citr, citrate; CoASH, coenzyme A; Di‐PGA, 2,3‐diphosphoglyceric acid; αKGA, α‐ketoglutaric acid; Mal, malate; OAA, oxaloacetate; Pi, inorganic phosphate; PPi, inorganic pyrophosphate; PPCox, oxidative pentose phosphate cycle; PPCred, reductive pentose phosphate cycle (Calvin cycle); PEP, phosphoenolpyruvate; Pyr, pyruvate; TCA‐C, tricarboxylic acid cycle; UDP and UTP, uridine‐di‐phosphate and uridine‐tri‐phosphate. Numbers refer to key enzymes highlighted in the text: (1) PEP‐carboxylase (PEPC); (2) H+‐transporting V‐ATPase at the tonoplast; (3) inward rectifying malate channel at the tonoplast; (4) NAD(P)‐dependent malic enzymes; (5) isocitrate dehydrogenase; (6) pyruvate, Pi dikinase (PPDK) and (7) NAD:glyceraldehyde‐3‐phosphate dehydrogenase.
Figure 2. Diurnal courses of net carbon dioxide exchange ( ), leaf‐conductance for water vapour ( ) and malate levels (per gram fresh weight, gFW) in a leaf of the CAM plant (Hamet et Perrier de la Bâthie). The dark grey bar on top of the graph indicates the night or dark period with nocturnal stomatal opening, that is, high , carbon dioxide uptake, that is, high and malate accumulation (phase I). An early morning peak of carbon dioxide uptake and stomatal opening between 8 and 9 h represents phase II of CAM. This is followed by daytime malate remobilisation and stomatal closure with negligible and (phase III). In the afternoon increases due to stomatal opening and there is carbon dioxide uptake and assimilation in the Calvin cycle (phase IV).
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References

Borland AM, Hartwell J, Jenkins GI, Wilkins MB and Nimmo HG (1999) Metabolic control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in crassulacean acid metabolism. Plant Physiology 121: 889–896.

Borland AM, Griffith H, Hartwell J and Smith JAC (2009) Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal lands. Journal of Experimental Botany 60: 2879–2896.

Borland AM, Zambrano VAB, Ceusters K and Shorrock K (2011) The photosynthetic plasticity of crassulacean acid metabolism: an evolutionary innovation for sustainable productivity in a changing world. New Phytologist 191: 619–633.

Borland AM, Hartwell J, Weston D, et al. (2014) Engineering crassulacean acid metabolism to improve water‐use efficiency. Trends in Plant Science 19: 327–338.

Boxall SF, Foster JM, Bohnert HJ, et al. (2005) Conservation and divergence of circadian clock operation in a stress‐inducible crassulacean acid metabolism species reveals clock compensation against stress. Plant Physiology 137: 969–982.

Carter PJ, Nimmo HG, Fewson CA and Wilkins MB (1991) Circadian rhythms in the activity of a plant protein kinase. EMBO Journal 10: 2063–2068.

Crayn DM, Terry RG, Smith JAC and Winter K (2000) Molecular systematic investigations in Pitcarnioideae (Bromeliaceae) as a basis for understanding the evolution of crassaulacean acid metabolism (CAM). In: Wilson KL and Morrison DA (eds) Monocots: Systematics and Evolution, pp. 569–579. Melbourne: CSIRO.

Crayn DM, Winter K and Smith JAC (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 USA 101: 3703–3708.

Crayn DM, Winter K, Schulte K and Smith JAC (2015) Photosynthetic pathways in Bromeliaceae: the phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species. Botanical Journal of the Linnean Society. DOI: 10.1111/boj.12275.

Cushman JC and Bohnert HJ (1997) Molecular genetics of crassulacean acid metabolism. Plant Physiology 113: 667–676.

Davis SC, LeBauer DS and Long SP (2014) Light to liquid fuel: theoretical and realized energy conversion efficiency of plants using crassulacean acid metabolism (CAM) in arid conditions. Journal of Experimental Botany 65: 3471–3478.

Dever LV, Boxall SF, Kneřová J and Hartwell J (2015) Transgenic perturbation of the decarboxylation phase of Crassulacean acid metabolism alters physiology and metabolism but has only a small effect on growth. Plant Physiology 167: 44–59.

Edwards EJ and Ogburn RM (2012) Angiosperm responses to a low‐CO2 world: CAM and C4 photosynthesis as parallel evolutionary trajectories. International Journal of Plant Sciences 173: 724–733.

Gehrig HH, Wood JA, Cushman MA, et al. (2005) Large gene family of phosphoenolpyruvate carboxylase in the crassulacean acid metabolism plant Kalanchoë pinnata (Crassulaceae) characterized by partial cDNA sequence analysis. Functional Plant Biology 32: 467–472.

Grams TEE, Borland AM, Roberts A, et al. (1997) On the mechanism of reinitiation of endogenous CAM‐rhythm by temperature changes. Plant Physiology 113: 1309–1317.

Griffiths H (1989) Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes. In: Lüttge U (ed.) Vascular Plants as Epiphytes. Evolution and Ecophysiology, pp. 42–86. Berlin: Springer.

Gustafsson MHG, Winter K and Bittrich V (2007) Diversity, phylogeny and classification of Clusia. In: Lüttge U (ed.) Clusia. A Woody Neotropical Genus of Remarkable Plasticity and Diversity, Ecological Studies, vol. 194, pp. 95–116. Berlin: Springer.

Hafke JB, Hafke Y, Smith JAC, Lüttge U and Thiel G (2003) Vacuolar malate uptake is mediated by an anion‐selective inward rectifier. The Plant Journal 35: 116–128.

Hartwell J, Nimmo G, Wilkins M, Jenkins G and Nimmo H (1999) Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression. Plant Journal 20: 333–342.

Holtum JAM, Aranda J, Virgo A, Gehrig HH and Winter K (2004) δ13C values and crassulacean acid metabolism in Clusia species from Panama. Trees: Structure and Function 18: 658–668.

Holtum JAM, Chambers D, Morgan D and Tan DKY (2011) Agave as a biofuel feedstock in Australia. Global Change Biology Bioenergy 3: 58–67.

Libik‐Konieczny M, Surówka E, Kuźniak E, Nosek M and Miszalski Z (2011) Effects of Botrytis cinerea and Pseudomonas syringae infection on the antioxidant profile of Mesembryanthemum crystallinum C3/CAM intermediate plant. Journal of Plant Physiology 168: 1052–1059.

Lüttge U (1988) Day‐night changes of citric‐acid levels in crassulacean acid metabolism: phenomenon and ecophysiological significance. Plant, Cell and Environment 11: 445–451.

Lüttge U (1998) Crassulacean acid metabolism. In: Raghavendra AS (ed.) Photosynthesis, pp. 136–149. Cambridge: Cambridge University Press.

Lüttge U (2000) The tonoplast functioning as the master switch for circadian regulation of crassulacean acid metabolism. Planta 211: 761–769.

Lüttge U (2002) CO2−concentrating: consequences in crassulacean acid metabolism. Journal of Experimental Botany 53: 2131–2142.

Lüttge U (2007a) Photosynthesis. In: Lüttge U (ed.) Clusia. A Woody Neotropical Genus of Remarkable Plasticity and Diversity, Ecological Studies, vol. 194, pp. 135–186. Berlin: Springer.

Lüttge U (2007b) Physiological ecology. In: Lüttge U (ed.) Clusia. A Woody Neotropical Genus of Remarkable Plasticity and Diversity, Ecological Studies, vol. 194, pp. 187–234. Berlin: Springer.

Lüttge U (2008) Stem CAM in arborescent succulents. Trees 22: 139–148.

Lüttge U (2010a) Ability of crassulacean acid metabolism plants to overcome interacting stresses in tropical environments. AoB Plants. DOI: 10.1093/aobpla/plq005.

Lüttge U (2010b) Photorespiration in phase III of crassulacean acid metabolism: Evolutionary and ecophysiological implications. Progress in Botany 72: 371–384.

Lüttge U and Ratajczak R (1997) The physiology, biochemistry and molecular biology of the plant vacuolar ATPase. In: Leigh R and Sanders D (eds) Advances in Botany: The Plant Vacuole, pp. 253–296. London: Academic Press.

Nobel PS (1996) High productivity of certain agronomic CAM species. In: Winter K and Smith JAC (eds) Crassulacean Acid Metabolism. Biochemistry, Ecophysiology and Evolution, pp. 255–265. Berlin: Springer.

Nosek M, Rozpądek P, Kornaś A, et al. (2015) Veinal‐mesophyll interaction under biotic stress. Journal of Plant Physiology 185: 52–56.

Ogburn RM and Edwards EJ (2010) The ecological water‐use strategies of succulent plants. Advances in Botanical Research 55: 179–225.

Osmond CB (1978) Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29: 379–414.

Pierce S, Winter K and Griffiths H (2002) Carbon isotope ratio and the extent of daily CAM use in Bromeliaceae. New Phytologist 156: 75–83.

Rascher U, Hütt M‐T, Siebke K, et al. (2001) Spatiotemporal variation of metabolism in a plant circadian rhythm: the biological clock as an assembly of coupled individual oscillators. Proceedings of the National Academy of Sciences of the USA 98: 11801–11805.

Silvera K, Santiago LS, Cushman JC and Winter K (2009) Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae. Plant Physiology 149: 1838–1847.

Silvera K, Winter K, Rodriguez BL, Albion RL and Cushman JC (2014) Multiple isoforms of phosphoenolpyruvate carboxylase in the Orchidaceae (subtribe Oncidiinae): implications for the evolution of crassulacean acid metabolism. Journal of Experimental Botany 65: 3623–3636.

Smith JAC (1989) Epiphytic bromeliads. In: Lüttge U (ed.) Vascular Plants as Epiphytes. Evolution and Ecophysiology, pp. 109–138. Berlin: Springer.

Smith JAC and Lüttge U (1985) Day‐night changes in leaf water relations associated with the rhythm of crassulacean acid metabolism in Kalanchoë daigremontiana. Planta 163: 272–282.

Taybi T, Patil S, Chollet R and Cushman J (2000) A minimal Ser/Thr protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in CAM‐induced leaves of Mesembryanthemum crystallinum. Plant Physiology 123: 1471–1482.

Vaasen A, Begerow D, Lüttge U and Hampp R (2002) The genus Clusia L.: molecular evidence for independent evolution of photosynthetic flexibility. Plant Biology 4: 86–93.

Winter K and Holtum JAM (2002) How closely do the δ13C values of CAM plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129: 1843–1851.

Winter K and Holtum JAM (2007) Environment or development? Lifetime net CO2 exchange and control of the expression of crassulacean acid metabolism in Mesembryanthemum crystallinum. Plant Physiology 143: 98–107.

Winter K and Holtum JAM (2014) Facultative crassulacean acid metabolism (CAM) plants: powerful tools for unravelling the functional elements of CAM photosynthesis. Journal of Experimental Botany 65: 3425–3441.

Winter K, Wallace BJ, Stocker GC and Roksandic Z (1983) Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57: 129–141.

Winter K, Medina E, Garcia V, Mayoral ML and Muniz R (1985) Crassulacean acid metabolism in roots of a leafless orchid, Campylocentrum tyrridion Garay & Dunsterv. Journal of Plant Physiology 118: 73–78.

Winter K, Aranda J and Holtum JAM (2005) Carbon isotope composition and water‐use efficiency in plants with crassulacean acid metabolism. Functional Plant Biology 32: 381–388.

Winter K, Garcia M and Holtum JAM (2008) On the nature of facultative and constitutive CAM: environmental and developmental control of CAM expression during early growth of Clusia, Kalanchoë, and Opuntia. Journal of Experimental Botany 59: 1829–1840.

Winter K, Garcia M and Holtum JAM (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: 4037–4042.

Winter K, Holtum JAM and Smith JAC (2015) Crassulacean acid metabolism: a continuous or discrete trait? New Phytologist. DOI: 10.1111/nph.13446.

Yang X, Cushman JC, Borland AM, et al. (2015) A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier world. New Phytologist 207: 491–504.

Further Reading

Hartwell J (2006) The circadian clock in CAM plants. In: Hall A and McWatters H (eds) Endogenous Plant Rhythms, pp. 211–236. Oxford: Blackwell.

Kluge M and Ting IP (1978) Crassulacean Acid Metabolism. Analysis of an Ecological Adaptation. Berlin: Springer.

Lüttge U (1987) Carbon dioxide and water demand: crassulacean acid metabolism (CAM), a versatile ecological adaptation exemplifying the need for integration in ecophysiological work. New Phytologist 106: 593–629.

Lüttge U (ed.) (1989) Vascular Plants as Epiphytes. Evolution and Ecophysiology. Berlin: Springer.

Lüttge U (1993) The role of crassulacean acid metabolism (CAM) in the adaptation of plants to salinity. New Phytologist 125: 59–71.

Lüttge U (2004) Ecophysiology of crassulacean acid metabolism (CAM). Annals of Botany 93: 629–652.

Lüttge U (2007) Clusia. A Woody Neotropical Genus of Remarkable Plasticity and Diversity. Ecological Studies, vol. 194. Berlin ‐ Heidelberg ‐ New York: Springer.

Lüttge U (2012) Ecophysiology of CAM photosynthesis. Chapter 6. In: Flexas J, Loreto F and Medrano H (eds) Terrestrial Photosynthesis in a Changing Environment. A Molecular, Physiological and Ecological Approach, pp. 71–84. Cambridge: Cambridge University Press.

Ting IP (1985) Crassulacean acid metabolism. Annual Review of Plant Physiology 36: 595–622.

Winter K and Smith JAC (eds) (1996) Crassulacean Acid Metabolism. Biochemistry, Ecophysiology and Evolution. Berlin: Springer.

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Lüttge, Ulrich(Nov 2015) Crassulacean Acid Metabolism. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001296.pub3]