Diversity of Kranz anatomy and biochemistry in C₄ eudicots

Abstract

C(4) photosynthesis and Kranz anatomy occur in 16 eudicot families, a striking example of convergent evolution. Biochemical subtyping for 13 previously undiagnosed C(4) eudicot species indicated that 10 were NADP-malic enzyme (ME) and three were NAD-ME. A total of 33 C(4) species, encompassing four Kranz anatomical types (atriplicoid, kochioid, salsoloid, and suaedioid), and 21 closely related C(3) species were included in a quantitative anatomical study in which we found that, unlike similar studies in grasses and sedges, anatomical type had no predictive value for the biochemical subtype. In a multivariate canonical discriminant analysis, C(4) species were distinguished from C(3) species by the mesophyll to bundle sheath ratio and exposure of the bundle sheath surface to intercellular space. Discrimination between NADP-ME and NAD-ME was not significant, although in a Mantel test grouping by biochemical subtype was significant, while grouping by family was not. This comprehensive survey of C(4) anatomy and biochemistry unequivocally demonstrated that atriplicoid anatomy and NADP-ME biochemistry predominate in many evolutionary lineages. In addition to a main decarboxylating enzyme, high activity of a second decarboxylating enzyme was often observed. Notably, PEP-carboxykinase activity was significant in a number of species, demonstrating that this enzyme could also serve as a secondary pathway for C(4) metabolism in eudicots.

The biology of Canadian weeds. 138. Kochia scoparia (L.) Schrad.

“…(c) Physiological Data * Kochia is a C 4 plant that utilizes NADP-ME in the C 4 photosynthetic pathway (Welkie and Caldwell 1970;Kadereit et al 2003), and displays a kochioid type of C 4 Krantz anatomy (Pyankov et al 1999;Muhaidat et al 2007). A specific feature of this type of C 4 pathway is the requirement for sodium (Na) as a micronutrient (Brownell and Crossland 1972).…”

Phylogenetic analyses reveal the shady history of C 4 grasses

“…The pathway also promotes more efficient photosynthetic water use, because the CO 2 concentration mechanism allows C 4 plants to maintain a lower stomatal conductance for a given photosynthetic rate. C 4 photosynthesis is estimated to have evolved at least 50 times in terrestrial plants (2,3) and is most prominent in grasses, where roughly half the species (∼5,000) are C 4 (4), including economically important species such as maize, sugarcane, sorghum, and switchgrass. C 4 grasses currently dominate wide regions of the Earth, and it is estimated that they account for up to 25% of global annual terrestrial primary production (5).…”

Anatomical enablers and the evolution of C 4 photosynthesis in grasses

“…Such enablers may include ecological factors, as well as genomic and anatomical properties (10). For optimal functioning of the C 4 pathway, foliar anatomy must be altered to increase the relative proportion of BS cells and reduce the average path length between M and BS cells (12)(13)(14)(15). These modifications guarantee an efficient centripetal increase of CO 2 concentration, but they also imply that C 4 evolution involved many mutations, unless the C 3 ancestors already possessed some C 4 -like anatomical characters.…”