Crassulacean Acid Metabolism. A Plastic Photosynthetic Adaptation to Arid Environments

Abstract

Crassulacean acid metabolism (CAM) is an important elaboration of photosynthetic carbon fixation that allows chloroplast-containing cells to fix CO2initially at night using phosphoenolpyruvate carboxylase (PEPC) in the cytosol. This leads to the formation of C4 organic acids (usually malate), which are stored in the vacuole. Subsequent daytime decarboxylation of these organic acids behind closed stomata creates an internal CO2 source that is reassimilated by Rubisco in the chloroplast. The refixation of this internal CO2 generates carbohydrates via the conventional photosynthetic carbon reduction cycle. Thus, CAM involves a temporal separation of carbon fixation modes in contrast to the spatial separation found in C4 plants. The first recognition of the nocturnal acidification process can be traced to the Romans, who noted that certain succulent plants taste more bitter in the morning than in the evening (Rowley, 1978). However, formal descriptions of the ability of succulent plants to conduct nocturnal CO2 fixation or to acidify photosynthetic tissues at night and deacidify them during the day did not appear until the early 19th century (de Saussure, 1804; Heyne, 1815). The term CAM was coined to give credit to Heyne's observations that were made usingBryophyllum calycinum, a succulent member of the Crassulaceae. Since these early descriptions, a detailed account of the sequence of biochemical reactions of the CAM cycle (Ranson and Thomas, 1960), the complexity of the biochemical variations in the pathway among different CAM species, and its regulation by the environment have been achieved (Osmond, 1978; Ting, 1985). Initial nocturnal CO2fixation by PEPC occurs when stomata are open and transpirational water losses are low. CO2 release during the day promotes stomatal closure and concentrates CO2around Rubisco, suppressing its oxygenase activity, thereby minimizing photorespiration. The net effect of this CO2-concentrating strategy is that CAM plants exhibit water use efficiency (WUE) rates severalfold higher than C3 and C4 plants under comparable conditions (Drennan and Nobel, 2000). Thus, CAM is typically, although not exclusively, associated with plants that inhabit extremely arid environments (e.g. deserts), semi-arid regions with seasonal water availability (e.g. Mediterranean climates), or habitats with intermittent water supply (e.g. tropical epiphytic habitats). Most notable among these are commercially or horticulturally important plants such as pineapple (Ananas comosus), agave (Agavesubsp.), cacti (Cactaceae), and orchids (Orchidaceae). CAM is also correlated with various anatomical or morphological features that minimize water loss, including thick cuticles, low surface-to-volume ratios, large cells and vacuoles with enhanced water storage capacity (i.e. succulence), and reduced stomatal size and/or frequency. The selective advantage of high WUE likely accounts for the extensive diversification and speciation among CAM plants principally in water-limited environments. Intensive ecophysiological studies over the last 20 years have documented that CAM is present in approximately 7% of vascular plant species, a much larger percentage than the percentage of C4 species (Winter and Smith, 1996a). The widespread distribution of CAM among 33 taxonomically diverse families (Smith and Winter, 1996) suggests that CAM most likely evolved independently on numerous occasions in different families and even within individual families (Griffiths, 1989; Ehleringer and Monson, 1993; Pilon-Smits et al., 1996). More recent phylogenetic reconstructions using PEPC sequence information have provided more convincing support for the polyphyletic origins of CAM (Gehrig et al., 1998b, 2001). It is curious that CAM is also found in aquatic vascular plants where it presumably enhances inorganic carbon acquisition in certain aquatic environments where CO2availability can become rate limiting for photosynthesis (Keeley, 1996,1998). Thus, the daytime limitation of CO2availability, brought about by water-conserving stomatal closure in arid terrestrial habitats or by competition from other species and the high diffusional resistances limiting access to CO2 in aquatic habitats, appears to be the common factor responsible for the evolution of CAM. One of most striking themes to emerge in recent years is the extent to which the phylogenetic and ecological diversity of CAM plants is also reflected in a remarkable plasticity of the basic metabolic scheme described above. Genotypic, ontogenetic, and environmental factors such as light intensity, relative humidity, and water availability combine to govern the extent to which the biochemical and physiological attributes of CAM are expressed (Cushman and Borland, 2001). The photosynthetic plasticity of CAM occurs within a continuum of diel gas exchange patterns that fall into four phases as defined byOsmond (1978). The nocturnal uptake of atmospheric and respiratory CO2 via PEPC to form