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Lüttge-2010-Ability of Crassulacean Acid Metabolism Plants to Overcome AoB PLANTS http://aobplants.oxfordjournals.org/ Open access – Review Ability of crassulacean acid metabolism plants to overcome interacting stresses in tropical environments Ulrich Lu¨ttge* Institute of Botany, Technical University of Darmstadt, Schnittspahnstrasse 3-5, D-64287 Darmstadt, Germany Received: 26 January 2010; Returned for revision: 16 March 2010; Accepted: 10 May 2010; Published: 13 May 2010 Citation details:Lu¨ttge U. 2010. Ability of crassulacean acid metabolism plants to overcome interacting stresses in tropical environments. AoB PLANTS 2010: plq005, doi:10.1093/aobpla/plq005 Abstract Background and Single stressors such as scarcity of waterand extreme temperatures dominate the struggle for life aims in severely dry desert ecosystems orcold polar regions and at high elevations. In contrast, stress in the tropics typically arises from a dynamic network of interacting stressors, such as availability of water, CO2, light and nutrients, temperature and salinity. This requires more plastic spatio- temporal responsiveness and versatility in the acquisition and defence of ecological niches. Crassulacean acid The mode of photosynthesis of crassulacean acid metabolism (CAM) is described and its flex- metabolism ible expression endows plants with powerful strategies for both acclimation and adaptation. Thus, CAM plants are able to inhabit many diverse habitats in the tropics and are not, as com- monly thought, successful predominantly in dry, high-insolation habitats. Tropical CAM Typical tropical CAM habitats or ecosystems include exposed lava fields, rock outcrops of insel- habitats bergs, salinas, savannas, restingas, high-altitude pa´ramos, dry forests and moist forests. Morphotypical and Morphotypical and physiotypical plasticity of CAM phenotypes allow a wide ecophysiological physiotypical amplitude of niche occupation in the tropics. Physiological and biochemical plasticity plasticity of CAM appear more responsive by having more readily reversible variations in performance than do morphological adaptations. This makes CAM plants particularly fit for the multi-factor stressor networks of tropical forests. Thus, while the physiognomy of semi-deserts outside the tropics is often determined by tall succulent CAM plants, tropical forests house many more CAM plants in terms of quantity (biomass) and quality (species diversity). Introduction assessing the struggle for life (Darwin, 1909) by CAM Crassulacean acid metabolism phenotypes and the plants in tropical ecosystems, we must consider the struggle against environmental impacts impact of environmental cues as stressors on CAM-plant The many intrinsic features of crassulacean acid metab- phenotypes. The complete set of phenological traits gen- olism (CAM) plants are well-covered by numerous erated by a genotype in the morphological domain is reviews and books (e.g. Black, 1973; Kluge and Ting, termed the morphotype and in the physiological 1978; Osmond, 1978; Cockburn, 1985; Martin, 1994; domain, the physiotype (Kinzel, 1972, 1982; Lu¨ttge, 2005). Winter and Smith, 1996; Lu¨ttge, 1998, 2002, 2003, 2004, Darwinian evolutionary selection is the outcome of the 2006, 2007, 2008a; Cushman and Bohnert, 1999). When struggle of individual phenotypic fitness pitted against * Corresponding author’s e-mail address: [email protected] AoB PLANTS Vol. 2010, plq005, doi:10.1093/aobpla/plq005, available online at www.aobplants.oxfordjournals.org & The Authors 2010. Published by Oxford University Press. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.5/uk/) which permits unrestricted non- commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS Vol. 2010, plq005, doi:10.1093/aobpla/plq005 & The Authors 2010 1 Lu¨ttge — Ability of CAM plants to overcome stresses in tropical environments environmental challenges. Naturally, the complement of organic acids, mainly malate/malic acid, which are all phenotypic properties together determines the stored during the dark period in vacuoles (Phase I). There fitness of the whole plant. In a necessarily simplifying is a transitory early morning Phase II when both vein, the present review examines physiotypes and mor- enzymes are active but with PEPC being down-regulated photypes separately before considering the performance and RUBISCO up-regulated. Then, the inorganic carbon of CAM plants in their various tropical environments. concentrating mechanism begins in Phase III when Crassulacean acid metabolism physiotypes are well stomata close and organic acid is remobilized from the studied in terms of physiology, especially their gas vacuoles and decarboxylated in the cytosol or mitochon- exchange and biochemistry and, increasingly, in terms dria. This regenerates CO2 that can temporarily result in of molecular biology. The morphotypes are currently internal CO2 concentrations of up to 2.5 % (v/v) in gas-filled receiving less attention. General principles and theories spaces behind closed stomatal pores (Lu¨ttge, 2002). This of the ecology and ecophysiology of plants have, in the physiotypical trait of CAM is often thought to bestow main, been worked out without much consideration for fitness in dealing with high irradiance stress, as the high CAM taxa. One likely reason for this is that CAM plants internal CO2 concentrations allow high photosynthetic were long considered to be a mere curiosity until activity and, with it, effective dissipation of photosynthetic Osmond (1978) placed them into context. solar excitation energy by photochemical work. The study of CAM plants supports the view that mor- photypic features generally are less plastic than physio- Water saving typic ones (Metlen et al., 2009) with physiotypic plasticity Nocturnal stomatal opening for CO uptake and daytime of CAM plants being the more important adaptive trait. 2 closure of stomata strongly reduce loss of water vapour The expression of CAM phases can be modulated in a by transpiration during the acquisition of inorganic versatile way in response to environmental stress. Most carbon. Moreover, the osmotic effect of nocturnal C /CAM intermediate plants can switch readily between 3 accumulations of vacuolar organic acids allows noctur- the modes of photosynthesis and use the CAM option nal acquisition of water from the transpiration stream in fine-tuned acclimations to environmental dynamics. and also from dew, and transitory storage of water in Thus, CAM is an excellent example of ‘plant behavioural vacuoles. This physiotypical trait of CAM bestows ecology’, where ‘physiological and biochemical plasticity’ fitness in dealing with stress from the limited water appear to be ‘more responsive and energy efficient than supply. Thus, in a highly simplified consideration, morphological plasticity’—as stated by Metlen et al. the central physiotypic properties of CAM plants, i.e. (2009) after considering foraging of plants for nutrients CO concentrating and high water use efficiency, make in the rooting medium. Rapid reversibility is an outstand- 2 them particularly fit to deal with high insolation and ing feature of physiotypic acclimation. Morphology is dryness. However, when we consider real environments, more involved in less plastic and less reversible ontogen- especially various tropical environments, relationships etic adaptation. We shall come to understand CAM as an turn out to be more complicated and subtle. effective strategy for both acclimation and adaptation, for developing diversity and for survival under stress. It is not a strategy for high productivity (Black, 1973). The role of CAM physiotypes in the struggle of CAM plants with interacting CAM physiotypes stressors in the tropics The two major features of CAM physiotypes are: (i) CAM Environmental cues of wet or dry and warm or cold as an inorganic carbon concentrating mechanism and tropics (ii) CAM as a water-saving mechanism. According to Lauer (1975), it is possible on a global scale to distinguish between wet or dry and warm or cold tropics; Inorganic carbon concentrating the wet tropics mostly comprising moist tropical forest Crassulacean acid metabolism plants fix CO2 nocturnally in ecosystems, the dry tropics comprising mainly savanna the dark period using the enzyme phosphoenolpyruvate and desert ecosystems. The warm tropics are found in carboxylase (PEPC), which is notable for its high affinity the lower altitudes and the cold tropics at high elevations 2 towards its inorganic carbon substrate HCO3 .Thisis (pa´ramos and punas or tropical ‘alpine’ regions). The 60-fold higher than the affinity of ribulosebisphosphate stressors and their combinations governing survival in carboxylase/oxygenase (RUBISCO) for its substrate CO2 these contrasting ecosystems differ accordingly. during fixation in the light period. This high affinity facili- Dominance of dryness and high insolation is restricted tates inorganic carbon acquisition by PEPC to produce to extreme tropical habitats, such as deserts, lava fields 2 AoB PLANTS Vol. 2010, plq005, doi:10.1093/aobpla/plq005 & The Authors 2010 Lu¨ttge — Ability of CAM plants to overcome stresses in tropical environments and inselbergs. They interact in a straightforward way CAM evolved polyphyletically, i.e. many times at all taxo- where, in addition, high insolation leads to the develop- nomic ranks: within the division of the Pteridophyta, in ment of stressor heat. Under the dominance of high irra- all
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