From proto-Kranz to C4 Kranz: building the bridge to C4 photosynthesis

In this review, we examine how the specialized Kranz anatomy of C-4 photosynthesis evolved from C-3 ancestors. Kranz anatomy refers to the wreath-like structural traits that compartmentalize the biochemistry of C-4 photosynthesis and enables the concentration of CO2 around Rubisco. A simplified version of Kranz anatomy is also present in the species that utilize C-2 photosynthesis, where a photorespiratory glycine shuttle concentrates CO2 into an inner bundle-sheath-like compartment surrounding the vascular tissue. C-2 Kranz is considered to be an intermediate stage in the evolutionary development of C-4 Kranz, based on the intermediate branching position of C-2 species in 14 evolutionary lineages of C-4 photosynthesis. In the best-supported model of C-4 evolution, Kranz anatomy in C-2 species evolved from C-3 ancestors with enlarged bundle sheath cells and high vein density. Four independent lineages have been identified where C-3 sister species of C-2 plants exhibit an increase in organelle numbers in the bundle sheath and enlarged bundle sheath cells. Notably, in all of these species, there is a pronounced shift of mitochondria to the inner bundle sheath wall, forming an incipient version of the C-2 type of Kranz anatomy. This incipient version of C-2 Kranz anatomy is termed proto-Kranz, and is proposed to scavenge photorespiratory CO2. By doing so, it may provide fitness benefits in hot environments, and thus represent a critical first stage of the evolution of both the C-2 and C-4 forms of Kranz anatomy.