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(American Journal of Botany. 2007;94:362-381.)
© 2007 Botanical Society of America, Inc.


Anatomy and Morphology

Diversity of Kranz anatomy and biochemistry in C4 eudicots1

Riyadh Muhaidat, Rowan F. Sage and Nancy G. Dengler4

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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