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Butnik A.A.* & Toderich K.N.**
*Institute of Plants and Animal Genepool, Academy of Sciences of Uzbekistan Tashkent, e-mail: email@example.com
** International Center for Biosaline Agriculture for Central Asia and Caucasus ICBA-CAC) ,e-mail:firstname.lastname@example.org
Main trends in the evolution of structural traits of Chenopodiaceae Vent.
The evolution of the Chenopodiaceae Vent. being widespread mainly in the arid zone is closely
connected with the process of xerophylization (Popov, 1958; Korovin, 1961; Bochansev, 1969;
Kamelin, 1973). Studies on morphology and anatomy of vegetative organs and fruits conducted by
us for 81species, representatives of 28 genera were identified new aspect of evolutionary trends
within Chenopodiaceae family. Fruits of Chenopodiaceae during process of its evolution were
changed towards complexity, fusion and sclerification of fruit covering elements, in which
formation apart from pericap, perianth segments, bracteoles and in less extent bracts were
participated. Fruits with multi-layers fleshy or dry pericarp and without covering elements were
categorized as primitive features (genera Coripermum, Anthochlamys and Anabasis). Fruits with
perianth covering, probably, have been appeared early and proved to be much adaptive to different
stresses environmental conditions that are evidently confirmed due to their abundance in all
subfamilies. Bractlets-covering (any species of subfamily Chenopodioideae) and bractlet-perianth
shaped covering (any species of subfamily Salsoloideae) can be seen as two specialized branches of
evolution with limited distribution. In general, Chenopodiaceae is characterized by a high evolution
level of fruit structure: single-seeded, lysicarpous, thin, a simple structure of testa, an insignificant
presence or absence of perisperm - all these parameters testifies about phylogenetic integrity and
evolutionary advancement of this family. A special separation within Chenopodiaceae, however,
occupies the halophytic species from Salicornioideae subfamily (genera Salicornia, Halocnemum,
Halostachys, Kalidium) and the genus Suaeda. With small seeds, testa relatively thick, with thick-
walled cells, embryos leicophylous and more abundant perisperm they possess an entire set of
primitive features that confirms the ancient origin of these genera. The reduction of the volume of
endosperm and perisperm and functions of the embryo was expanded traits related with efficient
nutrients utilization and consequently, and germination was more short. Based on seedlings
development two relevant groups: the ancestral “Foliary”, which is characterized by: non-
specialized mesophyll of cotyledons and well-differentiated bud of the embryo at its early stages of
development, leaf traces in hypocotyl and rosettelike growth type in its juvenile phase (Kochia,
Ceratoides, Nanophyton, S. gemmascens). The second “Cotyledonary” group is characterized by a
high-specialized cotyledons, poorly differentiated buds, predomination of cotyledon trace in the
hypocotyl and non rossete-like form of growth in the juvenile phase (Salsola richteri, S. paletzkiana,
S. paulsenii, genus Haloxylon). Cotiledonary seedlings development may have occurred as results of
neotenic reorganization of species with already existing distinct Kranz-mesophyll of leaves. The
process, when traits of adult individuals undergone at the early ontogenesis stage, and as results of
such transformation become embryonal features A. Severtsov (1945) interpreted as secondary
Based on the anatomy of assimilative organs we have identified four distinguished structural groups
within investigated chenopods: picnophyllous, sclerophyllous, succulent and aphyllous species.
Species with sclerophylous leaves (Raphidophyton, Nanophyton, Sympegma) are dated to rocky and
gravelly substrates habitats. According to the opinion of M. Popov (1958) Central Asian deserts
prior to the Pleistocene have typical hammada characters and only later sand accumulation taken
place, therefore species of stony habitats might kept ancestral features in the structure of their
organs. Species with succulent leaves are predominated among Central Asian chenopods. This
phenomenon is stipulated by soil salinity of open large space of the desert named as "Dry Ocean"
and also by littoral origin of many species. In the structure of cotyledons and leaves of
Chenopodiaceae a progressive structural feature named Kranz-tissue were revealed and as it was
postulated by many authors its appearance might be associated with the transition to a more
advance types of photosynthesis, such as C4 and CAM. A. Mokronosov (1983) considers the type of
C4 photosynthesis as an aromorphosis or arochemous. However, we followed concept of A.
Severtsov, 1945; I. Schmalhausen, 1968 and A. Severtsov, 1987, where leading aromorphic
symptoms persist for all forms of telogenesis (idioadaptation) and determine the occurrence of major
structural categories: vessels (plantae vasculares), angiospermous (angiosperm plants), flower
(anthophyta plants). Kranz-tissue expands the range of photosynthesis and the threshold of plants
tolerance and can be viewed as an idioadaptation. Based on the specificity of this parameter we have
distinguished two group of types leaves-like structures for the Chenopodiaceae including the
cotyledons: non-Kranz (5 types) and Kranz-structure (10 types) (Kadereit et al., 2003 – 17 types).
Kranz types of cotyledons are considered more primitive as those in the leaves as far as these
structural types keep dorsoventral mesophyll peculiarities. The presence of high specialized (Salsoid
- type) structure in the cotyledons could be taken as palingenesis – inheritance of adult ancestors
(Severtsov, 1945). The discovering of the completely new structure named Borszowia and Bienertia
– types (Freitag, Stichler, 2000; Voznesenskaya et al., 2001) confirmed the primary of metabolism
in the process of evolution. Comparative analysis of ratio value between non-Kranz mesophyll types
both in cotyledons showed the predominance of non-Kranz types (68,8% –Chenopodioideae and
67,3% % for Salsoloideae subfamily) in the cotyledons of the 3 subfamilies indicating on their
general community and mesophytic origin and predominant Kranz-structure in leaves Salsoloideae –
89,1%, against – 35% in Chenopodioideae. The described groups have been completed the top of its
development by aphylly and the formation of the assimilative cortex of non-Kranz type as it was the
case for Chenopodioideae and Kranz-type in the Salsoloideae subfamilies. The presence of aphylly
in both non-Kranz and Kranz-types version testify about its considerable ancient ages and
convergence direction of development of different structural groups in the limit of single
Chenopodiaceae family. Aphylly is considered as phenomenon of progressive substitution of organs
(as postulated by Severtsov, 1945), as results of replacement of carrying out of photosynthetic
functions of some organs (leaves) by others (shoots with assimilative cortex), which occurred much
better adapted to the arid conditions.
Controversial opinion is admitted regarding reversion of Kranz to non-Kranz photosynthesis types
as has been described early by V. Pyankov et al. (1997), Fisher et al. (1997). Three main variants
were revealed by our studies in the difference ratio value of mesophyll of cotyledons (C) and leaves
(L): C – non-Kranz, L – non-Kranz (Chenopodioideae – 58,8%, Salicornieae – 100%, Salsoloideae
– 21,1%, all Chenopods – 27,1%), C – non-Kranz, L – Kranz (Chenopodioideae – 11,8%,
Salsoloideae – 53,2%, all Chenopod – 43,2%), C – Kranz, L – Kranz (Chenopodioideae – 29,4%,
Salsoloideae - 36,7%, all Chenopod – 29,7%). The variant with Kranz- in cotyledons and non-Kranz
in leaves, which was not yet detected, should be treated as an indirect proof of impossible loss of so
important adaptive evolutionary traits (Dollo’s rule).
Polycambial secondary thickening of the axial organs in Chenopodiaceae should be also treated as
the progressive phenomenon of evolution process. Policambial features in the Chenopodiaceae
family were developed gradually from conventional cambial ring at a certain ontogenesis stage
(representative of the genera Kochia and Camphoporma) up to lacking of development of the beam
and interfascicular cambium in the most advanced genera and biomorphs, what was confirmed by
A. Timonin, 2011. Regarding adaptability and polycambial features of assimilative organs, however,
various opinions exist: the localization of the necrotic process, the accumulation of bound water in
the sclerenchyma shells, to the inhabitation of ancestral species in litoralis zone and toxic salts
impact on the meristem (cambium) differentiation. Inhibition of cambium activity, called for the
emergence of new, more stable structures, in the form of meristematic cambial zone and succession
of cambium. The main direction of adaptive evolution is manifested is the reduction of size organs,
tissues and cells, which is manifested in the reduction of plants habitat, microphylly, one-beam
structure of the leaf trace, reduction rows numbers of palisade parenchyma to one of the most
specialized leaves, the absence of interfascicular cambium with sclerenchyma-beam type,
polycambial and reducing the period of operation of the first and the extension of the cambium in
the axial organs, parvicellular of all tissues (tab l.).
Table 1.Trends of structural and functional changes in the Chenopodiaceae family
Full elimination of storage function;
Seed without endosperm
Partial elimination of protective
function and dissemination, reduction
Thin testa and pericarp
Extension of protective function and
fruit dissemination, structure
Presence of fruit covering with
perianth and bracteoles
Extension of storage function and
assimilation, complexity of structure
Specialized structure of
Partial or complete elimination and
Intensification of assimilative
function, reduction of numbers of
layers, complexity at sub-cellular
Appearance of kranz-structure
(C4 and CAM types of
Extension of the assimilative
function, complexity of structures
Assimilative cortex of stem
Elimination of functions and
reduction of initial/ primary
cambium. Intensification and
complexity of secondary thickenings
Increasing of aridity of climate might be treated as the main factor in the species survival and
adaptation of Chenopodiaceae. Acceleration of the rate of initiation and development of organs and
tissues are observed at all stages of plant ontogenesis for majority of Chenopods. Reduction of
function of pericarp and spermoderma is accompanied by extension of functions of the perianth and
bracteoles. Reduction of endosperm and perisperm was accompanied by development of fully
prepared to germination (accelerated) embryo. Replacement of reduced organs and tissues by others
(substitution of functions), whose functions are expanded, leads to the formation of cortical
assimilating shoots so called cambryonic meristematic zone in the axial organs.
The above-described changes in fruit structures provide the high specialization of organs and
promote successful reproduction and seed dispersion of species under dryland stressful conditions.
Altogether allowed to the majority species of Chenopodiaceae to survive and widespread under
harsh desert environments that leaded to decreasing in the competitive ability of species. Diversity
of fruits structure, assimilative organs, types of polycambial secondary thickening (structural
inhomogeneities, cladogenesis as has also been suggested by A. Takhtajan, 1966) indicates to the
progressive long-term phylogenetic pathways of Chenopods.
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2. Fisher, D.D. & Schenk, H.Y. & Jhorsch, Y.A. & Ferren, W.R. 1997: Leaf anatomy and
subdeneric affiliations of C3 and C4 species of Suaeda (Chenopodiaceae) in North America. –
American J. of Botany. – 84 (9): 1198-1210.
3. Fretag, Н. & Stichler, W. 2000: A remarkable new leaf type with unusual photosynthetic tissue in
a Central Asiatic genus of Chenopodiaceae. – Plant Biol. New York. – 2: 154-160.
4. Kadereit, G. & Borsch, T. Weising, K. & Freitag H. 2003: Phylogeny of Amaranthaceae and
Chenopodiaceae and the evolution of C4 photosynthesis. – J. Plant Sci. 164 (6): 959-986.
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Press. (in Russian)
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Sciences Press. (in Russian)
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carbon methabolism. – In: Carbon photosynthetic metabolism. 7-23. Sverdlovsk: Ural State
University Press. (in Russian)
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9. Pyankov, V.J. & Vosnesenskaya, E.V. & Kondratschik, A. & Black C. 1997: A comparative
anatomical and biochemical analysis in Salsola (Chenopodiaceae) species with and without a Kranz
type leaf anatomy: a possible reversion of C4 to C3 photosynthesis. – Amer. J. Bot. 84(5): 597-606.
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15. Voznesenskaya, E.V. & Franceschi, V.R. & Kiirats, O. & Freitag, H. & Edwards, G.E. 2001:
Kranz anatomy is not essential for terrestrial C4 plant photosynthesis. – Nature. 414(29): 543-546.