SINGLE-CELL C4 PHOTOSYNTHESIS VERSUS THE DUAL-CELL (KRANZ) PARADIGM

The efficiency of photosynthetic carbon assimilation in higher plants faces significant limitations due to the oxygenase activity of the enzyme Rubisco, particularly under warmer temperatures or water stress. A drop in atmospheric CO2 and rise in O2 as early as 300 mya provided selective pressure for the evolution of mechanisms to concentrate CO2 around Rubisco in order to minimize oxygenase activity and the resultant loss of carbon through photorespiration. It is well established that a carbon-concentrating mechanism occurs in some terrestrial plants through the process of C4 photosynthesis. These plants are characterized as having Kranz-type leaf anatomy, with two structurally and biochemically specialized photosynthetic cell types, mesophyll and bundle sheath, that function coordinately in carbon assimilation. C4 photosynthesis has evolved independently many times with great diversity in forms of Kranz anatomy, structure of dimorphic chloroplasts, and biochemistry of the C4 cycle. The most dramatic variants of C4 terrestrial plants were discovered recently in two species, Bienertia cycloptera and Borszczowia aralocaspica (family Chenopodiaceae); each has novel compartmentation to accomplish C4 photosynthesis within a single chlorenchyma cell. This review discusses the amazing diversity in C4 systems, how the essential features of C4 are accomplished in single-cell versus Kranz-type C4 plants, and speculates on why single-cell C4 plants evolved.