Table 1.
Hypothetical model for the evolution of C4 photosynthesis, showing three phases that are each observed in extant C3–C4 intermediates. The scheme is a simplified version of that presented by Sage [19], incorporating new evidence [70].
| phase 1. Evolution of ‘proto-Kranz anatomy’ |
| A reduction in the distance between leaf veins and an enlargement in bundle sheath cells (BSC) (figure 1b) may evolve under dry environmental conditions to enhance leaf water status [19,71,72]. Since photosynthetic activity is limited in the BSC of most C3 leaves, increases in the number of chloroplasts may initially serve to maintain leaf light absorpance as the BSC occupy a larger fraction of the leaf. An increase in the numbers and asymmetric distribution of mitochondria in the BSC may establish a photorespiratory CO2 pump that shuttles glycine and refixes CO2within single BSC (see phase 2). This combination of traits has been termed ‘proto-Kranz anatomy’, and occurs in C3 species that are closely related to C3–C4 intermediates [70]. |
| phase 2. Evolution of a photorespiratory CO2pump |
| Photorespiration liberates CO2 via a decarboxylation reaction catalysed by the enzyme glycine decarboxylase (GDC). The increasing localization of this enzyme in BSC mitochondria requires glycine to be shuttled between the mesophyll cells (MC) and the BSC, liberating CO2 in the BSC and allowing its refixation by Rubisco in this compartment (figure 1b). Efficiency of the glycine shuttle increases greatly if BSC walls are resistant to CO2 diffusion, thereby concentrating CO2 in the BSC. This type of photorespiratory CO2 pump is typical of C3–C4 intermediates [19]. |
| phase 3. Evolution of the C4cycle |
| Increases in the PEPC activity of MC may occur initially to scavenge CO2 that leaks from the BSC, but eventually allows the fixation of CO2 from intercellular airspaces (figure 1a). Once this occurs, enhancement of decarboxylase enzyme activities in the BSC is needed to recover the acceptor molecule for carbon-fixation (figure 1a). As carbon-fixation by PEPC increases above that of Rubisco, the C3 cycle is increasingly confined to the BSC, and activities of the C4 and C3 cycles are coordinated. Finally, enzymes recruited into the C4 cycle adapt to their new catalytic environment via changes in turnover rate, substrate affinity and regulation. Changes in stomatal conductance occur during this phase [19]. |