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Publication Type J
Authors Koteyeva, N. K., E. V. Voznesenskaya, J. O. Berry, S. D. X. Chuong, V. R. Franceschi and G. E. Edwards
Title Development of structural and biochemical characteristics of C-4 photosynthesis in two types of Kranz anatomy in genus Suaeda (family Chenopodiaceae)
Source Journal of Experimental Botany
Author Keywords C-3 plants C-4 plants Chenopodiaceae chloroplast ultrastructure immunolocalization in situ mRNA hybridization NAD-ME type photosynthetic enzymes Suaeda developing maize leaves dependent malic enzyme leaf development bundle-sheath zea-mays amaranth mitochondria cell-differentiation arundinella-hirta atriplex rosea expression
Abstract Genus Suaeda (family Chenopodiaceae, subfamily Suaedoideae) has two structural types of Kranz anatomy consisting of a single compound Kranz unit enclosing vascular tissue. One, represented by Suaeda taxifolia, has mesophyll (M) and bundle sheath (BS) cells distributed around the leaf periphery. The second, represented by Suaeda eltonica, has M and BS surrounding vascular bundles in the central plane. In both, structural and biochemical development of C-4 occurs basipetally, as observed by analysis of the maturation gradient on longitudinal leaf sections. This progression in development was also observed in mid-sections of young, intermediate, and mature leaves in both species, with three clear stages: (i) monomorphic chloroplasts in the two cell types in younger tissue with immunolocalization and in situ hybridization showing ribulose bisphosphate carboxylase oxygenase (Rubisco) preferentially localized in BS chloroplasts, and increasing in parallel with the establishment of Kranz anatomy; (ii) vacuolization and selective organelle positioning in BS cells, with occurrence of phosphoenolpyruvate carboxylase (PEPC) and immunolocalization showing that it is preferentially in M cells; (iii) establishment of chloroplast dimorphism and mitochondrial differentiation in mature tissue and full expression of C-4 biochemistry including pyruvate, Pi dikinase (PPDK) and NAD-malic enzyme (NAD-ME). Accumulation of rbcL mRNA preceded its peptide expression, occurring prior to organelle positioning and differentiation. During development there was sequential expression and increase in levels of Rubisco and PEPC followed by NAD-ME and PPDK, and an increase in the C-13/C-12 isotope composition of leaves to values characteristic of C-4 photosynthesis. The findings indicate that these two forms of NAD-ME type C-4 photosynthesis evolved in parallel within the subfamily with similar ontogenetic programmes.
Author Address [Chuong, Simon D. X.; Franceschi, Vincent R.; Edwards, Gerald E.] Washington State Univ, Sch Biol Sci, Pullman, WA USA. [Koteyeva, Nuria K.; Voznesenskaya, Elena V.] Russian Acad Sci, VL Komarov Bot Inst, Lab Anat & Morphol, St Petersburg 197376, Russia. [Berry, James O.] SUNY Buffalo, Dept Biol Sci, Buffalo, NY 14260 USA. Edwards, GE (reprint author), Washington State Univ, Sch Biol Sci, Pullman, WA USA. edwardsg@wsu.edu
ISSN 0022-0957
ISBN 0022-0957
29-Character Source Abbreviation J. Exp. Bot.
Publication Date May
Year Published 2011
Volume 62
Issue 9
Beginning Page 3197-3212
Digital Object Identifier (DOI) 10.1093/jxb/err021
Unique Article Identifier WOS:000291526500019
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