Deconstructing Kranz anatomy to understand C4 evolution.

Abstract

C4 photosynthesis is a complex physiological adaptation that confers greater productivity than the ancestral C3 photosynthetic type in environments where photorespiration is high. It evolved in multiple lineages through the coordination of anatomical and biochemical components, which concentrate CO2 at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). In most C4 plants, the CO2-concentrating mechanism is achieved via the confinement of Rubisco to bundle-sheath cells, into which CO2 is biochemically pumped from surrounding mesophyll cells. The C4 biochemical pathway relies on a specific suite of leaf functional properties, often referred to as Kranz anatomy. These include the existence of discrete compartments differentially connected to the atmosphere, a close contact between these compartments, and a relatively large compartment to host the Calvin cycle. In this review, we use a quantitative dataset for grasses (Poaceae) and examples from other groups to isolate the changes in anatomical characteristics that generate these functional properties, including changes in the size, number, and distribution of different cell types. These underlying anatomical characteristics vary among C4 origins, as similar functions emerged via different modifications of anatomical characteristics. In addition, the quantitative characteristics of leaves all vary continuously across C3 and C4 taxa, resulting in C4-like values in some C3 taxa. These observations suggest that the evolution of C4-suitable anatomy might require relatively few changes in plant lineages with anatomical predispositions. Furthermore, the distribution of anatomical traits across C3 and C4 taxa has important implications for the functional diversity observed among C4 lineages and for the approaches used to identify genetic determinants of C4 anatomy.