Journal
AMERICAN JOURNAL OF BOTANY
Volume 94, Issue 3, Pages 362-381Publisher
WILEY
DOI: 10.3732/ajb.94.3.362
Keywords
C-4 photosynthesis; Kranz anatomy; mesophyll to bundle sheath ratio; NAD-malic enzyme; NADP-malic enzyme; PEP-carboxykinase enzyme; vein density
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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.
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