Crassulacean acid metabolism: A continuous or discrete trait?

New Phytologist

Volumn 208, Issue 1, 2015, Pages 73-78

  Winter, Klaus ^a   Holtum, Joseph A M ^b   Smith, J Andrew C ^c  

^a SMITHSONIAN TROPICAL RESEARCH INSTITUTE   (Panama)

^b JAMES COOK UNIVERSITY   (Australia)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

C3 photosynthesis; CAM photosynthesis; Carbon isotope ratio 13C; Crassulacean acid metabolism (CAM); Evolution; Phosphoenolpyruvate carboxylase

Indexed keywords

ASSIMILATION EFFICIENCY; BIOENERGETICS; CARBON DIOXIDE; CARBON FIXATION; CARBON ISOTOPE; CRASSULACEAN ACID METABOLISM; ENZYME ACTIVITY; EVOLUTIONARY BIOLOGY; GENE EXPRESSION; ISOTOPIC RATIO; LIGHT AVAILABILITY;

CRASSULACEAE;

CARBON; CARBON DIOXIDE; WATER;

ADAPTATION; ECOSYSTEM; EVAPOTRANSPIRATION; EVOLUTION; GENETICS; LIGHT; METABOLISM; PHENOTYPE; PHOTOSYNTHESIS; PLANT; PLANT GENOME;

ADAPTATION, PHYSIOLOGICAL; BIOLOGICAL EVOLUTION; CARBON; CARBON DIOXIDE; CARBON ISOTOPES; ECOSYSTEM; GENOME, PLANT; LIGHT; PHENOTYPE; PHOTOSYNTHESIS; PLANT TRANSPIRATION; PLANTS; WATER;

EID: 84940467423     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13446     Document Type: Review

References (67)

1. 3 seeds and leaves as compared to the enzyme from maize. Plant Physiology 75: 387-392.
2. Arakaki M, Christin P-A, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ. 2011. Contemporaneous and recent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences, USA 108: 8379-8384.
3. 4 species Cleome gynandra. Journal of Experimental Botany 65: 3557-3566.
4. Baresch A, Smith JAC, Winter K, Valerio AC, Jaramillo C. 2011. Karatophyllum bromelioides L.D. Gómez revisited: a probable CAM fossil bromeliad. American Journal of Botany 98: 1905-1908.
5. Borland AM, Griffiths H, Hartwell J, 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.
6. Borland AM, Zambrano VAB, Ceusters K, 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.
7. 2 during a diel Crassulacean acid metabolism cycle in Kalanchoe daigremontiana and Kalanchoe pinnata. Plant, Cell & Environment 32: 567-576.
8. 4 plants. Plant Physiology 143: 4-10.
9. Cernusak LA, Ubierna N, Winter K, Holtum JAM, Marshall JD, Farquhar GD. 2013. Environmental and physiological determinants of carbon isotope discrimination in terrestrial plants. New Phytologist 200: 950-965.
10. 4 and CAM metabolism. Journal of Experimental Botany 65: 3609-3621.
11. 3 based on carbon isotope ratios for 1893 species. Botanical Journal of the Linnean Society 178: 169-221.
12. Crayn DM, Winter K, 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, USA 101: 3703-3708.
13. Darwin F. 1898. Observations on stomata. Philosophical Transactions of the Royal Society of London Series B 190: 531-621.
14. Davis SC, Dohleman FG, Long SP. 2011. The global potential for Agave as a biofuel feedstock. Global Change Biology Bioenergy 3: 68-78.
15. Dodd AN, Kusakina J, Hall A, Gould PD, Hanaoka M. 2014. The circadian regulation of photosynthesis. Photosynthesis Research 119: 181-190.
16. 4 photosynthesis as parallel evolutionary trajectories. International Journal of Plant Sciences 173: 724-733.
17. Ellenberg H. 1981. Ursachen des Vorkommens und Fehlens von Sukkulenten in den Trockengebieten der Erde. Flora 171: 114-169.
18. Gibson AC. 1982. The anatomy of succulence. In: Ting IP, Gibbs M, eds. Crassulacean acid metabolism. Rockville, MD, USA: American Society of Plant Physiologists, 1-17.
19. Griffiths H, Cousins AB, Badger MR, von Caemmerer S. 2007. Discrimination in the dark. Resolving the interplay between metabolic and physical constraints to phosphoenolpyruvate carboxylase activity during the crassulacean acid metabolism cycle. Plant Physiology 143: 1055-1067.
20. Hancock L, Edwards EJ. 2014. Phylogeny and the inference of evolutionary trajectories. Journal of Experimental Botany 65: 3491-3498.
21. Harris FS, Martin CE. 1991. Plasticity in the degree of CAM-cycling and its relationship to drought stress in five species of Talinum (Portulacaceae). Oecologia 86: 575-584.
22. Hartwell J. 2006. The circadian clock in CAM plants. In: Hall A, McWatters H, eds. Endogenous plant rhythms. Oxford, UK: Blackwell, 211-236.
23. Hartwell J, Smith LH, Wilkins MB, Jenkins GI, Nimmo HG. 1996. Higher plant phosphoenolpyruvate carboxylase kinase is regulated at the level of translatable mRNA in response to light or a circadian rhythm. Plant Journal 10: 1071-1078.
24. 4 dicarboxylic acid pathway of photosynthesis. Biochemical Journal 106: 141-146.
25. Herrera A. 2009. Crassulacean acid metabolism and fitness under water deficit stress: if not for carbon gain, what is facultative CAM good for? Annals of Botany 103: 645-653.
26. Holtum JAM, Chambers D, Morgan D, Tan DKY. 2011. Agave as a biofuel feedstock in Australia. Global Change Biology Bioenergy 3: 58-67.
27. Holtum JAM, Smith JAC, Neuhaus HE. 2005. Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Functional Plant Biology 32: 429-449.
28. Horn JW, Xi Z, Riina R, Peirson JA, Yang Y, Dorsey BL, Berry PE, Davis CC, Wurdack KJ. 2014. Evolutionary bursts in Euphorbia (Euphorbiaceae) are linked with photosynthetic pathway. Evolution 68: 3485-3504.
29. 13C-analysis of Crassulacean acid metabolism (CAM) in Kalanchoë (Crassulaceae) species of Africa and Madagascar. Botanica Acta 106: 320-324.
30. 2-Austausch und der Abgabe von Wasserdampf durch Bryophyllum daigremontianum Berg. Planta 77: 212-223.
31. i dikinase in crassulacean acid metabolism. Naturwissenschaften 8: 414-415.
32. Kluge M, Ting IP. 1978. Crassulacean acid metabolism. Analysis of an ecological adaptation. Berlin, Germany: Springer.
33. 2 by tobacco leaves. Plant Physiology 34: 123-127.
34. Lüttge U. 2006. Photosynthetic flexibility and ecophysiological plasticity: questions and lessons from Clusia, the only CAM tree, in the neotropics. New Phytologist 171: 7-25.
35. Martinoia E, Meyer S, De Angeli A, Nagy R. 2012. Vacuolar transporters in their physiological context. Annual Review of Plant Biology 63: 183-213.
36. Maxwell K, Borland AM, Haslam RP, Helliker BR, Roberts A, Griffiths H. 1999. Modulation of Rubisco activity during the diurnal phases of the crassulacean acid metabolism plant Kalanchoë daigremontiana. Plant Physiology 121: 849-856.
37. 2 fixation and acid accumulation in Kalanchoë daigremontiana. Australian Journal of Plant Physiology 8: 641-649.
38. Nelson EA, Sage RF. 2008. Functional constraints of CAM leaf anatomy: tight cell packing is associated with increased CAM function across a gradient of CAM expression. Journal of Experimental Botany 59: 1841-1850.
39. Nimmo HG. 2000. The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science 5: 75-80.
40. Nobel PS. 1988. Environmental biology of agaves and cacti. Cambridge, UK: Cambridge University Press.
41. Ogburn RM, Edwards EJ. 2010. The ecological water-use strategies of succulent plants. Advances in Botanical Research 55: 179-225.
42. Osmond CB. 1978. Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29: 379-414.
43. Pfeffer W. 1897. Pflanzenphysiologie. Ein Handbuch der Lehre vom Stoffwechsel und Kraftwechsel in der Pflanze, Erster Band: Stoffwechsel, 2nd edn. Leipzig, Germany: Wilhelm Engelmann.
44. Pierce S, Winter K, Griffiths H. 2002. Carbon isotope ratio and the extent of daily CAM use in Bromeliaceae. New Phytologist 156: 75-83.
45. Silvera K, Santiago LS, Cushman JC, Winter K. 2009. Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae. Plant Physiology 149: 1838-1847.
46. Silvera K, Santiago LS, Winter K. 2005. Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection for weak and strong modes. Functional Plant Biology 32: 397-407.
47. Silvera K, Winter K, Rodriguez BL, Albion RL, 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.
48. Smith JAC, Bryce JH. 1992. Metabolite compartmentation and transport in CAM plants. In: Tobin AK, ed. Plant organelles: compartmentation of metabolism in photosynthetic cells. Cambridge, UK: Cambridge University Press, 141-167.
49. Smith JAC, Ingram J, Tsiantis MS, Barkla BJ, Bartholomew DM, Bettey M, Pantoja O, Pennington AJ. 1996. Transport across the vacuolar membrane in CAM plants. In: Winter K, Smith JAC, eds. Crassulacean acid metabolism: biochemistry, ecophysiology and evolution. Berlin, Germany: Springer, 53-71.
50. Teeri JA, Tonsor SJ, Turner M. 1981. Leaf thickness and carbon isotope composition in the Crassulaceae. Oecologia 50: 367-369.
51. West-Eberhard MJ, Smith JAC, Winter K. 2011. Photosynthesis, reorganized. Science 332: 311-312.
52. Wilkins MB. 1959. An endogenous rhythm in the rate of carbon dioxide output of Bryophyllum I. Some preliminary experiments. Journal of Experimental Botany 10: 377-390.
53. von Willert DJ, Armbrüster N, Drees T, Zaborowski M. 2005. Welwitschia mirabilis: CAM or not CAM - what is the answer? Functional Plant Biology 32: 389-395.
54. Winter K. 1982. Properties of phosphoenolpyruvate carboxylase in rapidly prepared, desalted leaf extracts of the crassulacean acid metabolism plant Mesembryanthemum crystallinum. Planta 154: 298-308.
55. Winter K, Aranda J, Holtum JAM. 2005. Carbon isotope composition and water-use efficiency in plants with crassulacean acid metabolism. Functional Plant Biology 32: 381-388.
56. Winter K, Garcia M, 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.
57. 3 mode. Journal of Experimental Botany 62: 4037-4042.
58. 2 fixed during day and night? Plant Physiology 129: 1843-1851.
59. Winter K, Holtum JAM. 2011. Induction and reversal of crassulacean acid metabolism in Calandrinia polyandra: effects of soil moisture and nutrients. Functional Plant Biology 38: 576-582.
60. Winter K, 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.
61. 3 photosynthesis to crassulacean acid metabolism in Mesembryanthemum crystallinum growing in its natural environment. Oecologia 34: 225-237.
62. Winter K, Medina E, Garcia V, Mayoral ML, Muniz R. 1985. Crassulacean acid metabolism in roots of a leafless orchid, Campylocentrum tyrridion Garay & Dunsterv. Journal of Plant Physiology 118: 73-78.
63. Winter K, Smith JAC, eds. 1996. Crassulacean acid metabolism: biochemistry, ecophysiology and evolution. Berlin, Germany: Springer.
64. Winter K, Wallace BJ, Stocker GC, Roksandic Z. 1983. Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57: 129-141.
65. Winter K, Ziegler H. 1992. Induction of crassulacean acid metabolism in Mesembryanthemum crystallinum increases reproductive success under conditions of drought and salinity stress. Oecologia 92: 475-479.
66. Yang X, Cushman JC, Borland AM, Edwards EJ, Wullschleger SD, Tuskan GA, Owen NA, Griffiths H, Smith JAC, De Paoli HC 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.
67. Zambrano VAB, Lawson T, Olmos E, Fernández-García N, Borland AM. 2014. Leaf anatomical traits which accommodate the facultative engagement of crassulacean acid metabolism in tropical trees of the genus Clusia. Journal of Experimental Botany 65: 3513-3523.