Are crassulacean acid metabolism and C4 photosynthesis incompatible?

Abstract

This paper originates from a presentation at the IIIrd International Congress on Crassulacean Acid Metabolism, Cape Tribulation, Queensland, Australia, August 2001.

Despite sharing a similar metabolism, crassulacean acid metabolism (CAM) and C₄ photosynthesis are not known to occur in identical species, with the exception of Portulaca spp. In Portulaca, C₄ and weak CAM photosynthesis occur in distinct regions of the leaf, rather than in the same cells. This is in marked contrast to the situation in most CAM species where C₃ and CAM photosynthesis are active in the same cell over the course of a day and growing season. The lack of CAM and C₄ photosynthesis in identical cells of a plant indicates these photosynthetic pathways are incompatible. Incompatibilities between CAM and C₄ photosynthesis could have a number of biochemical, anatomical and evolutionary explanations. Biochemical incompatibilities could result from the requirement for spatial separation of C₃ and C₄ phases in C₄ plants versus temporal separation in CAM plants. In C₄ plants, regulatory systems coordinate mesophyll and bundle sheath metabolism, with light intensity being the major environmental signal. In CAM plants, a circadian oscillator coordinates day and night phases of CAM. The requirement for rapid intercellular transport in C₄ plants may be incompatible with the intracellular transport and storage needs of CAM. For example, the large vacuole required for malate storage in CAM could impede metabolite diffusion between mesophyll and bundle sheath cells in C₄ plants. Anatomical barriers could also exist because both CAM and the C₄ pathway require distinct leaf anatomies for efficient function. Efficient function of the C₄ pathway generally requires an outer layer of cells specialized for phosphoenolpyruvate (PEP) carboxylation and regeneration and an inner layer for CO₂ accumulation and refixation, while CAM species require enlarged vacuoles and tight cell packing. In evolutionary terms, barriers preventing CAM and C₄ photosynthesis in the same species may be the initial steps in the respective evolutionary pathways from C₃ ancestors. The first steps in C₄ photosynthesis are related to scavenging photorespiratory CO₂ via localization of glycine decarboxylase in the bundle sheath cells. The initial steps in CAM evolution are associated with the scavenging of respiratory CO₂ at night by PEP carboxylation. In each, simplified versions of the specialized anatomy may need to be present for the evolutionary sequence to begin. For C₄ evolution, enhanced bundle sheath size may be required in C₃ ancestors; for CAM evolution, succulence may be required. Thus, before CAM or C₄ photosynthesis began to evolve, the outcome of the evolutionary experiment may have been predetermined.