Intracellular transport and pathways of carbon flow in plants with crassulacean acid metabolism

Abstract

The massive daily reciprocal transfer of carbon between acids and carbohydrates that is unique to crassulacean acid metabolism (CAM) involves extensive and regulated transport of metabolites between chloroplasts, vacuoles, the cytosol and mitochondria. In this review of the CAM pathways of carbon flow and intracellular transport, we highlight what is known and what has been postulated. For three of the four CAM pathway variants currently known (malic enzyme-or PEP carboxykinase-type decarboxylase, and starch-or soluble sugar-type carbohydrate storage), the mechanisms of intracellular transport are still hypothetical and have yet to be demonstrated experimentally. Even in malic enzyme starch-storing species such as Kalanchoë daigremontiana Hamet et Perr. and Mesembryanthemum crystallinum L., the best-described variants of plants with the second-most common mode of photosynthetic carbon metabolism known, no tonoplast or mitochondrial transporter has been functionally described at a molecular level. Keywords: CAM, photosynthetic carbon metabolism, plant metabolite transport. © CSIRO 2005 10.1071/FP04189 1445-4408/05/050429 Functional Plant Biology J. A. M. Holtum et al. Dodd et al. 2002) and a comprehensive understanding of the basic molecular and circadian processes underpinning the CAM cycle (for reviews see

Evolution along the crassulacean acid metabolism continuum

“…Depending on the CAM species, a variety of storage carbohydrates (e.g. starch, glucans, soluble hexoses) might be catabolised to produce phosphoenolpyruvate (PEP), the substrate for carboxylation Holtum 1996, 1998;Holtum et al 2005). Phase I reflects the fundamental adaptation of CAM that results in reduced transpiration and improved water economy due to lower night-time evapotranspirational demands and associated water losses (Griffiths 1988).…”

“…This decarboxylation can lead to generation of internal leaf CO 2 partial pressures greater than 100 times atmospheric levels (Cockburn et al 1979;Spalding et al 1979), reduction in stomatal opening and transpiration and sometimes even release of CO 2 from the leaf despite low stomatal conductance (Frimert et al 1986). Decarboxylation is catalysed by either cytosolic PEP carboxykinase (PEPCK) or cytosolic NADP + -and/or mitochondrial NAD + -malic enzymes (ME) (Smith and Bryce 1992;Christopher and Holtum 1996;Holtum et al 2005). This CO 2 -concentrating mechanism or 'CO 2 pump' effectively suppresses photorespiration during this phase.…”

“…Some CAM species utilise PEP carboxykinase (PEPCK), which decarboxylates OAA resulting in the formation of PEP (not shown). Hexose-storing CAM species, such as Ananas comosus store hexose in the vacuole that is transported to the cytosol (see Holtum et al 2005). G6P, glucose-6-phosphate; TP, triose phosphate; PGA, 3-phosphoglycerate; PEP, phosphoenolpyruvate; OAA, oxaolacetate; MAL, malate; FUM, fumarate; PYR, pyruvate; TCA cycle, tricarboxylic acid cycle; PCR cycle, photosynthetic carbon reduction cycle.…”

“…unknown protein proposed to mediate malic acid efflux, possibly a tonoplast dicarboxylate transporter. This model is derived, in part, from information summarised by Holtum et al (2005).…”

“…Third, associated transport activities across the tonoplast (e.g. vacuolar H + -ATPase), mitochondrial (Holtum et al 2005;Cushman et al 2008b), and chloroplast envelope membranes (Häusler et al 2000;Kore-eda et al 2005) are needed to support these fluctuations (Fig. 1).…”