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JXB Advance Access originally published online on April 4, 2008
Journal of Experimental Botany 2008 59(7):1715-1734; doi:10.1093/jxb/ern028
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© The Author [2008]. Published by Oxford University Press [on behalf of the Society for Experimental Biology]. All rights reserved. For Permissions, please e-mail: journals.permissions@oxfordjournals.org

RESEARCH PAPER

Structural, biochemical, and physiological characterization of photosynthesis in two C4 subspecies of Tecticornia indica and the C3 species Tecticornia pergranulata (Chenopodiaceae)

Elena V. Voznesenskaya1, Hossein Akhani2, Nuria K. Koteyeva1, Simon D. X. Chuong3, Eric H. Roalson4, Olavi Kiirats4, Vincent R. Franceschi4 and Gerald E. Edwards4,*

1Laboratory of Anatomy and Morphology, V. L. Komarov Botanical Institute of Russian Academy of Sciences, Prof. Popov Street 2, 197376, St Petersburg, Russia
2Department of Plant Sciences, School of Biology, College of Sciences, University of Tehran, PO Box 14155-6455, Tehran, Iran
3Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada
4School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA

* To whom correspondence should be addressed. E-mail: edwardsg{at}wsu.edu

Among dicotyledon families, Chenopodiaceae has the most C4 species and the greatest diversity in structural forms of C4. In subfamily Salicornioideae, C4 photosynthesis has, so far, only been found in the genus Halosarcia which is now included in the broadly circumscribed Tecticornia. Comparative anatomical, cytochemical, and physiological studies on these taxa, which have near-aphyllous photosynthetic shoots, show that T. pergranulata is C3, and that two subspecies of T. indica (bidens and indica) are C4 (Kranz-tecticornoid type). In T. pergranulata, the stems have two layers of chlorenchyma cells surrounding the centrally located water storage tissue. The two subspecies of T. indica have Kranz anatomy in reduced leaves and in the fleshy stem cortex. They are NAD-malic enzyme-type C4 species, with mesophyll chloroplasts having reduced grana, characteristic of this subtype. The Kranz-tecticornoid-type anatomy is unique among C4 types in the family in having groups of chlorenchymatous cells separated by a network of large colourless cells (which may provide mechanical support or optimize the distribution of radiation in the tissue), and in having peripheral vascular bundles with the phloem side facing the bundle sheath cells. Also, the bundle sheath cells have chloroplasts in a centrifugal position, which is atypical for C4 dicots. Fluorescence analyses in fresh sections indicate that all non-lignified cell walls have ferulic acid, a cell wall cross-linker. Structural–functional relationships of C4 photosynthesis in T. indica are discussed. Recent molecular studies show that the C4 taxa in Tecticornia form a monophyletic group, with incorporation of the Australian endemic genera of Salicornioideae, including Halosarcia, Pachycornia, Sclerostegia, and Tegicornia, into Tecticornia.

Key words: C3 plants, C4 plants, Chenopodiaceae, chloroplast ultrastructure, Halosarcia, immunolocalization, NAD-ME type, photosynthetic enzymes, phylogeny, Tecticornia

Received 4 September 2007; Revised 16 January 2008 Accepted 21 January 2008


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