Plant Biol (Stuttg) 2007; 9(6): 745-757
DOI: 10.1055/s-2007-965579
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Structural, Biochemical, and Physiological Characterization of C4 Photosynthesis in Species Having Two Vastly Different Types of Kranz Anatomy in Genus Suaeda (Chenopodiaceae)

E. V. Voznesenskaya1 , S. D. X. Chuong2 , N. K. Koteyeva1 , V. R. Franceschi2 , H. Freitag3 , G. E. Edwards2
  • 1Laboratory of Anatomy and Morphology, V.L. Komarov Botanical Institute of Russian Academy of Sciences, Prof. Popov Street 2, 197376 St. Petersburg, Russia
  • 2School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA
  • 3Institute of Biology, Kassel University, 34109 Kassel, Germany
Further Information

Publication History

Received: October 19, 2006

Accepted: December 15, 2006

Publication Date:
21 September 2007 (online)


C4 species of family Chenopodiaceae, subfamily Suaedoideae have two types of Kranz anatomy in genus Suaeda, sections Salsina and Schoberia, both of which have an outer (palisade mesophyll) and an inner (Kranz) layer of chlorenchyma cells in usually semi-terete leaves. Features of Salsina (S. aegyptiaca, S. arcuata, S. taxifolia) and Schoberia type (S. acuminata, S. eltonica, S. cochlearifolia) were compared to C3 type S. heterophylla. In Salsina type, two layers of chlorenchyma at the leaf periphery surround water-storage tissue in which the vascular bundles are embedded. In leaves of the Schoberia type, enlarged water-storage hypodermal cells surround two layers of chlorenchyma tissue, with the latter surrounding the vascular bundles. The chloroplasts in Kranz cells are located in the centripetal position in Salsina type and in the centrifugal position in the Schoberia type. Western blots on C4 acid decarboxylases show that both Kranz forms are NAD-malic enzyme (NAD‐ME) type C4 species. Transmission electron microscopy shows that mesophyll cells have chloroplasts with reduced grana, while Kranz cells have chloroplasts with well-developed grana and large, specialized mitochondria, characteristic of NAD‐ME type C4 chenopods. In both C4 types, phosphoenolpyruvate carboxylase is localized in the palisade mesophyll, and Rubisco and mitochondrial NAD‐ME are localized in Kranz cells, where starch is mainly stored. The C3 species S. heterophylla has Brezia type isolateral leaf structure, with several layers of Rubisco-containing chlorenchyma. Photosynthetic response curves to varying CO2 and light in the Schoberia type and Salsina type species were similar, and typical of C4 plants. The results indicate that two structural forms of Kranz anatomy evolved in parallel in species of subfamily Suaedoideae having NAD‐ME type C4 photosynthesis.


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G. E. Edwards

School of Biological Sciences
Washington State University

Pullman, WA 99164-4236



Editor: R. C. Leegood