Single-cell C(4) photosynthesis versus the dual-cell (Kranz) paradigm

Abstract

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 CO(2) and rise in O(2) as early as 300 mya provided selective pressure for the evolution of mechanisms to concentrate CO(2) 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 C(4) 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. C(4) photosynthesis has evolved independently many times with great diversity in forms of Kranz anatomy, structure of dimorphic chloroplasts, and biochemistry of the C(4) cycle. The most dramatic variants of C(4) terrestrial plants were discovered recently in two species, Bienertia cycloptera and Borszczowia aralocaspica (family Chenopodiaceae); each has novel compartmentation to accomplish C(4) photosynthesis within a single chlorenchyma cell. This review discusses the amazing diversity in C(4) systems, how the essential features of C(4) are accomplished in single-cell versus Kranz-type C(4) plants, and speculates on why single-cell C(4) plants evolved.