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Diversity of Kranz anatomy and biochemistry in C₄ eudicots¹

Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, M5S 1A1, Canada; Department of Biological Sciences, Yarmouk University, Irbid, Hashemite Kingdom of Jordan

ABSTRACT

C₄ photosynthesis and Kranz anatomy occur in 16 eudicot families, a striking example of convergent evolution. Biochemical subtyping for 13 previously undiagnosed C₄ eudicot species indicated that 10 were NADP-malic enzyme (ME) and three were NAD-ME. A total of 33 C₄ species, encompassing four Kranz anatomical types (atriplicoid, kochioid, salsoloid, and suaedioid), and 21 closely related C₃ 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, C₄ species were distinguished from C₃ 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 C₄ 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 C₄ metabolism in eudicots.

Key Words: C₄ photosynthesis • Kranz anatomy • mesophyll to bundle sheath ratio • NAD-malic enzyme • NADP-malic enzyme • PEP-carboxykinase enzyme • vein density

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