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

Functional leaf anatomy of plants with crassulacean acid metabolism

Elizabeth A. Nelson A B , Tammy L. Sage A and Rowan F. Sage A

A Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON M5S3B2 Canada.

B Corresponding author. Email:

C This paper originates from a presentation at the IVth International Congress on Crassulacean Acid Metabolism, Tahoe City, California, USA, July–August 2004

Functional Plant Biology 32(5) 409-419
Submitted: 27 October 2004  Accepted: 31 January 2005   Published: 27 May 2005


Crassulacean acid metabolism (CAM) has evolved independently on dozens of occasions and is now found in over 7% of plant species. In this study, the leaf structure of a phylogenetically diverse assemblage of 18 CAM plants was compared with six C3 plants and four C4 plants to assess whether consistent anatomical patterns that may reflect functional constraints are present. CAM plants exhibited increased cell size and increased leaf and mesophyll thickness relative to C3 and C4 species. CAM species also exhibited reduced intercellular air space (IAS) and reduced length of mesophyll surface exposed to IAS per unit area (Lmes / area). The low volume of IAS and low exposure of mesophyll surface to IAS likely increases internal resistance to CO2 in CAM tissues. While this diffusional barrier may limit uptake of CO2 during Phases II and IV, carbon economy could be enhanced through the reduced loss of internal CO2 during all four phases of CAM.

Keywords: Crassulacean acid metabolism; C3; C4; intercellular air space; mesophyll; leaf anatomy.


Borland AM Griffiths H 1996 Variations in the phases of crassulacean acid metabolism and regulation of carboxylation patterns determined by carbon-isotope-discrimination techniques. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. Winter K Smith JAC 230 249 Springer-Verlag Berlin

Borland AM Tecsi LI Leegood RC Walker RP 1998 Inducibility of crassulacean acid metabolism (CAM) in Clusia species: physiological / biochemical characterization and intercellular localization of carboxylation and decarboxylation processes in three species which exhibit different degrees of CAM. Planta 205 342 351 DOI

Borland AM Maxwell K Griffiths H 2000 Ecophysiology of plants with crassulacean acid metabolism. In ‘Photosynthesis: physiology and metabolism’. Leegood RC Sharkey TD von Caemmer S 583 60 Kluwer Academic Publishers Dordrecht

Borland AM Dodd AN 2002 Carbohydrate partitioning in crassulacean acid metabolism plants: reconciling potential conflicts of interest. Functional Plant Biology 29 707 716 DOI

Evans JR Loreto F 2000 Acquisition and diffusion of CO2 in higher plant leaves. In ‘Photosynthesis: physiology and metabolism’. Leegood RC Sharkey TD von Caemmer S 321 351 Kluwer Academic Publishers Dordrecht

Friemart 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

Gibson AC 1982 The anatomy of succulence. In ‘Crassulacean acid metabolism’. Ting IP Gibbs M 1 30 American Society of Plant Physiologists Rockville

Griffiths H 1989 Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes. In ‘Vascular plants as epiphytes’. Luettge U 42 86 Springer-Verlag Berlin

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

Kluge M Ting IP 1978 ‘Crassulacean acid metabolism.’ Springer-Verlag Berlin

Evans JR von Caemmerer S 1996 Carbon dioxide fixation in leaves. Plant Physiology 110 339 346

Martin CE 1996 Putative causes and consequences of recycling CO2 via crassulacean acid metabolism. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. Winter K Smith JAC 192 203 Springer-Verlag Berlin

Martin CE Gravatt DA Loeschen VS 1994 Crassulacean acid metabolism in 3 species of Commelinaceae. Annals of Botany 74 457 463

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

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

Maxwell K Badger MR Osmond CB 1998 A comparison of CO2 and O2 exchange patterns and the relationship with chlorophyll fluorescence during photosynthesis in C3 and CAM plants. Australian Journal of Plant Physiology 25 45 52

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 Kalanchoe daigremontiana. Plant Physiology 121 849 856

Nobel PS 1988 ‘Environmental biology of agaves and cacti.’ Cambridge University Press Cambridge

Nobel PS 1996 High productivity of certain agronomic CAM species. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. Winter K Smith JAC 255 265 Springer-Verlag Berlin

Osmond CB Maxwell K Popp M Robinson S 1999 On being thick: fathoming apparently futile pathways of photosynthesis and carbohydrate metabolism in succulent CAM plants. In ‘Carbohydrate metabolism in plants’. Burrel M Bryant J Kruger N 183 200 BIOS Oxford

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

Sayed OH 2001 Crassulacean acid metabolism 1975–2000, a check list. Photosynthetica 39 339 352

Skillman JB Winter K 1997 High photosynthetic capacity in a shade-tolerant crassulacean acid metabolism plant: implications for sunfleck use, nonphotochemical energy dissipation, and susceptibility to photoinhibition. Plant Physiology 113 441 450

Smith JAC Heuer S 1981 Determination of the volume of intercellular spaces in leaves and some values for CAM plants. Annals of Botany 48 915 917

Smith JAC Winter K 1996 Taxonomic distribution of crassulacean acid metabolism. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. Winter K Smith JAC 427 436 Springer-Verlag Berlin

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 ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. Winter K Smith JAC 53 71 Springer-Verlag Berlin

Vitousek PM Field CB Matson PA 1990 Variation in foliar carbon 13 isotope ratios in Hawaiian Metrosideros polymorpha: a case of internal resistance? Oecologia 84 362 370

von Caemmerer S Furbank RT 1999 Modeling C4 photosynthesis. In ‘C4 plant biology’. Sage RF Monson RK 173 211 Academic Press San Diego

Williams EG Sage TL Thien LB 1993 Functional syncary by intercarpellary growth of pollen tubes in a primitive apocarpous angiosperm Illicium floridanum (Iliciaceae). American Journal of Botany 80 137 142

Winter K Smith JAC 1996 An introduction to crassulacean acid metabolism: biochemical principles and ecological diversity. In ‘Crassulacean acid metabolism: biochemistry, ecophysiology and evolution’. Winter K Smith JAC 1 10 Springer-Verlag Berlin

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