Photorespiration and the Evolution of C₄Photosynthesis

Abstract

C(4) photosynthesis is one of the most convergent evolutionary phenomena in the biological world, with at least 66 independent origins. Evidence from these lineages consistently indicates that the C(4) pathway is the end result of a series of evolutionary modifications to recover photorespired CO(2) in environments where RuBisCO oxygenation is high. Phylogenetically informed research indicates that the repositioning of mitochondria in the bundle sheath is one of the earliest steps in C(4) evolution, as it may establish a single-celled mechanism to scavenge photorespired CO(2) produced in the bundle sheath cells. Elaboration of this mechanism leads to the two-celled photorespiratory concentration mechanism known as C(2) photosynthesis (commonly observed in C(3)-C(4) intermediate species) and then to C(4) photosynthesis following the upregulation of a C(4) metabolic cycle.

Recruitment of pre-existing networks during the evolution of C 4 photosynthesis

“…An abrupt reduction in the concentration of atmospheric CO 2 during this period is thought to have favoured natural selection for the C 4 pathway [2,23]. However, over the next 20-30 Myr, the C 4 pathway continued to evolve in other lineages, suggesting that low CO 2 concentrations acted as a preconditioning event rather than the sole trigger for C 4 evolution [16]. Other factors such as high temperatures, salinity and fire frequency in tropical and subtropical regions have been proposed to contribute to the polyphyletic evolution of C 4 photosynthesis [24].…”

Introgression and repeated co-option facilitated the recurrent emergence of C4photosynthesis among close relatives

“…The C 4 advantages are achieved by increasing the concentration of CO 2 around Rubisco, the enzyme responsible for inorganic carbon fixation in the Calvin cycle of all photosynthetic organisms (von Caemmerer and Furbank 2003; Sage et al. 2012). To function, C 4 photosynthesis requires the coordinated action of numerous anatomical and biochemical components that lead to the emergence of a novel biochemical pathway, usually across two types of cells; the mesophyll and bundle sheath cells (Hatch 1987; Prendergast et al.…”

Ethylene Exerts Species-Specific and Age-Dependent Control of Photosynthesis

“…Both modes of photosynthesis deploy the same machinery present in C3 plants, but differ in the initial mode of carboxylation (West-Eberhard et al, 2011). Carbon uptake in C4 plants (about 1% of plant species) uses diurnal activity of phosphoenolpyruvate carboxylase (PEPC) in the leaf mesophyll cells followed by decarboxylation of the synthesized malic acid in the chloroplasts of bundle sheath cells where Rubisco activity is enhanced by achieving high internal CO2 concentrations (Sage et al, 2012). CAM plants (about 6% of plant species) employ a temporal separation between carboxylation events, allowing initial nocturnal CO2 sequestration by PEPC followed by Rubisco-mediated carboxylation during daytime behind closed stomata, thereby conserving considerable amounts of water (Borland et al, 2011).…”