Single-Cell C 4 Photosynthesis Versus the Dual-Cell (Kranz) Paradigm

The efficiency of photosynthetic carbon assimilation in higher plantsfaces significant limitations due to the oxygenase activity of the enzyme Rubisco,particularly under warmer temperatures or water stress. A drop in atmospheric CO2and rise in O2 as early as 300 mya provided selective pressure for the evolution ofmechanisms to concentrate CO2 around Rubisco in order to minimize oxygenase activityand the resultant loss of carbon through photorespiration. It is well establishedthat a carbon-concentrating mechanism occurs in some terrestrial plants through theprocess of C4 photosynthesis. These plants are characterized as having Kranz-typeleaf anatomy, with two structurally and biochemically specialized photosynthetic celltypes, mesophyll and bundle sheath, that function coordinately in carbon assimilation.C4 photosynthesis has evolved independently many times with great diversity in formsof Kranz anatomy, structure of dimorphic chloroplasts, and biochemistry of the C4cycle. The most dramatic variants of C4 terrestrial plants were discovered recently intwo species, Bienertia cycloptera and Borszczowia aralocaspica (family Chenopodiaceae);each has novel compartmentation to accomplish C4 photosynthesis within asingle 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 C4plants, and speculates on why single-cell C4 plants evolved.