Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
EVOLUTIONARY REVIEW

Evolution along the crassulacean acid metabolism continuum

Katia Silvera A , Kurt M. Neubig B , W. Mark Whitten B , Norris H. Williams B , Klaus Winter C and John C. Cushman A D

A Department of Biochemistry and Molecular Biology, MS200, University of Nevada, Reno, NV 89557-0200, USA.

B Florida Museum of Natural History, University of Florida, Gainesville, FL 32611-7800, USA.

C Smithsonian Tropical Research Institute, PO Box 0843-03092, Balboa, Ancón, Republic of Panama.

D Corresponding author. Email: jcushman@unr.edu

This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.

Functional Plant Biology 37(11) 995-1010 http://dx.doi.org/10.1071/FP10084
Submitted: 15 April 2010  Accepted: 2 August 2010   Published: 22 October 2010

Abstract

Crassulacean acid metabolism (CAM) is a specialised mode of photosynthesis that improves atmospheric CO2 assimilation in water-limited terrestrial and epiphytic habitats and in CO2-limited aquatic environments. In contrast with C3 and C4 plants, CAM plants take up CO2 from the atmosphere partially or predominantly at night. CAM is taxonomically widespread among vascular plants and is present in many succulent species that occupy semiarid regions, as well as in tropical epiphytes and in some aquatic macrophytes. This water-conserving photosynthetic pathway has evolved multiple times and is found in close to 6% of vascular plant species from at least 35 families. Although many aspects of CAM molecular biology, biochemistry and ecophysiology are well understood, relatively little is known about the evolutionary origins of CAM. This review focuses on five main topics: (1) the permutations and plasticity of CAM, (2) the requirements for CAM evolution, (3) the drivers of CAM evolution, (4) the prevalence and taxonomic distribution of CAM among vascular plants with emphasis on the Orchidaceae and (5) the molecular underpinnings of CAM evolution including circadian clock regulation of gene expression.

Additional keywords: phosphoenolpyruvate carboxylase, photosynthesis, δ13C.


References

Atwood JT 1986 The size of the Orchidaceae and the systematic distribution of epiphytic orchids. Selbyana 7 171 186

Barfuss MHJ Samuel R Till W Stuessy TF 2005 Phylogenetic relationships in subfamily Tillandsioideae (Bromeliaceae) based on DNA sequence data from seven plastid regions. American Journal of Botany 92 337 351
doi:10.3732/ajb.92.2.337

Bläsing O Westhoff P Svensson P 2000 Evolution of C4 phosphoenolpyruvate carboxylases in Flaveria, a conserved serine residue in the carboxyl-terminal part of the enzyme is a major determinant for C4-specific characteristics. Journal of Biological Chemistry 275 27 917 27 923

Bläsing O Ernst K Streubel M Westhoff P Svensson P 2002 The non-photosynthetic phosphoenolpyruvate carboxylases of the C4 dicot Flaveria trinervia – implications for the evolution of C4 photosynthesis. Planta 215 448 456
doi:10.1007/s00425-002-0757-x

Borland AM Dodd AN 2002 Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest. Journal of Experimental Botany 29 707 716

Borland AM Taybi T 2004 Synchronization of metabolic processes in plants with crassulacean acid metabolism. Journal of Experimental Botany 55 1255 1265
doi:10.1093/jxb/erh105

Borland AM Tecsi LI Leegood RC Walker RP 1998 Inducibility of crassulacean acid metabolism (CAM) in Clusia species; physiological/biochemical characterisation and intercellular localisation of carboxylation processes in three species which show different degrees of CAM. Planta 205 342 351 doi:10.1007/s004250050329

Borland AM Hartwell J Jenkins GI Wilkins MB Nimmo HG 1999 Metabolite control overrides circadian regulation of phosphoenolpyruvate carboxylase kinase and CO2 fixation in crassulacean acid metabolism. Plant Physiology 121 889 896 doi:10.1104/pp.121.3.889

Bouetard A Lefeuvre P Gigant R Bory S Pignal M Besse P Grisoni M 2010 Evidence of transoceanic dispersion of the genus Vanilla based on plastid DNA phylogenetic analysis. Molecular Phylogenetics and Evolution 55 621 630 doi:10.1016/j.ympev.2010.01.021

Boxall SF Foster JM Bohnert HJ Cushman JC Nimmo HG Hartwell J 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 doi:10.1104/pp.104.054577

Brulfert J Queiroz O 1982 Photoperiodism and crassulacean acid metabolism. Planta 154 339 343 doi:10.1007/BF00393912

Cameron KM (2005) Molecular systematics of Orchidaceae: a literature review and an example using five plastid genes. In ‘Proceedings of the 17th World Orchid Conference 2002 – Sustaining orchids for the future’. (Eds H Nair, J Arditti) pp. 80–96. (Kota Kinabalu, Natural History Publications: Borneo)

Ceusters J Borland AM Londers E Verdoodt V Godts C De Proft MP 2008 Diel shifts in carboxylation pathway and metabolite dynamics in the CAM bromeliad Aechmea ‘Maya’ in response to elevated CO2. Annals of Botany 102 389 397 doi:10.1093/aob/mcn105

Chase MW 1988 Obligate twig epiphytes: a distinct subset of Neotropical orchidaceous epiphytes. Selbyana 10 24 30

Chase MW , Cameron KM , Barrett RL , Freudenstein JV (2003) DNA data and Orchidaceae systematics: a new phylogenetic classification. In ‘Orchid conservation’. (Eds KW Dixon, SP Kell, RL Barrett, PJ Cribb) pp. 69–89. (Natural History Publications: Borneo)

Chase MW Hanson L Albert VA Whitten WM Williams NH 2005 Life history evolution and genome size in subtribe Oncidiinae (Orchidaceae). Annals of Botany 95 191 199
doi:10.1093/aob/mci012

Chollet R Vidal J O’Leary MH 1996 Phosphoenolpyruvate carboxylase: a ubiquitous, highly regulated enzyme in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47 273 298 doi:10.1146/annurev.arplant.47.1.273

Christopher JT Holtum JAM 1996 Patterns of carbohydrate partitioning in the leaves of crassulacean acid metabolism species during deacidification. Plant Physiology 112 393 399

Christopher JT Holtum JAM 1998 Carbohydrate partitioning in the leaves of Bromeliaceae performing C3 photosynthesis or crassulacean acid metabolism. Australian Journal of Plant Physiology 25 371 376
doi:10.1071/PP98005

Cockburn W 1985 Variation in photosynthetic acid metabolism in vascular plants: CAM and related phenomena. New Phytologist 101 3 24 doi:10.1111/j.1469-8137.1985.tb02815.x

Cockburn W Ting IP Sternberg LO 1979 Relationships between stomatal behavior and internal carbon dioxide concentration in crassulacean acid metabolism plants. Plant Physiology 63 1029 1032 doi:10.1104/pp.63.6.1029

Conran JG Bannister JM Lee DE 2009 Earliest orchid macrofossils: early Miocene Dendrobium and Earina (Orchidaceae: Epidendroideae) from New Zealand. American Journal of Botany 96 466 474 doi:10.3732/ajb.0800269

Crayn DM Winter K Smith JAC 2004 Multiple origins of crassulacan 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 3703 3708 doi:10.1073/pnas.0400366101

Cribb P , Govaerts R (2005) Just how many orchids are there? In ‘Proceedings of the 18th World Orchid Conference’. (Eds A Raynal-Roques, A Rogeuenant, D Prat) pp. 161–172. (Naturalia Publications: Dijon, France)

Cushman JC 2001 Crassulacean acid metabolism. A plastic photosynthetic adaptation to arid environments. Plant Physiology 127 1439 1448 doi:10.1104/pp.010818

Cushman JC Bohnert HJ 1999 Crassulacean acid metabolism: molecular genetics. Annual Review of Plant Physiology and Plant Molecular Biology 50 305 332 doi:10.1146/annurev.arplant.50.1.305

Cushman JC Borland AM 2002 Induction of crassulacean acid metabolism by water limitation. Plant, Cell & Environment 25 295 310 doi:10.1046/j.0016-8025.2001.00760.x

Cushman JC Meyer G Michalowski CB Schmitt JM Bohnert HJ 1989 Salt stress leads to differential expression of two isogenes of phosphoenolpyruvate carboxylase during crassulacean acid metabolism induction in the common ice plant. The Plant Cell 1 715 725

Cushman JC Agarie S Albion RL Elliot SM Taybi T Borland AM 2008 a Isolation and characterization of mutants of ice plant, Mesembryanthemum crystallinum, deficient in crassulacean acid metabolism. Plant Physiology 147 228 238
doi:10.1104/pp.108.116889

Cushman JC Tillett RL Wood JA Branco JM Schlauch KA 2008 b Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photosynthesis and crassulacean acid metabolism (CAM). Journal of Experimental Botany 59 1875 1894 doi:10.1093/jxb/ern008

Dodd AN Borland AM Haslam RP Griffiths H Maxwell K 2002 Crassulacean acid metabolism: plastic, fantastic. Journal of Experimental Botany 53 569 580 doi:10.1093/jexbot/53.369.569

Dodd AN Griffiths H Taybi T Cushman JC Borland AM 2003 Integrating diel starch metabolism with the circadian and environmental regulation of crassulacean acid metabolism in Mesembryanthemum crystallinum. Planta 6 789 797

Dressler R (1993) ‘Phylogeny and classification of the orchid family.’ (Dioscorides Press: Portland, OR)

Earnshaw MJ Winter K Ziegler H Sticher W Cruttwell NEG et al 1987 Altitudinal changes in the incidence of crassulacean acid metabolism in vascular epiphytes and related life forms in Papua New Guinea. Oecologia 73 566 572
doi:10.1007/BF00379417

Edwards EJ Osborne CP Strömberg CAE Smith SA C4 Grasses Consortium 2010 The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328 587 591 doi:10.1126/science.1177216

Ehleringer JR Monson RK 1993 Evolutionary and ecological aspects of photosynthetic pathway variation. Annual Review of Ecology and Systematics 24 411 439 doi:10.1146/annurev.es.24.110193.002211

Ehleringer JR , Osmond CB (1989) Stable isotopes. In ‘Plant physiological ecology’. (Ed. P Rundel) pp. 255–280. (Chapman and Hall: London)

Engelmann S Bläsing OE Westhoff P Svensson P 2002 Serine 774 and amino acids 296 to 437 comprise the major C4 determinants of the C4 phosphoenolpyruvate carboxylase of Flaveria trinervia. FEBS Letters 524 11 14 doi:10.1016/S0014-5793(02)02975-7

Engelmann S Bläsing OE Gowik U Svensson P Westhoff P 2003 Molecular evolution of C4 phosphoenolpyrvate carboxylase in the genus Flaveria – a gradual increase from C3 to C4 characteristics. Planta 217 717 725 doi:10.1007/s00425-003-1045-0

Eriksson ME Millar AJ 2003 The circadian clock. A plant’s best friend in a spinning world. Plant Physiology 132 732 738 doi:10.1104/pp.103.022343

Frimert V Kluge M Smith JAC 1986 Net CO2 output by CAM plants in the light: the role of leaf conductance. Physiologia Plantarum 68 353 358 doi:10.1111/j.1399-3054.1986.tb03365.x

Furumoto T Hata S Izui K 2000 Isolation and characterization of cDNAs for differentially accumulated transcripts between mesophyll cells and bundle sheath strands of maize leaves. Plant & Cell Physiology 41 1200 1209 doi:10.1093/pcp/pcd047

Gehrig HH Taybi T Kluge M Brulfert J 1995 Identification of multiple PEPC isogenes in leaves of the facultative crassulacean acid metabolism (CAM) plant Kalanchoë blossfeldiana Poelln. cv. Tom Thumb. FEBS Letters 377 399 402 doi:10.1016/0014-5793(95)01397-0

Gehrig HH Heute V Kluge M 2001 New partial sequences of phosphoenolpyruvate carboxylase as molecular phylogenetic markers. Molecular Phylogenetics and Evolution 20 262 274 doi:10.1006/mpev.2001.0973

Gehrig HH Aranda J Cushman MA Virgo A Cushman JC Hammel BE Winter K 2003 Cladogram of Panamanian Clusia based on nuclear DNA: implications for the origins of crassulacean acid metabolism. Plant Biology 5 59 70 doi:10.1055/s-2003-37983

Gehrig HH Wood JA Cushman MA Virgo A Cushman JC Winter K 2005 Large gene family of phosphoenolpyruvate carboxylase in the crassulacean acid metabolism plant Kalanchoë pinnata (Crassulaceae). Functional Plant Biology 32 467 472 doi:10.1071/FP05079

Gibson AC (1982) The anatomy of succulence. In ‘Crassulacean acid metabolism’. (Eds I Ting, M Gibbs) pp. 1–17. (American Society of Plant Physiologists: Rockville, MD)

Good-Avila SV Souza V Gaut BS Eguiarte LE 2006 Timing and rate of speciation in Agave (Agavaceae). Proceedings of the National Academy of Sciences of the United States of America 103 9124 9129 doi:10.1073/pnas.0603312103

Gravendeel B Smithson A Slik FJW Schuiteman A 2004 Epiphytism and pollinator specialization: drivers for orchid diversity? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 359 1523 1535 doi:10.1098/rstb.2004.1529

Griffiths H 1988 Crassulacean acid metabolism: a re-appraisal of physiological plasticity in form and function. Advances in Botanical Research 15 43 92 doi:10.1016/S0065-2296(08)60044-0

Griffiths H (1989) Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes. In ‘Vascular plants as epiphytes: evolution and ecophysiology’. (Ed. U Lüttge) pp. 42–86. (Springer-Verlag: Berlin)

Griffiths H 1992 Carbon isotope discrimination and the integration of carbon assimilation pathways in terrestrial CAM plants. Plant, Cell & Environment 15 1051 1062 doi:10.1111/j.1365-3040.1992.tb01655.x

Griffiths H Helliker B Roberts A Haslam RP Girnus J Robe WE Borland AM Maxwell K 2002 Regulation of Rubisco activity in crassulacean acid metabolism plants: better late than never. Functional Plant Biology 29 689 696 doi:10.1071/PP01212

Gustafson M , Winter K , Bittrich V (2007) Diversity, phylogeny and classification of Clusia. In ‘Clusia: a woody neotropical genus of remarkable plasticity and diversity’. (Ed. U Lüttge) pp. 95–116. (Springer-Verlag: Berlin)

Hartwell J (2005 a) The circadian clock in CAM plants. In ‘Endogenous plant rhythms. Annual Plant Reviews. Vol. 21’. (Eds AJW Hall, HG McWatters) pp. 211–236. (Blackwell: Oxford)

Hartwell J 2005 b The co-ordination of central plant metabolism by the circadian clock. Biochemical Society Transactions 33 945 948 doi:10.1042/BST20050945

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. The Plant Journal 10 1071 1078 doi:10.1046/j.1365-313X.1996.10061071.x

Hartwell J Gill A Nimmo GA Wilkins MB Jenkins GI Nimmo HG 1999 Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of gene expression. The Plant Journal 20 333 342 doi:10.1046/j.1365-313X.1999.t01-1-00609.x

Häusler RE Baur B Scharte J Teichmann T Elcks M Fischer KL Flugge U Schubert S Weber A Fischer K 2000 Plastidic metabolite transporters and their physiological functions in the inducible crassulacean acid metabolism plant Mesembryanthemum crystallinum. The Plant Journal 24 285 296 doi:10.1046/j.1365-313x.2000.00876.x

Hibberd JM Covshoff S 2010 The regulation of gene expression required for C4 photosynthesis. Annual Reviews of Plant Biology 61 181 207 doi:10.1146/annurev-arplant-042809-112238

Holtum JAM Winter K 1999 Degrees of crassulacean acid metabolism in tropical epiphytic and lithophytic ferns. Australian Journal of Plant Physiology 26 749 757 doi:10.1071/PP99001

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

Holtum JAM Smith JAC Neuhaus H 2005 Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism. Functional Plant Biology 32 429 449
doi:10.1071/FP04189

Holtum JAM Winter K Weeks MA Sexton TR 2007 Crassulacean acid metabolism of the ZZ plant, Zamioculcas zamiifolia (Araceae). American Journal of Botany 94 1670 1676 doi:10.3732/ajb.94.10.1670

Jabaily RS Sytsma KJ 2010 Phylogenetics of Puya (Bromeliaceae): placement, major lineages, and evolution of Chilean species. American Journal of Botany 97 337 356 doi:10.3732/ajb.0900107

Keeley JE (1996) Aquatic CAM photosynthesis. In ‘Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution’. (Eds K Winter, JAC Smith) pp. 281–295. (Springer-Verlag: Berlin)

Keeley J 1998 CAM photosynthesis in submerged aquatic plants. Botanical Review 64 121 175 doi:10.1007/BF02856581

Kellogg EA (1999) Phylogenetic aspects of the evolution of C4 photosynthesis. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 411–444. (Academic Press: San Diego)

Klak C Khunou A Reeves G Hedderson T 2003 A phylogenetic hypothesis for the Aizoaceae (Caryophyllales) based on four plastid DNA regions. American Journal of Botany 90 1433 1445 doi:10.3732/ajb.90.10.1433

Klak C Reeves G Hedderson T 2004 Unmatched tempo of evolution in Southern African semi-desert ice plants. Nature 427 63 65 doi:10.1038/nature02243

Kluge M Brulfert J Ravelomanana D Lipp J Ziegler H 1991 Crassulacean acid metabolism in Kalanchoë species collected in various climatic zones of Madagascar: a survey by δ13C analysis. Oecologia 88 407 414 doi:10.1007/BF00317586

Kluge M Brulfert J Lipp J Ravelomanana D Ziegler H 1993 A comparative study of δ13C analysis of crassulascean acid metabolism (CAM) in Kalanchoë (Crassulaceae) species of Africa and Madagascar. Botanica Acta 106 320 324

Kluge M Razanoelisoa B Brulfert J 2001 Implications of genotypic diversity and plasticity in the ecophysiological success of CAM plants, examined by studies on the vegetation of Madagascar. Plant Biology 3 214 222
doi:10.1055/s-2001-15197

Kore-eda S Noake C Ohishi M Ohnishi J Cushman JC 2005 Transcriptional profiles of organellar metabolite transporters during induction of crassulacean acid metabolism in Mesembryanthemum crystallinum. Functional Plant Biology 32 451 466 doi:10.1071/FP04188

Kreft H Jetz W 2007 Global patterns and determinants of vascular plant diversity. Proceedings of the National Academy of Sciences of the United States of America 104 5925 5930 doi:10.1073/pnas.0608361104

Kreps JA Wu Y Chang HS Zhu T Wang X Harper JF 2002 Transcriptome changes for Arabidopsis in reponse to salt, osmotic and cold stress. Plant Physiology 130 2129 2141 doi:10.1104/pp.008532

Lee HSJ Griffiths H 1987 Induction and repression of CAM in Sedum telephium L. in response to photoperiod and water stress. Journal of Experimental Botany 38 834 841 doi:10.1093/jxb/38.5.834

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 doi:10.1111/j.1469-8137.1987.tb00163.x

Lüttge U 2003 Circadian rhythmicity: is the ‘biological clock’ hardware or software? Progress in Botany 64 277 319

Martin SL Davis R Protti P Lin T-C Lin S-H Martin CE 2005 The occurrence of crassulacean acid metabolism in epiphytic ferns, with an emphasis on the Vittariaceae. International Journal of Plant Sciences 166 623 630
doi:10.1086/430334

Maxwell K 2002 Resistance is useful: diurnal patterns of photosynthesis in C3 and crassulacean acid metabolism epiphytic bromeliads. Functional Plant Biology 29 679 687 doi:10.1071/PP01193

Maxwell K von Caemmerer S Evans JR 1997 Is a low internal conductance to CO2 diffusion a consequence of succulence in plants with crassulacean acid metabolism? Australian Journal of Plant Physiology 24 777 786 doi:10.1071/PP97088

Maxwell K Borland AM Haslam RP Helliker BR Roberts A Griffiths H 1999 Modulation of ribulose-1,5-bisphosphate carboxylase activity during the diurnal phases of the crassulacean acid metabolism plant Kalanchoë daigremontiana. Plant Physiology 121 849 856 doi:10.1104/pp.121.3.849

Monson RK 1989 On the evolutionary pathways resulting in C4 photosynthesis and crassulacean acid metabolism (CAM). Advances in Ecological Research 19 57 110 doi:10.1016/S0065-2504(08)60157-9

Monson R (1999) The origins of C4 genes and evolutionary patterns in the C4 metabolic phenotype. In ‘C4 plant biology’. (Eds RF Sage, RK Monson) pp. 377–410. (Academic Press: San Diego)

Monson R 2003 Gene duplication, neofunctionalization, and the evolution of C4 photosynthesis. International Journal of Plant Sciences 164 S43 S54 doi:10.1086/368400

Moore PD 1982 Evolution of photosynthetic pathways in flowering plants. Nature 295 647 648 doi:10.1038/295647a0

Motomura H Yukawa T Ueno O Kagawa A 2008 The occurrence of crassulacean acid metabolism in Cymbidium (Orchidaceae) and its ecological and evolutionary implications. Journal of Plant Research 121 163 177 doi:10.1007/s10265-007-0144-6

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 doi:10.1093/jxb/erm346

Nelson EA Sage TL Sage RF 2005 Functional leaf anatomy of plants with crassulacean acid metabolism. Functional Plant Biology 32 409 419 doi:10.1071/FP04195

Nimmo HG 2000 The regulation of phosphoenolpyruvate carboxylase in CAM plants. Trends in Plant Science 5 75 80 doi:10.1016/S1360-1385(99)01543-5

Nobel PS (1996) High productivities of certain agronomic CAM species. In ‘Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution’. (Eds K Winter, JAC Smith) pp. 255–265. (Springer-Verlag: Berlin)

Osmond CB 1978 Crassulacean acid metabolism: a curiosity in context. Annual Review of Plant Physiology 29 379 414 doi:10.1146/annurev.pp.29.060178.002115

Osmond CB (1982) Carbon cycling and stability of the photosynthetic apparatus in CAM. In ‘Crassulacean acid metabolism’. (Eds I Ting, M Gibbs) pp. 112–127. (American Society of Plant Physiologists: Rockville, MD)

Paul MJ Loos K Stitt M Ziegler P 1993 Starch-degrading enzymes during the induction of CAM in Mesembryanthemum crystallinum. Plant, Cell & Environment 16 531 538 doi:10.1111/j.1365-3040.1993.tb00900.x

Pearson PN Palmer MR 2000 Atmospheric carbon dioxide concentrations over the past 60 million years. Nature 406 695 699 doi:10.1038/35021000

Pfahl J , Campacci MA , Holland Baptista D , Tigges H , Shaw J , Cribb P , George A , Kreuz K , Wood J (2008) World checklist of the Orchidaceae. The Board of Trustees of the Royal Botanic Gardens, Kew. Available at: http://www.kew.org/wcsp/ [Accessed 13 April 2010]

Pierce S Winter K Griffiths H 2002 Carbon isotope ratio and the extent of daily CAM use by Bromeliaceae. New Phytologist 156 75 83 doi:10.1046/j.1469-8137.2002.00489.x

Pilon-Smits EAH , ‘t Hart H , van Brederode J (1996) Evolutionary aspects of crassulacean acid metabolism in the crassulaceae. In ‘Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution’. (Eds K Winter, JAC Smith) pp. 349–359. (Springer-Verlag: Berlin)

Pridgeon A , Cribb P , Chase M , Rasmussen F (1999–2009) ‘Genera Orchidacearum.’ (Oxford University Press: Oxford)

Raven JA , Spicer RA (1996) The evolution of crassulacean acid metabolism. In ‘Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution’. (Eds K Winter, JAC Smith) pp. 360–385. (Springer-Verlag: Berlin)

Ritz D Kluge M Veith HJ 1986 Mass-spectrometric evidence for the double-carboxylation pathway of malate synthesis by crassulacean acid metabolism plants in light. Planta 167 284 291 doi:10.1007/BF00391428

Roberts A Borland AM Griffiths H 1997 Discrimination processes and shifts in carboxylation during the phases of crassulacean acid metabolism. Plant Physiology 113 1283 1292

Sage RF 2001 Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome. Plant Biology 3 202 213
doi:10.1055/s-2001-15206

Sage RF 2004 The evolution of C4 photosynthesis. New Phytologist 161 341 370 doi:10.1111/j.1469-8137.2004.00974.x

Sánchez R Cejudo FJ 2003 Identification and expression analysis of a gene encoding a bacterial-type phosphoenolpyruvate carboxylase from Arabidopsis and rice. Plant Physiology 132 949 957 doi:10.1104/pp.102.019653

Schuber M Kluge K 1981 In situ studies on crassulacean acid metabolism in Sedum acre L. and Sedum mite Gil. Oecologia 50 82 87 doi:10.1007/BF00378797

Silvera K Santiago LS Winter K 2005 Distribution of crassulacean acid metabolism in orchids of Panama: evidence of selection of weak and strong modes. Functional Plant Biology 32 397 407 doi:10.1071/FP04179

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 doi:10.1104/pp.108.132555

Silvera K Santiago LS Cushman JC Winter K 2010 The incidence of crassulacean acid metabolism in the Orchidaceae derived from carbon isotope ratios: a checklist of the flora of Panama and Costa Rica. Botanical Journal of the Linnean Society 163 194 222 doi:10.1111/j.1095-8339.2010.01058.x

Sipes DL Ting IP 1985 Crassulacean acid metabolism and crassulacean acid metabolism modifications in Peperomia camptotricha. Plant Physiology 77 59 63 doi:10.1104/pp.77.1.59

Smith JAC (1984) Water relations in CAM plants. In ‘Physiological ecology of CAM plants’. (Ed. E Medina) pp. 30–51. (CIET (Unesco-IVIC): Caracas, Venezuela)

Smith JAC , Bryce JH (1992) Metabolite compartmentation and transport in CAM plants. In ‘Plant organelles’. (Ed. AK Tobin) pp. 141–167. (Cambridge University Press: Cambridge)

Smith JAC , Winter K (1996) Taxonomic distribution of crassulacean acid metabolism. In ‘Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution’. (Ed. K Winter, JAC Smith) pp. 427–436. (Springer-Verlag: Berlin)

Smith JAC Griffiths H Lüttge U 1986 Comparative ecophysiology of CAM and C3 bromeliads. I. The ecology of the Bromeliaceae in Trinidad. Plant, Cell & Environment 9 359 376 doi:10.1111/j.1365-3040.1986.tb01750.x

Spalding MD Stumpf DK Ku MSB Burris RH Edwards GE 1979 Crassulacean acid metabolism and diurnal variations in internal CO2 and O2 concentrations in Sedum praealtum DC. Australian Journal of Plant Physiology 6 557 567 doi:10.1071/PP9790557

Stevens P (2008) Angiosperm phylogeny website. Version 9. Available at: http://www.mobot.org/MOBOT/research/APweb/ [Accessed 28 June 2010]

Szarek SR Johnson HB Ting IP 1973 Drought adaptation in Opuntia basilaris. Significance of recycling carbon through crassulacean acid metabolism. Plant Physiology 52 539 541 doi:10.1104/pp.52.6.539

Taybi T Patil S Chollet R Cushman JC 2000 A minimal Ser/Thr protein kinase circadianly regulates phosphoenolpyruvate carboxylase activity in CAM-induced leaves of Mesembryanthemum crystallinum. Plant Physiology 123 1471 1482 doi:10.1104/pp.123.4.1471

Taybi T Nimmo HG Borland AM 2004 Expression of phosphoenolpyruvate carboxylase and phosphoenolpyruvate carboxylase kinase genes. Implications for genotypic capacity and phenotypic plasticity in the expression of crassulacean acid metabolism. Plant Physiology 135 587 598 doi:10.1104/pp.103.036962

Teeri JA (1982 a) Photosynthetic variation in the Crassulaceae. In ‘Crassulacean acid metabolism’. (Eds I Ting, M Gibbs) pp. 244–259. (American Society of Plant Physiologists: Rockville, MD)

Teeri JA (1982 b) Carbon isotopes and the evolution of C4 photosynthesis and crassulacean acid metabolism. In ‘Biochemical aspects of evolutionary biology’. (Ed. MH Nitecki) pp. 93–130. (University of Chicago Press: Chicago, IL)

Teeri JA Tonsor SJ Turner M 1981 Leaf thickness and carbon isotope composition in the Crassulaceae. Oecologia 50 367 369 doi:10.1007/BF00344977

Ting I 1985 Crassulacean acid metabolism. Annual Review of Plant Physiology 36 595 622 doi:10.1146/annurev.pp.36.060185.003115

Vaasen A Begerow D Lüttge U Hampp R 2002 The genus Clusia L.: molecular evidence for independent evolution of photosynthetic flexibility. Plant Biology 4 86 93 doi:10.1055/s-2002-20440

von Willert D Armbrüster N Drees T Zaborowski M 2005 Welwitschia mirabilis: CAM or not CAM – what is the answer? Functional Plant Biology 32 389 393 doi:10.1071/FP01241

Vovides AP Etherington JR Dresser PQ Groenhof A Iglesias C Ramirez JF 2002 CAM-cycling in the cycad Dioon edule Lindl. in is natural deciduous forest habitat in central Veracruz, Mexico. Botanical Journal of the Linnean Society 138 155 162 doi:10.1046/j.1095-8339.2002.138002155.x

Westhoff P Gowik U 2004 Evolution of C4 phosphoenolpyruvate carboxylase. Gene and proteins: a case study with the genus Flaveria. Annals of Botany 93 13 23 doi:10.1093/aob/mch003

Wilkins MB 1992 Circadian rhythms: their origin and control. New Phytologist 121 347 375 doi:10.1111/j.1469-8137.1992.tb02936.x

Williams NH Chase MW Fulcher T Whitten WM 2001 a Molecular systematics of the Oncidiinae based on evidence from four DNA regions: expanded circumscriptions of Cyrtochilum, Erycina, Otoglossum and Trichocentrum and a new genus (Orchidaceae). Lindleyana 16 113 139

Williams NH Chase MW Whitten WM 2001 b Phylogenetic position of Miltoniopsis, Caucaea, a new genus, Cyrtochiloides, and relationship of Oncidium phymatochilum based on nuclear and chloroplast DNA sequence data (Orchidaceae: Oncidiinae). Lindleyana 16 95 114


Winter K 1982 Properties of phosphoenolpyruvate carboxylase in rapidly prepared, desalted leaf extracts of the crassulacean acid metabolism plant Mesembryanthemum crystallinum L. Planta 154 298 308
doi:10.1007/BF00393907

Winter K (1985) Crassulacean acid metabolism. In ‘Photosynthetic mechanisms and the environment’. (Eds J Barber, NR Baker) pp. 329–387. (Elsevier: Amsterdam)

Winter K Holtum JAM 2002 How closely do the δ13C values of crassulacean acid metabolism plants reflect the proportion of CO2 fixed during day and night? Plant Physiology 129 1843 1851 doi:10.1104/pp.002915

Winter K 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 doi:10.1104/pp.106.088922

Winter K , Smith JAC (1996) An introduction to crassulacean acid metabolism. Biochemical principles and ecological diversity. In ‘Crassulacean acid metabolism. Biochemistry, ecophysiology and evolution’. (Eds K Winter, JAC Smith) pp. 1–13. (Springer-Verlag: Berlin)

Winter K Wallace B Stocker G Roksandic Z 1983 Crassulacean acid metabolism in Australian vascular epiphytes and some related species. Oecologia 57 129 141 doi:10.1007/BF00379570

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

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
doi:10.1093/jxb/ern080

Wyka TB Bohn A Duarte HM Kaiser F Lüttge U 2004 Perturbations of malate accumulation and the endogenous rhythms of gas exchange in the crassulacean acid metabolism plant Kalanchoë daigremontiana: testing the tonoplast-as-oscillator model. Planta 219 705 713 doi:10.1007/s00425-004-1265-y

Zotz G 2004 How prevalent is crassulacean acid metabolism among vascular epiphytes? Oecologia 138 184 192 doi:10.1007/s00442-003-1418-x

Zotz G Ziegler H 1997 The occurrence of crassulacean acid metabolism among vascular epiphytes from Central Panama. New Phytologist 137 223 229 doi:10.1046/j.1469-8137.1997.00800.x


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