Evolution of C4 photosynthesis--looking for the master switch.

C4 PHOTOSYNTHESIS—THE BASICS C4 photosynthesis is a unique blend of biochemical, anatomical, and gene regulatory characteristics. In the vast majority of C4 plants, i.e. with the exception of single-cell C4 photosynthesis in the Chenopodiaceae, this photosynthetic pathway is the result of the integrated metabolic activities of two distinct, specialized leaf cell types, mesophyll and bundle sheath cells. CO2 is initially fixed in the mesophyll cells by phosphoenolpyruvate carboxylase. The resulting C4 acids diffuse into the bundle sheath cells, where CO2 is liberated by one or several of the decarboxylases NADP-malic enzyme, NAD-malic enzyme, or phosphoenolpyruvate carboxykinase, and channeled into the Calvin-Benson cycle. C4 photosynthesis is therefore essentially a pump that concentrates CO2 at the site of Rubisco in the bundle sheath cells (Kanai and Edwards, 1999). The division of labor between mesophyll and bundle sheath cells involves the compartmentation of enzymes and metabolite transporters of the photosynthetic carbon assimilation pathway, but also of the photosynthetic electron transport complexes and other metabolic pathways. It relies on the differential expression of the corresponding genes (Hibberd and Covshoff, 2010). As a consequence of the CO2-concentrating mechanism Rubisco becomes saturated with CO2, photorespiration is largely reduced, and Rubisco can achieve its maximal catalytic activity. In addition, C4 plants use water and nitrogen more efficiently than C3 species (Ehleringer and Monson, 1993). Not surprisingly, C4 plants contribute about 25% of total terrestrial photosynthesis, although they account for only 3% of the vascular plants. Entire ecosystems like the warmclimate grasslands or savannas are dominated and shaped by C4 plants of the grass family. The emergence of C4 grasses in the late Miocene and Pleistocene, i.e. 3 to 8 million years ago, and the concomitant displacement of C3 grasses demonstrates the adaptational advantage of the C4 photosynthetic pathway (Edwards et al., 2010). THE C4 SYNDROME—KRANZ ANATOMY AND VEIN SPACING