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Main trends in the evolution of structural traits of Chenopodiaceae Vent



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Butnik A.A.* & Toderich K.N.**
*Institute of Plants and Animal Genepool, Academy of Sciences of Uzbekistan Tashkent, e-mail:
** International Center for Biosaline Agriculture for Central Asia and Caucasus ICBA-CAC) ,
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
Organs, structure
Structural changes
Full elimination of storage function;
Seed without endosperm
Pericarp, testa
Partial elimination of protective
function and dissemination, reduction
Thin testa and pericarp
Bractlets, perianth
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
assimilation, reduction
Microphylly, aphylly
Intensification of assimilative
function, reduction of numbers of
layers, complexity at sub-cellular
Appearance of kranz-structure
(C4 and CAM types of
Primary cortex
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.
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carbon methabolism. In: Carbon photosynthetic metabolism. 7-23. Sverdlovsk: Ural State
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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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A phylogenetic analysis of Chenopodiaceae and Amaranthaceae was carried out using sequence variation of the chloroplast gene rbcL. Our sampling included 108 species of these two families along with 29 species of Caryophyllales serving as outgroups. Phylogeny inferences with maximum parsimony and maximum like-lihood indicate that the two families form a well-supported monophyletic clade that is sister to Achatocarpaceae. Despite extensive sampling, we found that the relationship between Chenopodiaceae and Amaranthaceae remains unclear as a result of short and weakly supported basal branches. The clearly monophyletic Polyc-nemoideae (traditionally considered a subfamily of Chenopodiaceae) appear as sister to Amaranthaceae sensu stricto. Within Amaranthaceae, most major lineages inferred except Gomphrenoideae and Celosieae do not correspond to recognized subfamilies and tribes. Bosea and Charpentiera branch first in the Amaranthaceae. Within Chenopodiaceae, the genera of Betoideae occur in basal and largely unresolved positions. The remaining Chenopodiaceae are divided into three major clades of unclear relationship: Chenopodioideae (Atripliceae s.str., Chenopodieae I-III); Corispermoideae (Corispermeae); and Salicornioideae (Haplopeplideae, Salicor-nieae), Suaedoideae (Suaedeae, Bienertieae), and Salsoloideae (Camphorosmeae, Sclerolaeneae, Salsoleae I-II). The rbcL tree is discussed also with regard to historical classifications and morphological support for the major clades. The molecular results are used to elucidate the evolution of C 4 photosynthesis in the two families. C 4 photosynthesis has evolved independently at least three times in Amaranthaceae and at least 10 times in Chenopodiaceae. A survey of C 4 leaf anatomy revealed 17 different leaf types that in most cases mark an independent origin of C 4 photosynthesis. The application of a molecular clock indicates an age of C 4 pho-tosynthesis of 11.5–7.9 Ma in Atriplex (Chenopodioideae) and 21.6–14.5 Ma in subfamily Salsoloideae.
Full-text available
An important adaptation to CO2-limited photosynthesis in cyanobacteria, algae and some plants was development of CO2-concentrating mechanisms (CCM). Evolution of a CCM occurred many times in flowering plants, beginning at least 15-20 million years ago, in response to atmospheric CO2 reduction, climate change, geological trends, and evolutionary diversification of species. In plants, this is achieved through a biochemical inorganic carbon pump called C4 photosynthesis, discovered 35 years ago. C4 photosynthesis is advantageous when limitations on carbon acquisition are imposed by high temperature, drought and saline conditions. It has been thought that a specialized leaf anatomy, composed of two, distinctive photosynthetic cell types (Kranz anatomy), is required for C4 photosynthesis. We provide evidence that C4 photosynthesis can function within a single photosynthetic cell in terrestrial plants. Borszczowia aralocaspica (Chenopodiaceae) has the photosynthetic features of C4 plants, yet lacks Kranz anatomy. This species accomplishes C4 photosynthesis through spatial compartmentation of photosynthetic enzymes, and by separation of two types of chloroplasts and other organelles in distinct positions within the chlorenchyma cell cytoplasm.
: From the hygrohalophyte Borszczowia aralocaspica Bunge (Chenopodiaceae), a new leaf type with 1-layered chlorenchyma is described as “borszczovoid” and compared with other leaf types in subfamily Salsoloideae. The chlorenchyma is suspected to represent a unique C4 type. Evidence is cited from anatomical studies and documented by micrographs and Carbon isotope determinations (ä13C values). The 1-layered photosynthetic tissue combines all essential anatomical characters of a 2-layered chlorenchyma of regular C4 plants and is in intimate contact with concentrically arranged peripheral bundles. The ä13C values are − 13.03 ‰ from young stems and − 13.78 ‰ from leaves. The results are discussed in the anatomical, physiological and taxonomic framework. In addition, from distantly-related Suaeda species of section Conosperma the conospermoid leaf type is re-described. It is characterized by typical palisade and Kranz layers and differs from the C4 suaedoid type by an external water-storaging hypodermis and an arrangement of Kranz cells reminiscent of the atriplicoid type from subfamily Chenopodioideae. From eight other species of Chenopodiaceae ä13C values are given for the first time.
The process of organic evolution requires consideration of factors facilitating the transformation of the organisms as well as factors responsible for preserving the modifications. The author stresses the stabilizing role of natural selection. The four sections deal with: (1) the individual variability, especially the phenomena of mutation; (2) the dynamics of the variability of populations; (3) individual adaptability and regulatory mechanisms of morphogenesis; and (4) factors determining the rate of evolution. As pointed out in the preface, the treatment exemplifies the convergence and unification of contributions to the evolutionary thought coming from comparative embryology and anatomy, genetics, paleontology, and systematics. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
The halophytic genus Suaeda (Chenopodiaceae) includes species with the C3 and C4 photosynthetic pathways. North American species of this genus were investigated to determine whether C3 and C4 leaf anatomy are consistent within the two sections of Suaeda, Chenopodina and Limbogermen, present on this continent. All species from section Chenopodina were found to possess C3 anatomy, whereas all species from section Limbogermen were found to be C4 species. Characteristics of leaf anatomy and chloroplast ultrastructure are similar to those reported from C3 and C4 species, respectively, from the Eastern Hemisphere. All species from section Limbogermen have the suaedoid type of leaf anatomy, characterized by differentiation of the mesophyll into palisade parenchyma and a chlorenchymatous sheath surrounding central water-storage tissue, as well as leaf carbon isotope ratios (_13C) of above -20. All species from section Chenopodina have austrobassioid leaf anatomy without a chlorenchymatous sheath and _13C values of below -20. According to our literature review, the photosynthetic pathway has now been reported for about half (44) of the Suaeda species worldwide. The C3 and C4 photosynthetic syndromes are with few exceptions distributed along sectional or subsectional lines. These findings throw new light on the infrageneric taxonomy of this genus.
Genus Salsola L. composition, history of development and dissemination. -Avtoreferat of Dr of biological sciences
  • V P Bochantsev
Bochantsev, V.P. 1969: Genus Salsola L. composition, history of development and dissemination. -Avtoreferat of Dr of biological sciences. Leningrad: 45 (in Russian)
Floristic analysis of native Flora of Middle Asia 356 Leningrad
  • R V Kamelin
Kamelin, R.V. 1973: Floristic analysis of native Flora of Middle Asia 356 Leningrad: Nauka Press. (in Russian)
Genetics and phenotypic factors in the determination of photosynthetic carbon methabolism
  • A T Mokronosov
Mokronosov, A.T. 1983: Genetics and phenotypic factors in the determination of photosynthetic carbon methabolism. -In: Carbon photosynthetic metabolism. 7-23. Sverdlovsk: Ural State University Press. (in Russian)
The basic features of the history of development of Central Asian Flora
  • M G Popov
Popov, M.G. 1958: The basic features of the history of development of Central Asian Flora. 182-241. Ashgabat: Selected Press.
A comparative anatomical and biochemical analysis in Salsola (Chenopodiaceae) species with and without a Kranz type leaf anatomy: a possible reversion of C 4 to C 3 photosynthesis. -Amer
  • V J Pyankov
  • E V Vosnesenskaya
  • A Kondratschik
  • C Black
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 C 4 to C 3 photosynthesis. -Amer. J. Bot. 84(5): 597-606.