1021-4437/03/5001- $25.00 © 2003
Russian Journal of Plant Physiology, Vol. 50, No. 1, 2003, pp. 4–18. From Fiziologiya Rastenii, Vol. 50, No. 1, 2003, pp. 8–23.
Original English Text Copyright © 2003 by Artyusheva, Edwards, P’yankov.
In recent years, the quantitative structural analysis
has been considered a reliable approach to develop-
mental studies of the photosynthetic apparatus of both
plants at the cell and tissue levels [1–3].
A pronounced feature of C
plants is the cooperative
functioning of two distinct types of chlorenchyma tis-
sues, namely, M and BS cells, described in numerous
reviews [4, 5]. Different arrangements of these cell
types generally known as Kranz-anatomy has led to
special anatomical classiﬁcations of C
dicots [6, 7].
Four main types of leaf structure in C
dicots are distin-
guished. In one type, BS cells form a ring around each
vein, in turn, surrounded by the layer of more or less
radially arranged M cells. This type of Kranz-structure,
designated as atriplicoid, was named after the genus
(Chenopodiaceae) exhibiting this structural
pattern. Atriplicoid type is similar to that in some C
grasses and widespread among dicotyledonous C
plants [6–9]. The other three types of Kranz-anatomy,
designated as kochioid, salsoloid, and Kranz-suaedoid
tively) are mostly conﬁned to the family Chenopodi-
aceae [6, 7, 10]. Chenopodiaceae species with atripli-
coid and suaedoid structures studied up to now belong
to the NAD-ME subgroup of C
species, whereas those
with kochioid Kranz-anatomy have NADP-ME as the
principal decarboxylating enzyme. There are both
NADP- and NAD-ME species with the salsoloid type
of mesophyll structure [11–13].
ﬁxation in C
plants is partitioned between M
and BS cells, among various C
subtypes, and is corre-
lated with different structural and biochemical features
[6, 10, 14, 15]. Such structural/biochemical divergence
is a result of different developmental programs in the
cells of these two types. Most knowledge about the
development of the Kranz-syndrome came from the
studies of monocot leaves [10, 16–18]. Only a few dicot
Amaranthus hypochondriacus, Atriplex
) have been studied developmentally [19–23].
Both species are characterized by the atriplicoid type
Photosynthesizing Tissue Development in C
E. G. Artyusheva*, G. E. Edwards**, and V. I. P’yankov*
*Department of Plant Physiology, Faculty of Biology, Ural State University, pr. Lenina 51, Yekaterinburg, 620083 Russia;
fax: 7 (3432) 55-7401; e-mail: Elena.Artiowscheva@usu.ru
**School of Biological Sciences, Washington State University, Pullman, WA 99164-4236 USA
Received September 7, 2001
—The quantitative anatomy of developing cotyledons of NAD-malic enzyme species
and NADP-malic enzyme species
(Chenopodiaceae) was studied.
the group of species with foliar type of seedling development characterized by slowly growing cotyledons and
a rosette form at juvenility. The rosette is the consequence of fast leaf formation, which was correlated with a
low rate of leaf growth.
belongs to the group with the cotyledonous type of seedling development.
A high growth rate of cotyledons, slow leaf formation, and absence of the rosette characterize this type. Slow
leaf formation was correlated with a high rate of leaf growth. The Kranz–anatomy in cotyledons of
(atriplicoid type) and
(salsoloid type) determines the duration of cotyledon development pro-
ceeding for 15 days after seed germination. The rate of growth changes during the developmental period was
correlated with the type of seedling development. Cotyledons of a foliar species
exhibit 2 to 5
times slower growth changes in cotyledon area, width, thickness, volume of mesophyll and bundle sheath cells,
and number of chloroplasts per bundle sheath cell than the cotyledons of a cotyledonous species
During cotyledon development in both species, the number of chloroplasts per mesophyll cell remained
unchanged, and developmental changes in the bundle sheath occurred at higher rate than in mesophyll cells.
Thus, these two indices seem to be independent of the type of Kranz–anatomy. The presence of atriplicoid type
cotyledons in the species with salsoloid structure of true leaves might indicate a close genetic relationship
between these two patterns of Kranz-anatomy.
Key words: Salsola incanescens - S. paulsenii - development - cotyledons - Kranz-anatomy - evolution - Che-
—total area of cells per unit leaf area; BS—
bundle sheath; M—mesophyll; NAD-ME—NAD-malic enzyme;
NADP-ME—NADP-malic enzyme; PEPC—PEP carboxylase.
*This article was submitted by the authors in English.