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2.2.6 - Single-cell C4 photosynthesis

The fundamental paradigm underpinning the efficiency of C4 photosynthesis in terrestrial plants is the ‘division of labour’ between the initial fixation of CO2 into C4 acids, and their subsequent utilisation to generate high concentrations of CO2 for ultimate fixation by Rubisco. The basic model for C4 plants with classical kranz anatomy consists of two photosynthetic cycles (C3 and C4) operating across two photosynthetic cell types (mesophyll and bundle sheath), with strict cell- and organelle-specific localisation of key enzymes and with sufficient resistance to CO2 back-diffusion. Indeed, the discovery of the kranz anatomy by Haberlandt preceded that of C4 biochemistry by a century. The prevailing consensus has been that efficient C4 photosynthesis necessitates the collaboration of two cell types.

Recently, this notion has been challenged by the discovery of non-kranz or single-cell C4 photosynthesis in shrubs (Borszczowia aralocaspica and Bienertia cycloptera; Chenopodiaceae family) found in the salt deserts of Central Asia (Voznesenskaya et al. 2002, 2003). These plants show CO2 and O2 responses typical of C4 photosynthesis but lack the kranz anatomy. They perform C4 photosynthesis through the spatial localisation of dimorphic chloroplasts (as well as other organelles and photosynthetic enzymes) in distinct positions within a single chlorenchyma cell. Yet, the details of the partitioning differ between the two species (Edwards et al. 2004).

In Bienertia, the central cytoplasmic compartment of the chlorenchyma cell plays the role of bundle sheath cells in kranz-type C4 (NAD-ME) plants; it is filled with mitochondria surrounded by chloroplasts. The peripheral cytoplasm lacks mitochondria and plays the role of the mesophyll cell in kranz-type C4 plants. Accordingly, chloroplastic Rubisco and mitochondrial NAD-ME and glycine decarboxylase are restricted to the central compartment; chloroplastic pyruvate, Pi dikinase is restricted to the peripheral compartment, which is highly enriched with cytosolic PEP carboxylase. In Borszczowia, the compartmentation occurs at the distal (mesophyll equivalent) and proximal (bundle sheath equivalent) ends of the elongated, cylindrical chlorenchyma cell. The inter-connecting cytoplasm between the two intra-cellular compartments provides a liquid diffusion path, thus replacing the role of the bundle sheath cell wall in kranz-type C4 plants (Edwards et al. 2004).

A low conductance for CO2 diffusion out of the bundle sheath cells (or its equivalent cellular compartment) is critical for the efficient operation of C4 photosynthesis. The total diffusive resistance to CO2 has multiple components with different levels of contribution. These components include bundle sheath walls, membranes, bundle sheath chloroplast position, the site of C4 acid decarboxylation, and the liquid-phase diffusion path. For kranz-type C4 plants, calculated total bundle sheath resistance on a leaf area basis can range from 50 to 150 m2 s-1 mol-1 (von Caemmerer and Furbank 2003). Evidently, single-cell C4 plants have sufficient resistance to CO2 back-diffusion which is essentially made of the cytoplasmic liquid phase and the special localisation of the (Rubisco-containing) chloroplasts surrounding the mitochondria (site of C4 acid decarboxylation).

Thus, single-cell C4 plants have efficient photosynthesis which is not inhibited by O2, and their carbon isotope values are similar to kranz-type C4 plants. Although, single-cell C4 photosynthesis breaks away from the classical kranz anatomy, it remains within the general ‘division of labour’ paradigm.